The role of small pelagic fish in the ecosystem

25 January 2007

Lynne Shannon, Marta Coll, Sergio Neira, Philippe Cury and Jean-Paul Roux

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Abstract

Small pelagic fish are termed “wasp-waist” species as they dominate mid-trophic

levels, comprise relatively few species but attain large abundances that can vary

drastically in size. They have been shown to exert top-down control on their prey

species and bottom-up control on their predators and, in this way, appear to induce

unsuspected ecosystem dynamics. This chapter explores these effects and associated

dynamics, not only to reveal the importance of small pelagic fish in structuring marine

ecosystems but also to examine the consistency of the role of small pelagic fish across

various upwelling systems. The Northern and Southern Benguela, Southern

Humboldt, South Catalan Sea and North and Central Adriatic Sea ecosystems are

compared in terms of the importance and role of small pelagic fish using information

gained from landings: i) Trophic level of the catch, ii) the Fishing-in-Balance (FiB)

index and iii) the ratio of pelagic:demersal fish. Indicators derived from trophic

models of these ecosystems are selected to assist in defining the effects of small

pelagic fisheries, and include: i) Catch/Biomass ratios for small pelagic fish, ii)

Exploitation rate E=F/Z, where F is fishing mortality and Z is total mortality (natural

and fishing mortality combined) for the main commercial fish species in each system,

iii) Sum of all flows to detritus. Models of the Southern Benguela, Southern

Humboldt and South Catalan Sea are used to perform two simulations: 1) Closure of

fishery on small pelagic fish and 2) Collapse of small pelagic fish, to further explore

the roles of small pelagic fish in the dynamics of these ecosystems.

Tracking pelagic:demersal fish catch and biomass ratios over time is a means of

detecting collapse in the small pelagic fish stocks, and comparing these ratios across

ecosystems highlights the greater importance of small pelagic fish in the Humboldt

compared to other ecosystems. The trophic level of the catch severely declined in the

Northern Benguela and Southern Humboldt ecosystems, reflecting collapses in small

pelagic and/or other fisheries in these regions. In the Mediterranean Sea, fluctuations

in TL of the catch, in conjunction with the FiB index, reflects the collapse of the small

pelagic fish and disruption of the ecosystem. Small pelagic fishing mortalities are

smallest in the Adriatic (maximum F = 0.2 y-1), and the Southern Benguela

(maximum F= 0.3 y-1 for anchovy and sardine in the 1980s), whereas fishing

mortality rates exceeding 0.3 y-1 and 0.5 y-1 are estimated for anchovy in the South

Catalan and Northern Benguela, respectively. Estimated fishing mortalities are greater

than 0.6 y-1 for sardine in the South Catalan, and F of anchovy and common sardine is

estimated to have exceeded 0.7 y-1 in the Southern Humboldt ecosystem in 1992. Thus

it appears that smaller fishing mortalities can be supported in the systems exhibiting

greater biodiversity (shallow bank and upwelling area of the Southern Benguela;

diverse environmental conditions responsible for diverse habitats in the Adriatic).

Models analyzed in this study show how a decrease in small pelagic fish abundance

will have detrimental effects on both higher and lower trophic levels of the food web,

causing a decrease in predators and the proliferation of other species that are preys or

competitors of small pelagic fish, but which do not constitute an alternative pathway

for the flow of primary productivity to higher trophic levels. Trophic model

simulations showed consistently that gelatinous zooplankton increase when small

pelagic fish stocks decline and conversely, there is a decrease in jellyfish abundance

when closure of the pelagic fisheries is simulated. Model simulations of small pelagic

fishery collapses in the southern Benguela, Southern Humboldt and South Catalan Sea

all emphasize the dependency of avian and to a lesser extent more opportunistic

mammalian and fish predators, on healthy stocks of small pelagic fish. Moreover,

collapses of small pelagic fish generally disrupt energy flows, which could result in an

increase in flows to detritus, demersal processes within the system becoming more

important, stronger overall mixed trophic interactions of the pelagic component on the

demersal component in more recent periods (usually when fishing has increased), and

often reduced summed impacts of the demersal compartment on the degraded pelagic

food web. Examination of summed mixed trophic impacts of detritus on both the

pelagic and demersal food webs further supported the hypothesis that detritus

becomes increasingly more important as ecosystems are fished and/or degraded.

However, in the Northern Benguela, the near-total collapse of the pelagic ecosystem

has weakened detritus-pelagic food web linkages, whereas detritus-demersal linkages

have strengthened.

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Chapter contents:

1. INTRODUCTION: ROLE OF SMALL PELAGIC FISH IN MARINE ECOSYSTEMS

1.1. Small pelagic fish as the wasp-waist of ecosystems

1.2. Outline of the chapter

2. THE ECOSYSTEMS EXAMINED

2. 1. Benguela upwelling region

2.2. Humboldt upwelling system

2.3. Mediterranean ecosystems of the Catalan and Adriatic seas

3. METHODS

3.1. Catch and abundance data series

3.2. “Static” (“Snapshot”) models

3.3. Models fitted to time series data

3.4. Simulations

4. MODEL RESULTS

4.1 Catch ratios and abundances

4.2 Fishing mortality, predation and exploitation rates

4.3 Gelatinous zooplankton and proliferation of other species

4.4. Effects of small pelagic fish on top predators

4.5. Flows to detritus

4.6 Coupling demersal-pelagic compartments

5. DISCUSSION

5.1. Trophic flow controls, fishing and the environment

5.2. Generic effects of fishing on small pelagic fish

5.3. Proliferation of species

5.4. Effects of small pelagic fish on top predators

5.5. Increased pelagic-benthic coupling and flow to detritus

5.6. Enhancing catches of commercially valuable predatory fish by reducing small

pelagic fish catches?

6. SMALL PELAGIC FISH AS INDICATORS OF ECOSYSTEM COLLAPSE?

6.1. Ecosystem indicators

6.2. Recommended exploitation rates

6.3. Disruption of trophic pathways

1. INTRODUCTION: ROLE OF SMALL PELAGIC FISH UP AND DOWN

THE FOOD WEB

1.1 Small pelagic fish as the wasp-waist of ecosystems

Small pelagic fish, dominating mid-trophic levels and being comprised of relatively

few species but attaining large abundances that can vary drastically in size, have been

named “wasp-waist” species (Rice, 1995; Bakun 1996, Fig. 1). Small pelagic fish

have been shown to exert top-down control on their prey species and bottom-up

control on their predators, which has been described as a ‘wasp-waist’ control (Cury

et al., 2000). The ‘‘boom-bust’’ dynamics of pelagic fish and populations that interact

trophically with them suggests a ‘‘predator pit’’ type of dynamics according to Bakun

(2006). This special configuration in certain marine food webs and the role and

dynamics of pelagic fish appears to induce unsuspected ecosystem dynamics. These

effects and associated dynamics need to be explored in detail, not only to reveal the

importance of small pelagic fish in structuring marine ecosystems but also to examine

the consistency of their role in various upwelling systems.

Regime shifts or switches in pelagic fish species abundance may be initiated or

sustained by changes in zooplankton availability (Schwartzlose et al., 1999). On the

other hand, changes in abundance of small pelagic fish may have top-down effects on

the abundance and community structure of zooplankton prey (Schwartzlose et al.,

1999). Between the 1950s and the 1990s, the proportion of small cyclopoid copepods

off the west coast of South Africa increased, compared to a decrease in the relative

abundance of large calanoid copepods, and the biomass of copepods increased tenfold

whereas total copepod abundance increased 100-fold (Verheye and Richardson, 1998;

Verheye et al., 1998). Both bottom-up and top-down effects of small pelagic fish on

zooplankton in this region have been proposed (Verheye et al., 1998), although Cury

et al. (2000) showed that the general rule in upwelling systems, including the

Benguela, is that small pelagic fish exert top-down control on their zooplankton prey.

Small pelagic fish have been shown to exert important controls over their predators

too. Seabirds, in particular, have been found to respond strongly to changes in pelagic

fish abundances. Seabird guano harvests off South Africa and Peru reflected changes

in pelagic fish abundance (Crawford and Jahncke, 1999) and several population

parameters measured for African penguins, Cape cormorants and swift terns off South

Africa have been related to stock fluctuations of anchovy and sardine (Best et al.,

1997). These have been verified through changes in seabird diet compositions in

response to changes in pelagic fish abundance (e.g. that of the Cape gannet Morus

capensis, Crawford and Dyer, 1995). Similarly, off Namibia, as sardine abundance

decreased, pelagic goby replaced sardine as the important prey item in the diets of

Cape Gannets, Cape Cormorants Phalacrocorax capensis and African Penguins

Spheniscus demersus (Crawford et al., 1985). Off Namibia, sardine were an important

prey of the Cape fur seal, Arctocephalus pusillus pusillus in earlier years whereas

goby, supplemented by myctophids in the southern part of the Northern Benguela, and

horse mackerel in the central and northern parts of the Northern Benguela, became the

main prey of seals in later years (Mecenero and Roux, 2002; J.-P. Roux, NMFR,

Namibia, pers. comm.). The dominant large pelagic fish predator in the southern

Benguela, namely snoek (Thyrsites atun), preys non-selectively on pelagic fish (M.

Griffiths, Marine and Coastal Management, pers. obs.) and diet studies have shown

that snoek feed on anchovy and sardine in accordance with their relative abundances

in the ocean (Crawford et al., unpublished ms). In the Mediterranean Sea, small

pelagic fish have been shown to be important prey for demersal fish, marine mammals

and seabirds (Bozzano et al., 1997; Ríos, 2000; Arcos, 2001; Blanco et al., 2001;

Stergiou and Karpouzi, 2002).

Empirical studies reveal patterns of interaction with small pelagic fish (e.g. with top

predators such as birds and seals or with zooplankton prey) that have been obtained at

different spatial and temporal resolutions. Thus the time series used to study the effect

of changes in biomass of small pelagic fish on seals or birds are estimated at the level

of the ecosystem and on an annual basis, while the time series of plankton have

usually been collected locally at a fine temporal scale. These differences in the

resolution can substantially bias the way we analyze control versus what might be

regarded as a local depletion with no effect on the overall population, and such

interactions need to be explored in a broader perspective.

Piscivorous fish (such as snoek and hake) support fisheries of high commercial value

and thus the linkages between small pelagic fisheries and these fisheries can be very

important. It is often debated as to whether there would be value in fishing more

lightly on small pelagic fish in order to leave more forage fish for predatory fish,

thereby potentially benefiting fisheries on these predatory fish. This is still an open

question, to which answers may be provided through model simulations or the

implementation of carefully designed experimental fishing scenarios. It is the former

option that is very briefly explored in this study, although more rigorous and detailed

modelling is recommended.

As we are now fishing down marine food webs (Pauly and Palomares, 2005), fishing

pressure is increasing on organisms at lower trophic levels, such as small pelagic fish

(FAO, 2005). Therefore, their increased exploitation is expected to have a wide

impact on the pelagic food web and might provoke the dysfunction of the ecosystem

and the further depletion of populations of dependent predators at higher trophic

levels. This can cause, as has already been observed when top predators are

overfished (Springer et al., 2004; Frank et al., 2005), large trophic cascades and

proliferation of species located at lower trophic levels or having shorter life spans

(Daskalov, 2002; Cury et al., 2005b). All these changes on exploited marine

ecosystems point to the existence of a sequence of flow controls as ecosystems are

fished down or as community turn-over rates increase, which is of great relevance in

terms of recovery of intense exploited ecosystems (Fig. 2). There is thus a need to

characterize what changes are occurring where and why, as well as which ecosystem

elements favour these changes in relation to fishing pressure, control mechanisms and

environmental variability. An essential element is to analyze to what extent observed

ecosystem changes due to the collapse of the pelagic system and changes in flow

control are reversible.

1.2. Outline of the chapter

In this chapter, we focus on the following ecosystems in which small pelagic fish play

important roles, both commercially and within the food web: the Benguela (South

Africa and Namibia), the Southern Humboldt (Chile), the Mediterranean Sea (South

Catalan and the North and Central Adriatic), and to a lesser extent also the Northern

Humboldt (Peruvian) system, representing a gradient of exploited ecosystems.

In a previous study, comparative trophic models of upwelling ecosystems have been

considered, and taking into account the exploitation history of these ecosystems,

selected indicators were analysed to test an initial hypothesis that an ecological model

representing the South Catalan Sea (Northwestern Mediterranean) would be ranked

within the high impacted areas of Namibia and Peru, which were differentiated in

terms of ecosystem impact from the moderately impacted regions of Chile and South

Africa (Moloney et al., 2005; Coll et al., 2006a).

This chapter aims to define, in a quantifiable respect, the disruption of food webs

(Fig. 2) as a result of small pelagic fish collapse (by comparing with healthy situations

where small pelagic fish are considered to be sustainably exploited), and to show how

small pelagic fish can be used as indicators or warning signs of a future ecosystem

collapse or change.

2. THE ECOSYSTEMS EXAMINED

2.1. Benguela upwelling region

The Benguela upwelling region is subdivided by the permanent Lűderitz upwelling

cell around 26oS into two systems, namely the Southern Benguela ecosystem off

South Africa and the Northern Benguela ecosystem off Namibia. The Northern

Benguela ecosystem extends from the Angola-Benguela front located between 14oS

and 16oS (Meeuwis and Lutjeharms, 1990) southwards to Lűderitz. In addition to an

upwelling region along the south-western coast, the Southern Benguela ecosystem is

uniquely characterised by a shallow bank region, the Agulhas Bank in the south. This

is the reason for the more abundant and ecologically important demersal and benthic

biota in the Southern Benguela ecosystem compared to “traditional” (and non-

collapsed) upwelling systems (Shannon and Jarre-Teichmann, 1999a, b).

Although fisheries in the Northern and Southern Benguela ecosystems target similar

demersal (Cape hake, Merluccius capensis and M. paradoxus) and pelagic fish

species (sardine, Sardinops sagax, anchovy, Engraulis encrasicolus, horse mackerel,

Trachurus t. capensis), they have experienced different exploitation histories and

environmental perturbations, and contrast in their species compositions, community

structures and abundance trajectories.

Total catches in the Southern Benguela ecosystem have fluctuated around 0.5 million

tonnes since the early 1960s. Since the 1950s and even before then, hake off South

Africa have been targeted by bottom trawlers. Catches of hake increased slowly from

about 50 000 tonnes to about 140 000 tonnes between 1950 and 1977, when a 200-

mile Fishing Zone was proclaimed by South Africa (Payne, 1989), and have remained

relatively stable since. Most of the catch was comprised of sardine from 1950 until

1965, thereafter the fishing industry used nets of smaller mesh size to target anchovy,

which dominated the catches until the mid 1990s, and in the early 2000s, significant

quantities of both small pelagic species have been caught. The sustainability of

catches off South Africa is largely attributable to relatively conservative management

measures, for example pelagic fish catches have been maintained well below 25% of

estimated annual biomass since the early 1990s (Cury et al., 2005a), although the

initialization of the unusually high abundance of both anchovy and sardine off South

Africa in the early 2000s has been attributed to a favourable sequence of short-lived

environmental events (Roy et al., 2001).

Sardine, anchovy and hake off Namibia have been sequentially exploited and

depleted, largely because effective management measures could not be implemented

until Namibia’s independence and proclamation of a 200-mile EEZ in 1990.

Subsequently, there has been a modest recovery of hake catches but sardine have

remained at very low levels. Catches have been dominated by horse mackerel since

the 1970s although there has been a slight decline since the late 1980s. There has been

a steady decline in total catches, which peaked in 1968 at more than 2 million tonnes

and decreased to around 0.5 million tonnes in the late 1990s.

Sardine were abundant off Namibia in the early 1960s, but year-classes were poor

from 1965, whereas catches were still large from 1967–1969, and sardine biomass

thus declined (Crawford et al., unpublished ms). Unlike off South Africa, anchovy

alone did not replace sardine, rather a suite of planktivorous fish, including horse

mackerel, bearded goby Sufflogobius bibarbatus and to a lesser degree anchovy, filled

the previously occupied niche from the late 1970s and early 1980s (Boyer and

Hampton, 2001). Between 1986 and 1991, sardine and hake biomass increased

(Crawford et al., unpublished ms). However, two environmental anomalies occurred

in the Northern Benguela between 1993 and 1995 (a low oxygen event in 1993/4 and

an intrusion of warm water-Benguela Niño-in 1995), and were linked to distributional

shifts in several fish species, poor sardine recruitment, declines to low biomass levels

of most commercial species and reduced catch rates of hake (Boyer et al., 2001),

which migrated offshore between 1993 and 1995 (Hamukuaya et al., 1998), monkfish

(Maartens, 1999) and horse mackerel (Boyer and Hampton, 2001). Concomitant

declines were also observed in top predators such as seals, which, due to starvation,

declined by a third in the mid-1990s (Roux, 1998) and Bank cormorants,

Phalacrocorax neglectus (Crawford et al., 1999).

2.2. Humboldt upwelling system

The upwelling system off central Chile is located in the southern section of the

Humboldt Current System, which is one of the four major eastern boundary

ecosystems of the world. This system supports one of the highest levels of primary

productivity recorded for the open Ocean (1.7 gC/m-2 year-1; Daneri et al., 2000) and

globally significant landings (>4.5 million tons in 1995). Despite this high biological

productivity, the state of exploited stocks is far from healthy (Arancibia and Neira,

2003). In fact, the main target species have been fully exploited or even overexploited

for many years, leading to a series of recent stock collapses, for example of horse

mackerel (1998), red squat lobster and yellow squat lobster (1999), and Chilean hake

(2004).

The Southern Humboldt system off central Chile, as considered in this chapter,

extends from 33ºS to 39ºS and from the coast line up to 30 nautical miles offshore,

covering a total area of approximately 50 000 km2. This geographical unit

corresponds to the “Mediterranean District” and is ecologically independent from the

“Peruvian Province” and the “Austral District” located northward and southward,

respectively (Camus, 2001). The main oceanographic and biogeographic patterns that

characterize the Southern Humboldt are: a rather narrow continental shelf (<30

nautical miles), strongly seasonal upwelling (September to March) and high levels of

primary productivity (Strub et al., 1998; Daneri et al., 2000; Escribano et al., 2004).

Oceanographically, four main water masses are present, which leads to a very diverse

marine environment along the central Chilean coast: Subtropical Surface Water

(STSW), Subantarctic Water (SAW), Antarctic Intermediate Water (AAIW), and

Equatorial Subsurface Water (ESSW) (for a review of the physical and chemical

characteristics of each water mass see Strub et al. 1998). Wind driven coastal

upwelling brings the ESSW to the surface in the coastal zone, causing a persistent and

characteristic shallow oxygen minimum zone (> 0.5 ml O2.l-1). Based on the

correlation between the low frequency coastal modes and the Pacific and Atlantic sea

surface temperature (SST), Montecinos et al. (2003) suggest that the coastal SST

seems to comprise two main large-scale climate processes affecting the Southern

Humboldt. At the inter-annual scale the main source of variability is the El Niño

Southern Oscillation cycle. At the long-term scale, an inter-decadal oscillation occurs

at a basin-wide, and maybe even global, scale.

In terms of the main biological components, the Southern Humboldt sustains a diverse

and productive food web. The phytoplankton group is dominated by large diatoms for

most of the year (Avaria and Muñoz, 1982), while the zooplankton is dominated by

herbivorous copepods and euphausiids. Jellyfish (Hydrozoa) also constitute an

important group in the plankton domain (Palma and Rosales, 1995).

Macrocrustaceans are significant benthic components and some species such as red

squat lobster (Pleuroncodes monodon), yellow squat lobster (Cervimunida johni) and

pink shrimp (Heterocarpus reedi) support important fisheries. The fish community is

dominated by pelagic species. Small pelagic fishes such anchovy (E. ringens) and the

endemic common sardine (S. bentincki) are present at high biomass levels in the

Southern Humboldt and dominate landings. These species feed primarily on

phytoplankton and secondarily on zooplankton (Arrizaga et al., 1993). The horse

mackerel (Trachurus symmetricus) is a major fishery resource in the study area. This

highly migratory species performs large-scale migrations in the Pacific Ocean. Off

Chile, horse mackerel feed mainly on euphausiids (Miranda et al., 1998). The

demersal fish community is dominated by the Chilean hake (Merluccius gayi) both in

biomass and landings. Hake inhabits mid-depth waters (200-400 m), feeds on

euphausiids, galatheid crustaceans and small pelagic fish (Meléndez 1983; Arancibia

1989; Cubillos et al., 2003) and is highly cannibalistic (Arancibia et al., 1998).

The Southern Humboldt ecosystem also represents an independent management unit,

comprising the main fishing ground for the Chilean purse seine and trawling fleets,

both industrial and small scale operations and accounting for approximately 75% of

the total landings in Chile (Neira and Arancibia, 2004; Neira et al., 2004). The

industrial fishery, based on fish and crustacean species, started in the 1940s, when

demersal trawlers targeted Chilean hake (Merluccius gayi). However, landings of this

fleet were significant only from mid 1950s onwards. By the early 1960s, an industrial

pelagic fishery came into operation, targeting small pelagic fishes, mainly common

sardine (Strangomera bentincki) and anchovy (Engraulis ringens). At the same time,

an industrial fleet operated on a medium-sized pelagic fish, namely horse mackerel

(Trachurus symmetricus), landings only becoming globally significant from 1975

onwards.

When expanding the trophic analysis to the whole food web, Arancibia and Neira

(2005) found a significant decrease in the mean trophic level of the catch, which

indicates a likely change in community structure induced by fishing. The current

status and basic ecology of top predators such marine birds, sea lions and cetaceans

are poorly known, but it is likely that their abundances are very low compared to the

period at the start of the industrial fisheries in Central Chile (1940s).

The Northern Humboldt system (Peruvian system) is world famous because it

supports one of the most productive fisheries of the world (Ryther, 1969).

Specifically, during the 1960s and 1970s, it supported the largest single-species

fishery in the world, targeting anchovy (Engraulis ringens). The Peruvian system is

dominated by the dynamics of anchovy and subject to frequent direct environmental

perturbations of the El Niño Southern Oscillation (ENSO). The long-term dynamics

of the Humboldt Current ecosystem off Peru are controlled by shifts between

alternating anchovy (cool) and sardine (warm) regimes that restructure the entire

ecosystem from phytoplankton to top predators (Alheit and Niquen, 2004).

The Peruvian food web, considered to be the northern-central subsystem of the

Humboldt that extends from 4º-14ºS and west up top 60 nautical miles, and covering

approximately 82 000 km2, has previously been modelled (Jarre-Teichmann et al.,

1998). That model represents the period 1973-1981, corresponding to the period

following the collapse of the huge anchoveta fishery of the late 1960s, while sardine

biomass was increasing, and did not span any major El Niño events. The model

considers the main distribution area of small pelagic fish such as anchovy and sardine,

i.e., over the Peruvian continental shelf. This geographic delimitation means that only

part of the biomass of horse mackerel, mackerel, and mesopelagic fish are included,

since these species are distributed farther offshore (Jarre-Teichmann, 1998).

One of the most remarkable features of the Peruvian system is the rise and collapse of

the Peruvian anchovy fishery from 700 thousand tonnes in 1958 to a maximum of 12

million tonnes in 1973 (Walsh, 1981). The evolution in the Peruvian anchovy fishery

was accompanied by marked changes in fluxes in the carbon budget of the food web

(Walsh, 1981). Similar results can be found in Jarre-Teichmann (1998). The

significant drop in anchovy biomass led to a decrease in grazing pressure, allowing

plankton biomass to increase. These changes were accompanied by increased stocks

of sardine and hake, increased carbon loading and sulphate reduction at the

downstream sea bed, and a decline in oxygen and nitrate content of the water column

(Walsh, 1981). Trophic flows in the system decreased in one order of magnitude

between the periods 1964-1971 (anchovy dominated) and 1973-1981 (before the

anchovy collapse), and the flow to detritus from the phytoplankton compartment

increased of two orders of magnitude between the same periods (Jarre-Teichmann,

1998)

2.3. Mediterranean ecosystems of the Catalan and Adriatic seas

The South Catalan Sea (NW Mediterranean Sea) is an oligotrophic area, where

enrichment occurs due to regional environmental events, mainly related to wind

conditions, the existence of a temporal thermocline and a shelf-slope current and river

discharges (Estrada 1996; Salat 1996; Agostini and Bakun, 2002). These episodes

greatly influence the productivity and fishing activity of the area (Agostini and

Bakun, 2002; Lloret et al., 2004), which yields almost half of the total landings of the

Catalan coast (Lleonart, 1990) and which is especially relevant for the reproduction of

small pelagic fishes, mainly the European anchovy (Engraulis encrasicolus).

Moreover, this is also a strategic area for marine vertebrate conservation, sheltering

important colonies of terns and gulls (Zotier et al., 1998; Abelló et al. 2003). Some of

these species forage actively on the marine shelf and find a complementary food

source in the discards generated by the trawling and purse seine fleets (Oro et al.,

1997; Oro and Ruíz, 1997; Arcos, 2001).

Although artisanal gears are still important, most fleets have developed towards a

nearly industrial type of activity fully exploiting continental shelves and upper slopes

of the area, associated with the highest landings and mainly composed of bottom

trawlers, purse seines and longliners. Small pelagic fishes, overcoat sardine (Sardina

pilchardus) and anchovy (Engraulis encrasicolus), constitute the principal component

of the catch in terms of biomass and are mainly caught by purse seiners and bottom

trawlers. Increasing concern about recruitment overfishing is related to the

Northwestern Mediterranean anchovy stocks (Papaconstantinou and Farrugio, 2000).

Moreover, sardine has decreased steadily since the 1980s apparently due to fishing

and environmental factors (Coll et al., 2005; Palomera et al., accepted). Other small

and medium-sized pelagic fish (e.g. horse mackerel Trachurus spp., mackerel

Scomber spp. and sardinella Sardinella aurita) are much less exploited. The demersal

fishery comprises mainly juveniles of several target species, e.g. hake (Merluccius

merluccius), red mullet (Mullus barbatus) and blue whiting (Micromesistius

poutassou), caught principally by the trawling fleet. Growth overfishing affects some

demersal resources because for many species the sizes at first catch are very similar to

those at which the fish recruit (Lloret and Lleonart, 2002; Sardà et al., 2005).

Moreover, the introduction of new fishing procedures such as modern longlines, e.g.

for adult hake, has eliminated the spawning refugia of some species and has lead to an

increasing concern for recruitment overfishing of some demersal stocks (Lleonart and

Maynou, 2003). Large demersal fish (e.g. adult hake) and large pelagic fish (e.g.

Atlantic bonito Sarda sarda, bluefin tuna Thunnus thynnus and swordfish Xiphias

gladius) are caught by longline and troll bait fleets and show low population levels.

Official landings from the area increased dramatically from the early 1960s to the

early 1980s, mainly due to governmental aids to the fishing sector. Marked

fluctuations in landings occurred thereafter until catches progressively declined from

1994 to the present. Total official landings from 2003 were similar to those reached in

the late 1970s. From 1994 to 2003 a decrease of 55% on total official landings has

been observed. This reduction is mainly based on the pelagic fraction. Demersal

landings have been maintained at similar levels since 1983 with a reduction of 18% in

landings and underwent smaller fluctuations over the period of decline in the pelagic

fraction. Pelagic and demersal landings reached similar values for the first time in

2003 (Coll et al., 2006b).

The Northern and Central Adriatic Sea constitutes the widest continental shelf in the

Mediterranean Sea (Pinardi et al., 2006) and is of great value for fishing within the

Italian and the European context (Bombace, 1992; Mannini and Massa, 2000). Owing

to river runoff and oceanographic conditions, nutrient concentration and production in

the Adriatic diminishes from north to south and from west to east (Fonda Umani,

1996; Zavatarelli et al., 1998), where northern parts related with shallow waters and

river runoff are considered eutrophic, the central area is considered mesotrophic and

the southern region, oligotrophic. The area is characterized by a high diversity of

environmental conditions that is translated into a high biodiversity (Ott, 1992).

Numerous studies describe the distribution and abundance of marine fauna and flora

of the Adriatic Sea (e.g. Riedl, 1986; Zupanovic and Jardas, 1989; Jukic-Peladic et

al., 2001). Moreover, it is also a strategic area for marine vertebrate conservation,

sheltering important seabird populations (Zotier et al., 1998; Baccetti et al., 2002) as

well as endangered marine mammals and turtles (Manoukian et al., 2001; Bearzi et

al., 2004).

Small pelagic fish, mainly sardine (Sardina pilchardus) and anchovy (Engraulis

encrasicolus), constituted the principal component of the catch in terms of biomass in

the 1990s and are mainly caught by purse seiners and mid water trawlers (Arneri,

1996; Mannini and Massa, 2000). The demersal fishery is highly multispecific and

mainly comprises juveniles of several target species, e.g. hake (Merluccius

merluccius) and red mullet (Mullus barbatus), caught principally by the trawling fleet.

Invertebrates (cephalopods and crabs) also constitute an important proportion of the

catch.

Important changes in landings have been recorded in the Adriatic, with a dramatic

increase from the mid 1970s to the mid 1980s, mainly due to the increase of small

pelagic fish in the catch. This was followed by marked fluctuations in landings until

catches progressively declined from late 1980s to the present; primarily because of the

decrease in small pelagic fish, especially of European anchovy (Engraulis

encrasicolus) and sardine (Sardina pilchardus) (Cingolani et al., 1996; Azzali et al.,

2002; Santojanni et al., 2003, 2005). Total official landings from 2000 are lower than

those reached in the late 1970s and existing data show a significant decrease in fish

landings, coupled with an increase of invertebrate landings (Coll et al., 2007). Various

target demersal species have been reported to be overexploited (e.g. Papaconstantinou

and Farrugio, 2000; Jukic-Peladic et al., 2001), and significant quantities are

discarded (Pranovi et al., 2000, 2001; Tudela, 2004). Simultaneously, proliferation of

some jellyfish species in the Adriatic Sea since the 1980s has been reported (e.g.

Rottini-Sandrini and Stravini, 1981; Zavodnik, 1991; Arai, 2001; Mills, 2001), in

parallel with the decrease in small pelagic fish and the increase in eutrophication.

Likewise, in the Black Sea, overfishing and eutrophication have been related to

massive jellyfish explosions during the 1970s and 1980s (Daskalov, 2002; Gucu,

2002).

3. METHODS

Data series and selected models available for the Benguela, Humboldt and

Mediterranean regions were compared in terms of indicators quantifying the roles of

small pelagic fish in the respective ecosystems examined.

3.1. Catch and abundance data series

Landings have been compiled for the selected ecosystems and are summarised in the

indicators i) Trophic level of the catch, ii) the Fishing-in-Balance (FiB) index and iii)

the ratio of pelagic:demersal fish in reported landings. Where available, research

survey biomass indices of pelagic and demersal species are used to illustrate how the

pelagic:demersal fish species ratios have changed over time. This was only possible

for the Southern Benguela and South-Central Chile.

3.2. “Static” (“Snapshot”) models

Several available trophic models representing each of the five ecosystems discussed

above are used. To facilitate meaningful comparisons between systems, these models

were standardized according to the methods described by Moloney et al. (2005).

Here, with the aim of exploring the effects of small pelagic fish on different

ecosystems, we select some of these models as a representative and comparable set

capturing the main characteristic periods within each system.

For the Southern Benguela, trophic models of the period 1980-1989 and 1990-1997

are available (Shannon and Jarre-Teichmann, 1999b; Shannon et al., 2003) and an

additional, comparable model of the period 2000-2004 has been developed. For the

Northern Benguela, several models have been constructed (Roux and Shannon 2004;

Shannon and Jarre-Teichmann, 1999a, b; Heymans et al., 2004). For purposes of this

chapter, standardized, updated models have been constructed for the 1960s, 1980s and

1995-1999, and are used to illustrate the main ecosystem changes that have occurred

off Namibia. For the Southern Humboldt ecosystem, models have been constructed

for 1992 and 1998 (Neira and Arancibia 2004; Neira et al. 2004) and more recently,

also for 2004-2005 (Neira in prep.). For the South Catalan Sea, trophic models

calibrated with time series of data and representing 1978 and 1994 have been used,

while in the case of the North and Central Adriatic Sea, models representing the

1980s and 1990s are available (Coll, 2006; Coll et al., 2005, 2006b, 2007).

Indicators derived from the static models and which were selected to assist in defining

the effects of small pelagic fish in the five ecosystems considered, include:

i) Catch/Biomass ratios for small pelagic fish (this is an index of the level of

exploitation and essentially equates to fishing mortality),

ii) Exploitation rate E=F/Z, where F is fishing mortality and Z is total mortality

(natural and fishing mortality combined) for the main commercial fish species in each

system,

iii) Sum of all flows to detritus.

In addition, Mixed Trophic Impact (MTI) analysis (Christensen and Walters, 2004) is

also used to quantify the variation in benthic-pelagic coupling of trophic interactions

in the ecosystems. Two (oldest and most recent) snapshot models from the Southern

and Northern Benguela, Southern Humboldt and the Mediterranean Sea are used and

the squared sum of all trophic impacts from the pelagic compartment on the demersal

one and vice versa, computed and compared by means of percentage variation in the

squared sum of the MTIs between the early and most recent modelled periods. The

sum of all trophic impacts from detritus on the demersal and pelagic compartment is

considered.

3.3. Models fitted to time series data

Models of the Southern Benguela, the South Catalan Sea and South-Central Chile

have been fitted to time series data and are used here to quantify, in ecosystem terms,

the changes in these three ecosystems since the 1970s.

A trophic model of the Southern Benguela ecosystem has been fitted to catch and

abundance time series data for 1978-2002 by means of forcing by fishing effort over

time, and environmental forcing of primary productivity, using flow control

parameters for model tuning (Shannon et al., 2004). This model is being updated for

revised and additional data series (Shannon et al., in prep. a). The ecological model

developed for the South Catalan Sea was fitted with time series of data from 1978 to

2003 and was able to satisfactorily reproduce the dynamics of several target species

considering fishing, trophic interactions and the environment (Coll et al., 2005; Coll,

2006, Coll et al., in prep.). Similarly, an ecosystem model of the Southern Humboldt

has been fitted to time series data from 1970-2004 (Neira et al., in prep.).

The advantage of using fitted models is that they can provide an estimate of the

abundance trajectories of species for which time series data are not available, and can

be used to quantify likely changes in predation mortality as a result of biomass and

fishery fluctuations. Biomass estimates of small pelagic fish and other important

groups are plotted over time using the three fitted time series models.

3.4. Simulations

One “snapshot” (static) model was selected for each of the following ecosystems (see

section 3.2): Southern Benguela (1980s), South Catalan (1994), North and Central

Adriatic Sea (1990s) and South-Central Chile (1992), and two hypothetical extreme

fishing scenarios were simulated to explore whether the effects of small pelagic fish

were similar across the systems and to identify any system specific attributes relating

to the role of small pelagic fish in these ecosystems.

All three models fitted to time series data (see section 3.3) as explained before

(Southern Benguela, South Catalan Sea and Southern Humboldt) showed that wasp-

waist flow control emerges when trying to fit our models to time series data. In the

model scenarios presented here, we adopt a standardized “wasp-waist flow control”

assumption, setting vulnerabilities (v’s, the model parameter describing the

availability of a prey species to a predator, see Walters et al., 1997; Christensen and

Walters, 2004) for wasp-waist control by small pelagic fish: v=1000 for top down

control of small pelagic fish on their plankton prey; v=1 for bottom up control of

small pelagic fish on their predators. These vulnerabilities are applied to trophic

interactions of the main small pelagic fish in the ecosystems considered: for Southern

Benguela simulations, wasp-waist settings were adopted for anchovy, sardine, “other

small pelagic fish” (e.g. flying fish, saury) and redeye; for Southern Humboldt and

Mediterranean simulations, wasp-waist settings are assumed for anchovy and sardine

only. V’s for all other interactions are set to the default v=2 for mixed flow controls.

Simulations are run for an initial 5-year period, during which no alterations to fishing

are simulated (for ease of visualization of model results and extraction of parameter

values in year 1). Two fishing scenarios are subsequently simulated for an additional

15-year period and model results extracted for the final year of simulation. Two main

simulations are performed:

Simulation 1: Closure of fishery on small pelagic fish

For each of the four models, the fishery on small pelagic fish is closed and biomass

trajectories plotted to examine which species benefited or are deleteriously affected.

Changes in the ratios of pelagic:demersal fish biomass are tracked over the simulation

periods.

Simulation 2: Collapse of small pelagic fish

For each of the four snapshot models selected for simulation purposes, the

exploitation rate E (E=F/Z) in year 5, required to collapse anchovy and sardine stocks

by year 16, are compared. Changes in biomass of the main groups responding to the

collapse of anchovy and sardine are plotted over the 15-year simulation period. As

above, pelagic:demersal fish biomass ratios are compared.

4. MODEL RESULTS

4.1 Catch and abundances

The ratio of small pelagic fish to demersal fish catches ranged between 1 and 9 in the

Northern and Southern Benguela, the South Catalan Sea and the North and Central

Adriatic, whereas in the Southern Humboldt, the ratio ranges from 1 all the way up to

60 (if horse mackerel, of which a significant portion are caught in the open ocean, are

included as pelagic fish) and 18 when horse mackerel are excluded (Fig. 3a-c),

reflecting the far greater importance of small pelagic fish in the Humboldt compared

to other fisheries examined.

TL of the catch (Fig. 4a) increased in the 1990s in the Northern Benguela, and from

1999 onwards in the Southern Humboldt, as a result of the collapse of small pelagic

fish, and thus the increase in the FiB index that was observed in these two cases are

misleading as they do not reflect an expansion of the fisheries but rather an underlying

collapse (Namibia) or at least a reduction in catches (Chile) of small pelagic fish. Off

South Africa, the recent short-term decline in the FiB reflects the high abundances of

small pelagic fish, in particular sardine, in the early 2000s, rather than the traditional

“fishing down the food web” situation.

By the late 1970s, horse mackerel became the most important fishery resource off

Central Chile due to the development and later westward expansion of an important

offshore fishery, mainly composed of an industrial purse-seine fleet. Consequently,

landings of horse mackerel have influenced total landings in Central Chile in the last

decades (Fig. 3b). The high landings of horse mackerel during the 1980s and 1990s

also masked the process of fishing down the food web from being detected in the

exploited community inhabiting the continental shelf (Arancibia and Neira, 2005).

Therefore, the indicators are presented with and without including landings of horse

mackerel for the Southern Humboldt ecosystem (Fig. 4b). The TL excluding horse

mackerel shows an increase in 2001, probably due to a combined decrease in landings

of common sardine and anchovy and an increase in landings of hake. The FiB shows

an increasing trend until mid 1990s that reflects the westward expansion of the fleet

targeting horse mackerel (Fig. 4c). Conversely, FiB excluding horse mackerel shows a

decreasing trend since the mid 1980s to minimum (negative) values in late 1990s (Fig.

4c). During early 2000s, both series of FiB (with and without horse mackerel)

increase (Fig 4c), probably owing to high landings of hake during this period.

However, this trend should not be interpreted as ecosystem recovery since Chilean

hake has recently collapsed and it is expected that the trend in FiB will strongly

decline in the next few years.

In the Catalan Sea (Fig. 4c), TL of the catch and the FiB index show the dynamics of

small pelagic fisheries, reflecting the expansion of the fishery and subsequent local

depletion of pelagic fish stocks (Coll et al., 2006a). In the case of the North and

Central Adriatic Sea (Fig. 4c) catch data suggest an increase of the TL of the catch

(due to decrease of small pelagic fisheries during the 1980s and a fishery based on

demersal species) and a following decrease due to increased invertebrate landings

(Coll et al. 2007). From the 1990s the decrease in the FiB indices reflected

deteriorating ecosystems and fisheries.

It is of interest to highlight that simulations of closures of small pelagic fisheries show

that after ten years, the pelagic:demersal biomass ratios increase from around 1 to

over 2.5 in the Southern Benguela, following a steady recovery of anchovy and

sardine over the ten-year simulation period (Fig. 5a). By contrast, the

pelagic:demersal biomass ratios for the South Catalan Sea, the Adriatic Sea and the

Southern Humboldt, which are all higher to begin with (around 5 for Chile and 14 for

the Mediterranean), increase following the pelagic fishery closure, as expected, but

subsequently decline to original levels or below as a result of increased hake biomass

levels in response to increased availability of sardine and anchovy prey (Fig. 5b,c,d).

Previous simulations of the Northern Benguela (Shannon et al., 2001; Roux and

Shannon, 2004) showed that a moratorium on sardine catches would have some

benefit to sardine but only small effects on other groups unless abundance of pelagic

goby was also reduced. These results provide an interesting contrast to those for other

upwelling systems, suggesting that the Benguela may operate differently to the others

examined, possibly because both Southern and Northern Benguela sub-systems have

an additional, largely unfished and abundant small pelagic fish resource (round

herring in the south and pelagic goby in the north, both forage fish species).

Alternatively, it is possible that after the intense exploitation of small pelagic fish in

the Southern Humboldt and Mediterranean systems, the subsequent sudden simulated

release of fishing pressure allows small pelagic fish to increase very fast initially,

whereas at least in the case of the Southern Benguela, small pelagic fish were not too

heavily exploited to begin with. However, in the northern Benguela, the observed

pelagic:demersal catch ratio increased over time as a result of increase in catches of

horse mackerel relative to piscivorous hake. Overall, the ratios indicate a shift towards

greater importance of demersal fish in the Benguela since the 1950s.

When simulating the collapse of small pelagic fish, the pelagic:demersal biomass

ratios decrease in the Southern Benguela, South Catalan Sea and North and Central

Adriatic Sea (Fig. 6) due to the decrease of pelagic biomasses. Decreases of 33% and

46% are observed in the Catalan and Adriatic cases respectively, while the Southern

Benguela shows a smaller reduction in the pelagic: demersal biomass ratio of 25%. In

the Southern Humboldt case, the simulated collapse of small pelagic fish results in a

decrease in the pelagic demersal biomass ratio and in the small pelagic fish/hake

biomass ratio of 25% and 100%, respectively (Fig. 6b).

4.2 Fishing mortality, predation and exploitation rates

Catch/biomass ratios are equivalent to fishing mortality rates and are compared in Fig.

7. Fishing mortalities are smallest in the Adriatic (maximum F = 0.2 y-1 for sardine

and anchovy), and the Southern Benguela (maximum F= 0.3 y-1 for anchovy and

sardine in the 1980s), whereas fishing mortality rates exceeding 0.3 y-1 and 0.5 y-1 are

estimated for anchovy in the South Catalan and Northern Benguela, respectively.

Estimated fishing mortalities are greater than 0.6 y-1 for sardine in the South Catalan,

and F of anchovy and common sardine is estimated to have exceeded 0.7 y-1 in the

Southern Humboldt ecosystem in 1992. It appears that smaller fishing mortalities can

be supported in the systems exhibiting greater biodiversity (shallow bank and

upwelling area of the Southern Benguela; diverse environmental conditions

responsible for diverse habitats in the Adriatic).

Using ecosystem models fitted to time series data to estimate predation mortality rates

on small pelagic fish, it was found that in the Southern Benguela, predators exerted

between 0.6 and 1.2 y-1 predation mortality over the last 25 years, between 0.2 and 1.6

y-1 in the Catalan and are higher, between 0.7 and 1.4 y-1 off Chile (Fig. 8a,b,c). This,

combined with the high fishing pressure on small pelagic fish off Chile, suggests high

total mortality exerted on small pelagic fish in the Southern Humboldt especially

during the late 1990s and early 2000s, and reiterates the fact that model results need to

be considered in the context of species dominance and abundance regimes.

Exploitation rates, equivalent to the ratio of fishing mortality to total mortality

(E=F/Z), are shown in Fig. 9. Sardine exploitation rates are higher in the South

Catalan Sea during the 1980s and 1990s, Southern Benguela during the 1980s and

1990s and Northern Benguela during 1980s and 1995 than in the other periods

modelled per system (Fig. 9a,c). Anchovy in the Southern Humboldt were also

subjected to high exploitation rates in 1998 (Fig. 9c). Exploitation rates registered for

hake and anglerfish in the South Catalan Sea during the 1990s, as well as for mullets

and demersal sharks during the 1980s and 1990s in the Adriatic Sea (Fig. 9e), are

higher than the maximum 0.8 recommended for groundfish stocks (Mertz and Myers,

1998; Rochet and Trenkel, 2003).

In Southern Benguela model simulations, in order to collapse the pelagic fishery

within the 10- year simulation period, fishing mortalities need to be increased by a

factor of 2.5 of the 1980s levels, corresponding to F=0.8y-1 for anchovy and F=0.3y-1

for sardine in that period (Fig. 6a), which corresponded to exploitation rates of 0.57

for anchovy and 0.25 for sardine. Note that the purse seine fishery is modelled as a

single unit so that anchovy and sardine fishing mortalities are not adjusted

independently in these simulations, and thus only provide a very rough guideline of

what would have been required to collapse these stocks at that time.

In the Southern Humboldt model (Fig. 6b), in order to collapse the pelagic fishery

within the 10- year simulation period, fishing mortalities need to be increased by a

factor of 1.7 of the 1992s levels, corresponding to F=0.73 y-1 for anchovy and F=0.77

y-1 for common sardine in that period (with E = 0.25 for anchovy and 0.32 for

common sardine). In this simulation, the purse seine fishery targeting small pelagic

fish is modelled as a single unit, so that anchovy and common sardine fishing

mortalities are not adjusted independently.

In the South Catalan Sea, the pelagic fishery of anchovy and sardine collapse within

10 years of simulation when fishing mortality are hypothetically increased by a factor

of 2, corresponding to an exploitation rate of 0.62 for anchovy and 0.64 for sardine,

with F=1.70 y-1 and F=2.15 y-1, respectively. In the North and Central Adriatic Sea,

fishing mortality is increased by a factor of 2.3 and exploitation rate resulted in 0.78

and 0.79 for anchovy and sardine (F= 1.57 y-1 and F= 1.61 y-1), respectively (Fig. 6c).

These high fishing mortalities may mean that the Mediterranean ecosystems would be

likely to show much higher levels of exploitation than the Chilean and South African

systems (Coll et al. 2006a).

4.3. Gelatinous zooplankton and proliferation of other species

Simulations yield relatively consistent results where gelatinous zooplankton increase

when small pelagic fish stocks collapse and conversely, there is a decrease in jellyfish

abundance when closure of the pelagic fisheries is simulated (Table 1). In Southern

Benguela simulations, macro-zooplankton follows similar trajectories to gelatinous

zooplankton, increasing by 8% when a collapse of the purse seine fishery is

simulated, and declining to 68% of original levels when the purse seine fishery is

closed. Phytoplankton biomass remained unchanged. In the case of the Catalan Sea,

jellyfish increase when a collapse of the small pelagic fishery is simulated, while there

is also an increase in micro-mesozooplankton and macrozooplankton of 21% and

35%, respectively. On the contrary, the model simulation predicts an 8% decrease in

phytoplankton biomass. Similarly, in the North and Central Adriatic Sea, simulations

suggest an increase in jellyfish biomass when small pelagic fisheries collapse, while

micro-meso and macrozooplankton show an increase of 18% and 2%, respectively.

Phytoplankton biomass decreases by 5% in the Adriatic. Similar results were found

by Roux and Shannon (2004) when a hypothetical fishery on jellyfish was modelled,

in that anchovy and several predatory fish species were favoured when 50% of

gelatinous zooplankton production was “removed” through “fishing”.

Simulations also show the proliferation of other species when small pelagic fish

stocks collapse (Fig. 6). Both ecological models from the Catalan and Adriatic Sea

highlight the increase in abundance of other small pelagic fish and benthopelagic fish

(Fig. 6a). Similar results were also seen when fitting the models to time series of data

(Fig. 10). In the South Catalan Sea (Coll et al., 2005, Coll et al., in prep.) a general

decrease in the biomass of small pelagic fishes was predicted in parallel with an

increase of the biomass of bentho-pelagic fish, cephalopods, as well as jellyfish, all of

them showing important fluctuations in terms of abundance (Fig. 10c).

Table 1. Ratio of biomass of gelatinous zooplankton groups in year 15 compared to

year 1 (expressed as a percentage) when a collapse of small pelagic fisheries is

simulated (scenario 1) and when closure of small pelagic fisheries is simulated

(scenario 2).

Scenario S. Benguela S. Catalan Adriatic S. Humboldt

1. Collapse 108% 164% 118% 109%

2. Closure 76% 32% 75% 16%

4.4. Effects of small pelagic fish on top predators

In the southern Benguela, simulation of a collapse in small pelagic fish suggest severe

declines in large pelagic fish (48% reduction in biomass), seals (17% decline), birds

(33% decline) and cetaceans (27% decline). On the contrary, model biomass of seals,

seabirds, cetaceans and large pelagic fish predators all increase (by factors of between

1.5 and 2.2 of original levels by year 15) when closure of the South African purse

seine fishery is simulated. In the Southern Humboldt simulation of small pelagic

fishery collapse, seabirds collapsed and sea lions decline to 29% of original values,

whereas simulated closure of the fishery suggests huge increases in seabirds and sea

lions, by a factor of 9 and 12 respectively over the 15 year simulation period.

Similarly, in the South Catalan Sea, seabirds declined to less than half their biomass,

and totally collapsed in the North and Central Adriatic. The ecological model of the

South Catalan Sea also highlights that the decline of small pelagic fish biomass occurs

in parallel with a decrease of abundance of demersal and pelagic predators such as

European hake, anglerfish, demersal sharks and large pelagic fish (Fig. 10c). This

could exemplify the importance bottom-up flow control on predators by their small

pelagic fish prey.

In the case of the South Catalan Sea, however, seabirds have shown an increase in

abundance since the 1980s, even though the fishing effort (and thus bycatch) has

increased in the region. This is also partially reproduced by the model fitted to data

through a mediation function (Coll et al. 2005; Coll et al. in prep.) (Fig. 10c) and it is

mainly due to the increase in discards from trawling and the protection of breeding

colonies in the area since the beginning of the 1980s, which compensated for a

decrease in forage fish available on the continental shelf (Oro, 1996; Oro et al., 1996;

Oro and Ruíz, 1997). In the Southern Humboldt, simulations suggest that when small

pelagic fishing is stopped, small pelagic fish increase in biomass, followed by a rapid

increase in the biomass of sea lions, marine birds and Chilean hake. By comparison, a

simulated collapse of small pelagic fish is followed by a sharp decline of the same

groups, reflecting the role of small pelagic fish as important drivers of ecosystem

dynamics.

4.5 Flows to detritus

From the snapshot models it appears that flows to detritus tend to increase when small

pelagic fish biomass declines. In the Northern Benguela, total flow to detritus was

lower in the earlier period (1960s), before small pelagic fish had collapsed (Fig. 11a).

Similarly, in the Southern Humboldt, pelagic fish declined in the 2000s and this was

the period for which flows to detritus were highest (Fig. 11b). By comparison, there

was little change in the total flows to detritus in the three periods examined in the

Southern Benguela (Fig. 11a), although total flows to detritus were marginally smaller

in the recent period when pelagic fish abundance was exceptionally high. Nor were

their marked differences between flows to detritus in the two periods considered for

the South Catalan or the Adriatic Sea (Fig. 11c).

The general trend of reduced flows to detritus when small pelagic fish are abundant

was less well illustrated through simulations, probably as a result of possible model

competitor release of other small pelagic fish or mesopelagic fish when anchovy and

sardine decline. In fact, flows to detritus increased slightly when closure of the small

pelagic fishery of the South Catalan, North and Central Adriatic and Southern

Benguela ecosystems were simulated (Table 2). By comparisons, the Southern

Humboldt simulations suggested that flows to detritus decreased to 76% when the

pelagic fishery was closed (and pelagic fish abundance increased), and increased

slightly when the modelled pelagic fishery collapsed anchovy and sardine stocks

(Table 2). Overall, standardized snapshot models revealed that flows to detritus were

three times larger off Chile than in the other ecosystems considered, reflecting the

high productivity of this ecosystem in comparison to the others.

Table 2 Ratio of total flows (all combined) to detritus in year 15 compared to year 1

(expressed as a percentage) when a collapse of small pelagic fisheries is simulated

(scenario 1) and when closure of small pelagic fisheries is simulated (scenario 2).

Scenario S. Benguela S. Catalan Adriatic S. Humboldt

1. Collapse 99% 95% 97% 102%

2. Closure 100% 113% 108% 76%

Differences between ecosystems were found in the sum squared of all trophic impacts

of detritus on the demersal and pelagic compartments. In the Southern and Northern

Benguela and South Catalan Sea, the sum squared of the mixed trophic impacts of

detritus on the demersal compartments increased over time, while in the Adriatic Sea,

this measure declined (Table 3). The sum squared of the mixed trophic impacts of

detritus on the pelagic compartment increased in the case of the Southern Benguela

and the Mediterranean Sea case studies. In the southern Humboldt models, no changes

were observed in the impacts of detritus on the demersal groups. On the other hand, a

small increase in the impacts of detritus on pelagic groups was observed (Table 3).

The likely explanation for these results is a strong decrease in the biomass of the main

demersal fish species in the system (hake) and the low biomass levels of detritivorous

groups such red squat lobster and yellow squat lobster in the most recent model.

Table 3 Variation (%) of the sum (squared) of all trophic impacts of detritus on the

demersal and pelagic components, derived from the Mixed Trophic Impact analysis of

snapshot models of Southern and Northern Benguela, Southern Humboldt and

Mediterranean Sea case studies.

Scenario S. Benguela

(early 2000s

compared to

1980s)

N. Benguela

(1960s

compared to

late 1990s)

S. Catalan

(1994

compared

to 1978)

Adriatic

(1990s

compared

to 1975)

S. Humboldt

(2004-05

compared to

1992)

1.

Detritus-

demersal

252.5% 52.8% 6.0% -30.7% 0.0%

2.

Detritus-

pelagic

246.6% -32.7% 7.5% 13.8% 6.7%

4.6 Coupling demersal-pelagic compartments

Aggregated MTI analysis was also used to quantify the changes in the mixed trophic

impacts for demersal and pelagic compartments. In the Southern Benguela, Catalan

and Adriatic Sea, the sum of all mixed trophic impacts of the pelagic compartment on

the demersal one increased over time (and in the Mediterranean case, with increasing

fishing pressure), while the demersal impacts on the pelagic compartment decreased

in the Southern and Northern Benguela, Southern Humboldt and Catalan Sea, but

showed little change in the Adriatic (Table 4). The collapse of the pelagic ecosystems

in the northern Benguela and the recent collapses of horse mackerel, squat lobsters

and hake in the Southern Humboldt are exemplified by the noticeable decreases in

demersal-pelagic MTIs.

Table 4 Variation (%) of the sum (squared) of all trophic impacts of the pelagic

component on the demersal component, and vice versa, derived from the Mixed

Trophic Impact analysis of snapshot models of Southern and Northern Benguela,

Southern Humboldt and Mediterranean Sea case studies.

Scenario S. Benguela

(early 2000s

compared to

1980s)

N. Benguela

(1960s

compared to

late 1990s)

S. Catalan

(1994

compared

to 1978)

Adriatic

(1990s

compared

to 1975)

S. Humboldt

(2004-05

compared to

1992

1. Pelagic

on

Demersal

32.2% -15.2% 4.8% 70.0% -32.0%

2.

Demersal

on Pelagic

-18.7% -50.7% -19.6 0.5% -36.0%

5. DISCUSSION

5.1. Trophic flow controls, fishing and environment

An ecosystem model of trophic flows in the Southern Benguela was fitted to time

series data from 1978-2002 (Shannon et al., 2004b) and is currently being revised and

improved by incorporation of updated and revised time series (Shannon et al., in prep.

a). These studies support the findings of a hypothetical simulation study (Shannon et

al., 2004a) showing that off South Africa, environmental factors have been more

important drivers of ecosystem dynamics than fishing over the latter part of the 20th

century, explaining up to 23% of observed variability in the major ecosystem

components examined (Shannon et al., in prep. a). In particular, model simulation

studies suggest that environmental forcing changing the relative availability of

mesozooplankton to anchovy and sardine may be a key factor in driving changes in

the abundance of small pelagic fish in the southern Benguela (Shannon et al., 2004c).

These mechanisms and their physical forcings are still being explored in more detail

(Shannon et al., in prep. b). As mentioned earlier, Verheye et al. (1998) found both

bottom-up and top-down effects of small pelagic fish on zooplankton off the South

African west coast. The latter model result would be a case for bottom-up control of

small pelagic fish. Shannon et al. (2004b) found that model parameterisation

describing prey vulnerability to predators accounted for over 40% of the observed

variability in the time series examined, and suggested clear wasp-waist flow control

by small pelagic fish as a characteristic of this upwelling system.

A model representing the Southern Humboldt upwelling system in the year 1970 was

fitted to available time series of relative biomass, catch and fishing mortality for the

period 1970 to 2004 (Neira et al., in prep.). Fishing mortality explained 28% of the

variability in the times series, whereas vulnerability (v) parameters estimated using

EwE explained an additional 21%. When a function affecting primary production is

calculated by Ecosim to minimize the Sum of Squares (SS) of the time series, a

further 11% to 16% of variability is explained. The best fit model indicated that a

long-term change in primary production might have affected the dynamics of groups

in the Southern Humboldt system since no statistical evidence was found to support

the null hypothesis that all of the deviations between model and predicted abundances

are due to chance alone (p value<0.05), indicating that there is a consistent pattern in

the deviations. This result is reinforced when the primary productivity anomaly

proposed by the model is compared with independent time series of sea surface

temperature and an upwelling index in the system for the period 1970 to 2000 (Neira

et al., in prep). The fitting process revealed that changes in the SS are sensitive to,

amongst others, trophic relationships involving common sardine and anchovy as

predators, but not as prey, in agreement with the hypothesis of wasp-waist control in

upwelling ecosystems (Cury et al., 2000; Cury et al., 2005b). Although the

combination of v values for the best fit model seems to indicate a pattern in terms of

small pelagic fish controlling their prey (top-down), bottom-up control of small

pelagics on their predators was not as clear, which could be related to the lack of time

series for top predators. However, independent analysis indicates that in last 15 years

the biomass of hake was positively and significantly correlated to the biomass of

small pelagic fish (likely bottom-up control; Neira et al., 2006). Using Generalized

Linear Models, these authors show that the only explanatory variable affecting the

biomass of small pelagic fish in last 15 years is sea surface temperature (S. Neira,

University of Cape Town, South Africa, unpublished data; Neira, in prep.). The above

results are in agreement with the hypothesis of wasp-waist where the dynamics of

small pelagics are not controlled by predation (hake biomass and fishing mortality) or

food availability but are rather affected by environmental variability.

When fitting the ecological model of the South Catalan Sea to available time series of

data (Coll, 2006; Coll et al., 2005, Coll et al., in prep.) similar results were found.

Trophic interactions accounted for half of the observed data variability, while fishing

and the environment had similar contributions (approximately 7%) to explaining the

variability in time series data. Moreover, small pelagic fish were found to be exerting

wasp-waist (sardine) and bottom-up (anchovy) flow control, also in line with previous

hypotheses. The function affecting primary production calculated by Ecosim to

minimize the Sum of Squares of the time series was significant, and later negatively

correlated with sea surface temperature and the NAO index.

Therefore, configuration of the trophic web seems to play a major role in explaining

the dynamics of marine ecosystems and small pelagic fish, and its modification by

fishing and the environment can have important impacts on the whole ecosystem. The

synchrony in the dynamics of small pelagic stocks around the world (Kawasaki, 1983;

Lluch-Belda et al., 1992) may mean that the link between environmental and

ecosystem change could be less complex than initially expected (the environment is

acting either directly on small pelagic fish or their main food, and through small

pelagic fish these effects are propagated up and down the food web). On the other

hand, the effects of overexploiting small pelagic fish could lead to dramatic and

possibly even irreversible ecosystem change, since collapse due to overfishing small

pelagic fish can exacerbate “natural” fluctuations induced by the environment. For

example, there has been a drastic change in the pelagic ecosystem of the Northern

Benguela since the 1980s (Bakun and Weeks, 2004), including a collapse of anchovy

and sardine stocks and proliferation of jellyfish, as a result of a series of unfavourable

environmental events which have been exacerbated by heavier fishing than was in fact

sustainable at the low stock biomasses at the time (Boyer et al., 2001). Similarly, in

the Black Sea (Daskalov, 2002) a regime shift has been described in relation to both

overexploitation (causing a trophic cascades down the food web), and eutrophication,

and a collapse of small pelagic fish has been followed by the proliferation of

jellyfishes. However, other factors may account for jellyfish outbreaks, such as the

beneficial impacts of bottom trawling to benthic-spawning jellyfish. Mills (2001) has

reported outbreaks of new non-indigenous jellyfish species in certain areas linked to

changes in climatic conditions.

5.2. Generic effects of fishing on small pelagic fish

Frank (2006) showed a north-south geographical gradation in flow controls in the

North Atlantic, with more productive and diverse ecosystems better able to deal with

top-down perturbations (such as fishing) and instead rather showing stronger bottom-

up influences, whereas he showed that top-down effects are large in less productive

and less diverse ecosystems of the northern North Atlantic. Carr (2002), when

examining productivity of eastern boundary current ecosystems, found a mismatch

between the estimated fish yield (given productivity estimates in these upwelling

ecosystems) and the reported landings of small pelagic fish, suggesting that the

trophic structure of upwelling ecosystems differ from one another. In particular, Carr

(2002) contrasted the high productivity of the Benguela and the lower productivity of

the Humboldt, noting that small pelagic fish production was much higher in the

Humboldt than in the Benguela ecosystem. Nevertheless, our model comparisons

seem to suggest the overarching commonality of upwelling systems being wasp-waist

controlled. The major coastal upwelling systems are characterized by variability in

their chemical-physical conditions over a wide range of spatial and temporal scales

(Hill et al., 1998) (and, to a lesser extent, also the Mediterranean, Bosc et al., 2004).

Individuals, populations and food webs respond in different ways to this variability.

On the other hand, fishing has more generic effects on populations and communities

such as decreasing trophic level and size structure of populations and exploited

communities (i.e., Pauly et al., 1998). Therefore, despite the importance of different

environmental drivers in each system, we expect that the “generic” effects of fishing

in driving changes in the systems analysed could be comparable given the common

wasp-waist ecosystem structure pivoting around small pelagic fish. In particular,

strong changes in the abundance of small pelagic fish (populations located in the

waist of the food webs where they occur, see introduction), induced by fishing, could

have comparable effects on ecosystem structure and function.

Models analyzed in this study show how a decrease in small pelagic fish abundance

will have important effects on both higher and lower trophic levels of the food web,

causing a decrease in predators and the proliferation of other species that are preys or

competitors. Changes in small pelagic fish disrupt energy flows, which could result in

an increase in flows to detritus, demersal processes within the system becoming more

important and stronger coupling of pelagic to demersal trophic compartments.

In addition, the collapse of small pelagic fish could lead to a change in the kind of

trophic control in a food web, for example from the generic wasp-waist control

characteristic of several upwelling ecosystems, to a system that is more bottom-up

influenced by the environment or by replacement of opportunistic species that benefit

from excess plankton production but do not transfer this production to upper trophic

levels, either because they are not widely edible (i.e., jellyfish) or because their

bathymetric distributions (e.g. of mesopelagic fish) make them inaccessible to

predators with limited diving capacity (seabirds). Modelling can improve our

understanding of these changes although admittedly we are only beginning to

understand how fishing changes the structure and functioning of ecosystems.

5.3. Proliferation of species

The simulations explored in this chapter suggest that jellyfish may proliferate when

small pelagic fish are heavily fished (Table 1). In the four models used for simulation

purposes, jellyfish biomass increased after modelled small pelagic stocks were

collapsed. The proliferation of gelatinous zooplankton is linked not only to the

availability of a trophic niche, but also to their higher turnover rate (and possibly also

environmental conditions). Fishing, by disturbing the structure and functioning of

marine ecosystems, tends to result in communities dominated by small bodied and

rapidly reproducing species. According to Odum (1985), in stressed ecosystems it is

expected that a decrease in K-selected species will be followed by an increase in

opportunistic r-selected species. Therefore, classic food web analysis based on trophic

relationships may not be sufficient to analyze extreme scenarios such as ecosystem

collapse. The effect of turnover rate of functional groups should also be taken into

account when modelling and analyzing strong ecosystem changes (Leibol et al, 1997).

Further understanding of these processes is essential to predict jellyfish outbreaks,

which are of high concern in tourist areas.

Although there is not empirical data available, the fitted South Catalan Sea model

shows that some non target species could have also proliferated in the area. This

would be the case for benthopelagic fish, due to the decline of competitors (e.g. small

pelagic fish) and predators (e.g. demersal fish) and increased availability of prey (e.g.

phytoplankton). The Alboran Sea, Southwestern Mediterranean, has shown a

proliferation of boarfishes Capros aper (Linnaeus, 1758) after the collapse of small

pelagic fisheries due to high fishing intensity and environmental changes (Abad and

Giraldez, 1990). Improved understanding of these processes is of special interest for

fisheries and coastal management.

Simulation results also show that changes on small pelagic fish abundance have

important impacts on other zooplanktonic species and support the idea that pelagic

fish exert top-down control on their zooplanktonic preys (Cury et al., 2000).

5.4. Effects of small pelagic fish on top predators

Fluctuations of small pelagic fish have an important impact on predator populations,

as can be seen from model simulations that illustrate the importance of these

organisms as prey for demersal and pelagic feeders such as tunas, seabirds, marine

mammals and groundfish predators.

In the southern Benguela, a system in which marine mammals and birds are relatively

abundant, a simulated collapse of the small pelagic fish suggests severe declines in

large pelagic fish, seals, birds and cetaceans. In addition to “simple” direct predator-

prey effects that have been modelled are other indirect influences; African penguin

breeding success has been found to be significantly related to fish prey abundance

(Crawford et al. 2006), and the proportion of penguins choosing to breed in any

particular year has also been found to be prey related (Crawford et al. 1999).

In the case of the South Catalan Sea, top predators feeding on small pelagic fish (e.g.

hake, anglerfish and dolphins) also show decreasing biomass when these prey

organisms collapse. However, seabirds have shown an increase in abundance due to

the increase of discards, as already discussed, highlighting the indirect effects of

fishing. A moratorium on trawling activities in the Catalan Sea affected populations

of seabirds due to reduced food availability during the breeding season (Oro et al.,

1996).

Moreover, and not yet considered in ecological modelling studies such as the

simulations presented in this chapter, it is not only the quantity of food available to

predators that is an important factor affecting trophic mechanisms up the food web,

but also the quality of that food. Not only do predators and prey need to overlap in

time (Cushing’s [1990] match/mismatch hypothesis) and in space, but the quality of

the prey needs to be of a suitable quality (Beaugrand et al., 2003). For example, in

2004, the common guillemot (Uria aalge), which usually feeds on sandeel

(Ammodytes marinus) during its breeding season, fed sprat (Sprattus sprattus) to its

chicks; breeding success was poor and the chicks produced were in poor condition

(Wanless et al., 2005). Although daily food intake by the chicks in 2004 did not differ

from previous years, the nutritional content of sprat was found to be much lower than

that of sandeel, pointing to food quality as an important factor in seabird breeding

success (Wanless et al., 2005). Changes in the availability of essential fatty acids has

been shown to have drastic effects on fish population dynamics, as they contribute to

regime shift effects on fish populations (Litzow, 2006). Environmentally-induced

decreases in availability of lipid-rich fish to seabirds can also justify dramatic declines

in number of breeding marine kittiwakes (Kitaysky et al., 2006). Another example is

the Alaskan Steller sea lion (Eumetopias jubatus). Sea lion pups have been found to

starve in times when alternative prey such as gadids appear to be abundant, because

the energy density and digestibility of gadid prey is low, whereas forage fish are a

high energy source that is more digestible (Winship and Trites, 2003). Pup mortalities

increased when South American sea lion adjusted their diets and maternal attendance

patterns in response to El-Nino-induced annual changes in the abundance and

distribution of fish prey (Soto, 2006). Following the 1970s Pacific Decadal

Oscillation regime shift, walleye pollock Theragra chalcogramma, a lipid-poor

species, increased in abundance, while capelin Mallotus villosus, a lipid-rich species,

declined.

Changes in stock sizes of small pelagic fish are often associated with shifts in the

geographical distribution of these fish (Lluch-Belda et al., 1989). This has been found

to be true of anchovy (Barange et al., 1999) and sardine (Janet Coetzee, MCM, South

Africa, pers. comm.) off South Africa; their distributions are expanded at large stock

sizes. Thus, small pelagic fish cause, or at least themselves are associated with shifts

in the distributions of several other ecosystem components, in particular their

predators. This is particularly well illustrated off southern Africa, where changes in

the distribution of small pelagic fish, and therefore also the availability of prey to

predators such as seabirds, have been observed. There has been an eastward shift in

the distribution of pelagic fish resources off South Africa (van der Lingen et al.,

2006), which has led to a large reduction in size of the African penguin colonies along

the South African west coast as a result of severely reduced availability of prey to

land-bound breeders (Crawford, 2006). The eastward distributional shift of small

pelagic fish in the southern Benguela in recent years has been matched by a similar

southward geographical shift in west coast rock lobster (Mayfield and Branch, 2000),

attributed to large scale environmental forcing (Cochrane et al., 2004). Off Namibia,

there has been a northward distributional shift on seals and seabirds such as African

penguins between the early 1980s and the 2000s, which is concurrent with northward

contraction of anchovy and sardine spawning stocks in that region (van der Lingen et

al., 2006).

Unfortunately, no biomass/abundance time series for top predators such as marine

birds and marine mammals are available off central Chile. Therefore, the effects of

changes in the abundance of small pelagics in their populations are practically

unknown. Off Peru, changes in population size of guano-producing seabirds

(cormorant, Phalacrocorax bougainvillii; booby, Sula variegata; pelican, Pelecanus

thagus) could be a response to changes in primary and secondary production of the

Peruvian upwelling system, likely mediated by anchovy (Jhanke et al., 2004). Using a

modelling approach, these authors indicate that seabirds would have consumed 14.4%

of the available anchovy resource during the period prior to the development of the

fishery targeting anchovy. Once the fishery was in full operation, seabirds only

accessed 2.2% of the available anchovy resource (Jhanke et al., 2004)

5.5. Increased pelagic-benthic coupling and flow to detritus

Benthic-pelagic coupling is viewed as an important process in highly exploited

ecosystems. For example, this was found to be important in the Namibian upwelling

ecosystem after depletion of stocks due to industrial fishing and environmental events,

an important feature that appears to set this system apart from other upwelling

ecosystems (Moloney et al., 2005). The Namibian region shows some similarities

with the South Catalan Sea (Coll et al., 2006a), and this is also characteristic of highly

fished temperate regions (Sánchez and Olaso, 2004).

Results from the North and Central Adriatic Sea model also highlight the importance

of coupling between the pelagic and demersal compartments in that ecosystem,

mainly due to the link between detritus and benthic and pelagic invertebrates (Coll et

al., 2007). This is likely explained by the shallow waters and the oceanographic

features of the area (Ott, 1992). For example, zooplankton production that is directed

to detritus is high and has an impact on benthic production, underlining the

importance of pelagic production for the maintenance of benthic production within

the ecosystem (Ölscher and Fedra, 1977; Ott, 1992). Moreover, benthic invertebrates

are partially fished but there is an overall low use of their production, which is also

converted into detritus, favouring zooplankton dynamics further. This also indicates

the importance of detritus from the benthic compartment in favour of planktonic

production (Giordani et al., 1992).

The Humboldt system, comprised by the northern (Peru) and southern (Chile) sub-

systems, is probably the largest in terms of size when compared to other upwelling

systems (Jarre-Teichmann and Christensen, 1998; Neira et al., 2004). In addition, this

system has probably exhibited the most pronounced changes in system size after the

collapse of the anchovy stock off Peru, and horse mackerel off Chile. After the

collapse of anchovy, the Peruvian system became similar to the northern Benguela

system, the latter decreasing in size from the mid-1970 to the early 1980s due to the

strong decrease of small pelagics (mainly sardine), which was not compensated for by

the increased abundance of horse mackerel (Jarre and Christensen (1998). The simple

simulations examined here suggest that reducing small pelagic fish abundance will

most likely result in an increase in flows to detritus, probably due to the disruption of

energy transfer from low to high trophic levels (i.e. excess primary production that is

not efficiently transferred up the food web). These results are in line with Peruvian

ecosystem (Northern Humboldt) (Walsh, 1981) where trophic flows to detritus from

1966 to 1979 were seen to increase due to overfishing of anchovy. Therefore, flows to

detritus may be of importance and could be seen as a measure of increasing pelagic-

benthic coupling.

The increase in flows to detritus in the Mediterranean was smaller than in other

ecosystems analysed, most probably due to the fact that fluctuations of small pelagic

fish abundances are smaller in the Mediterranean and that this area has a history of

being heavily fished (Margalef, 1985; Pauly et al., 1998).

5.6. Enhancing catches of commercially valuable predatory fish by reducing

small pelagic fish catches?

Simulation of closed small pelagic fisheries in the Southern Benguela suggests that

higher demersal fish biomasses would be unlikely to be supported despite the

increased abundances of forage fish (Fig. 5a). By comparison, closed small pelagic

fisheries in the South Catalan, North and Central Adriatic and Southern Humboldt

models suggest that larger stocks of demersal fish, especially hake, would be

supported (Fig. 5b,c,d), thus benefiting the demersal fisheries. This was especially

noticeable in the Chilean case, where the potential benefits of closing the small

pelagic fishery appear to be larger, and projected model hake biomass increases

almost nine-fold (compared to 3-4-fold increases in hake biomass in the Catalan and

Adriatic models respectively). As the demersal fishery is of greater economic

importance in the Mediterranean areas than the small pelagic fisheries, temporal

closure of the small pelagic fish fishery could be economically beneficial. However,

formal simulations based on sound economic data would need to be carefully

designed and examined to analyze this. Specifically, in these simulation results,

demersal groups might benefit from an increase in small pelagic fish provided their

own fishery is kept at a constant level during the simulation period, suggesting that

benefits of increased small pelagic fish abundance may only be reaped if the predator

stocks are also sustainable managed (or maintained at healthy levels, in the case of

charismatic species).

As previously mentioned (section 4.1), the Benguela ecosystems (north and south)

differ from the others by also supporting large stocks of a third abundant small

pelagic, namely round herring in the Southern Benguela and pelagic goby in the

Northern Benguela. It is unlikely that round herring and pelagic goby are strong

competitors with anchovy and sardine for zooplankton food as they exhibit different

feeding behaviours. Tanaka (2006) found that feeding behaviour of filter-feeding

Japanese anchovy, and thus zooplankton composition in its diet, differs from that of

particulate-feeding Pacific round herring and Japanese jack mackerel in the East

China Sea, bringing about a certain degree of trophic partitioning in this pelagic

ecosystem. Round herring off South Africa feed on different species and sizes of

zooplankton to anchovy and sardine (Wallace-Fincham, 1987; C. van der Lingen,

MCM, South Africa, pers. comm.). Diet analyses of pelagic goby off Namibia have

recently shown that this species can feed on macrobenthos as well as on zooplankton

in the water column (J.-P. Roux, NMFR, Namibia, pers. comm.). However, despite

the largely limited competition for food amongst these small pelagic fish, model

simulations suggest an indirect effect of anchovy and sardine on other small pelagic

fish, possibly through predator niche overlaps.

In the closed pelagic fishery simulation using the Southern Benguela model, the round

herring stock declines to a mere 13% of its original 1980s level, and the “other small

pelagic fish” group is reduced to 28% of starting biomass, in response to competition

with the expanding populations of anchovy and sardine. In addition, the Southern

Benguela ecosystem also differs from the Catalan, Adriatic and Humboldt ecosystems

by supporting relatively large stocks of large, predatory pelagic fish, in particular

snoek. Trophodynamic responses of the latter to a closed purse seine fishery may

explain the apparent lack of favourable effects on demersal predatory fish species

when the modelled purse seine fishery is closed, given that projected large pelagic

fish biomass increased by a factor of 2.3 over the ten year simulation period (Fig. 5a).

It is also probable that in the Southern Benguela, the simulated biomass of small

pelagic fish and thus also some of their predators do not increase substantially when

the model purse seine fishery is closed because small pelagic Fishing mortalities were

relatively low to begin with (F of around 0.3 y-1), compared to Fs of anchovy and

sardine in the Mediterranean and Chilean models. Another relevant factor to consider

is how heavily fished hake are in the various ecosystems. In the Southern Benguela,

the exploitation rate of hake was between one quarter and one tenth of that in the

Chilean and Mediterranean systems (Fig. 9), so this would not lend support for the

argument that hake are more heavily fished in the Benguela and thus less likely to be

able to respond to increased forage fish abundance. A final point of consideration

must be the relative importance of small pelagic fish in the diets of hake and other

predatory fish in the different modelled ecosystems. In the Southern and Northern

Benguela, small pelagic fish comprise around a third of the diet of hake, and even less

than this in the 1980s model of the Southern Benguela (before both anchovy and

sardine were abundant in the early 2000s). On the other hand, large pelagic fish such

as snoek are estimated to be relying on anchovy and sardine for 30-40% of their diet

off South Africa. By comparison, hake in the Mediterranean and Humboldt

ecosystems are estimated to fill 50-60% in the Mediterranean (see Stergiou and

Karpouzi, 2002 for a review) and between 30 and 50% of their diet composition with

small pelagic fish.

6. SMALL PELAGIC FISH AS INDICATORS OF ECOSYSTEM COLLAPSE?

6.1 Ecosystem Indicators

By comparing ecosystem indicators between systems in different time periods when

the ecosystems were considered to have functioned “normally” or at least to have

been sustainably fished, to those that have been over-exploited or that have collapsed

because of the synergistic effects of the environment and exploitation, we examined

the values/trends exhibited by overexploited ecosystems. Ideally, we would have liked

to be in a position to propose levels/ ranges/ limits of indicators which should be

avoided when managing systems that are not yet overexploited/collapsed.

Exploitation rates applicable to certain kinds of fish, such as small pelagic fish, may

be one of the better examples available. However, most indicators, especially those

quantifying trophodynamics, are largely still descriptive and reference points are yet

to be agreed upon. Cury et al. (2005a) concluded that a suite of trophodynamic

indicators is needed to track complex fisheries and ecosystem changes and that,

although helpful in understanding ecosystem and fisheries dynamics that arise as a

result of interactions between species, these kinds of indicators tend to respond

relatively slowly to structural change. Instead of trying to propose values and limits

for indicators, Garcia and Staples (2000) propose focussing on how indicators can be

implemented in fisheries management to minimize the adverse effects of fishing.

There is currently much effort being put into development of “indicator dashboards”

that attempt to bring together information and management guidance based on

indicators derived from a variety of sources (Shin, 2006).

Ecological modelling is a key tool to monitor and quantify proposed indicators, as has

been illustrated by virtue of trophic models considered in this chapter. However,

models rely on sufficient high quality data, and the need for real time sampling

integrated at the level of ecosystem-based management of marine ecosystems has

been strongly recognized (Shannon et al., 2006).

6.2 Recommended exploitation rates

Managing fisheries by maintaining fishing mortality (Fmax) to achieve maximum

sustainable yield (MSY) is not necessarily applicable to small pelagic fisheries

because recruitment is likely to decline at such reduced stock sizes as those under

Fmax, leading to stock collapse (Patterson 1992). Patterson (1992) analysed 28 pelagic

fish stocks comprising 11 species, fitting a model to 10-year periods of fishing to

estimate the likelihood of stocks declining at different exploitation levels. For mature

fisheries and assuming that small pelagic fish stocks from temperate and tropical

systems behave in a similar way, Patterson (1992) estimated a 50% probability of

stock decline at an exploitation level (E=F/Z where F is fishing mortality and Z is

total mortality) of 0.4. On a decadal scale, he found E>0.5 to be associated with stock

decline whereas E<0.3 allowed stocks to recover.

Taking into account Patterson’s (1992) E=0.4 target reference point for pelagic fish,

and Clarke’s (1991) finding that target fishing mortality rate calculated on the basis of

life history parameters approximated natural mortality (i.e. E=0.5), Rochet and

Trenkel (2003), in their review of community indicators that measure the impacts of

fishing, considered E=0.5 to be the limit reference point above which stocks should be

considered over-exploited. Mertz and Myers (1998) presented a simplified

formulation for calculating fish production, showing that yield/production is

approximated by F/Z. The authors showed that it is possible to harvest half the virgin

production of a fish stock under certain conditions e.g. that juveniles are not fished

(which is not the case in many small pelagic fisheries such as the Cape anchovy

recruit fishery off South Africa, the anchovy and common sardine fishery off central

Chile or Mediterranean fisheries). Mertz and Myers (1998) calculated E across a

broad range of taxa and found E=0.8 for piscivorous fish (largely groundfish), E=0.5

for prey species.

In the Northern Benguela Fs rose to high levels between the 1970s and 1980s (Cury et

al. in prep) and have decreased since as a result of the collapsed ecosystem in the late

1990s. In the Southern Benguela, decadal average exploitation rates from trophic

models all fell below 0.5, with small pelagic Es less than 0.3 over the last few decades

(Fig. 9a, Cury et al., in prep.). This is in agreement with Fairweather et al’s (2006)

findings. From acoustic survey abundance estimates (since 1984), catch records and

trophic model estimates of total mortality Z, the authors were able to calculate E for

sardine from 1984 to 2005, finding that sardine E generally fell well below the 0.4

target reference point and concluding that the indicator reflects successful sardine

fishery management. In the Northern Benguela, exploitation rates of anchovy, sardine,

and horse mackerel are notably higher than in the Southern Benguela, although Es fell

below 0.32 for anchovy and sardine. In the case of the South Catalan Sea, the

exploitation rate for sardine was higher than the maximum 0.5 recommended for

small pelagic fish during both 1978 and 1990s, and in fact there has been a decline

reported for sardine catches and biomass in this area (Palomera et al., in press), while

anchovy values for both Catalan and Adriatic Sea were also high (E>0.3).

In Central Chile, the stocks of common sardine and anchovy have been decreasing,

especially common sardine, since early 2000s. The highest landing for this species in

last 15 years was found in 1999 with >900 thousand tonnes of common sardine and

>700 thousand tonnes of anchovy. Landing for these species has decreased since then.

Fishing mortality (landing/total biomass) for these species was around 0.3 year-1

during the most of the 1990s, except for years 1999 and 2000 when F was >0.6 year-1.

Since then, F has returned to the levels found during the 1990s.

The two major drivers of fluctuations and collapses in small pelagic fish stocks, and

thus, by virtue of their wasp-waist role in the food web, the propagation of these

effects up and down the food web, are i) climatic effects on small pelagic fish, and ii)

fishing effects on small pelagic fish. The three models fitted to time series data and

discussed above (section 5.1) all illustrated the importance of considering the often

synergistic effects of the environment and fishing. Interactions between the

environment and marine resources can be synergistic or antagonistic, and van der

Lingen et al. (2006) point out that a change in the structure of an ecosystem is likely

to result in a change in the response of the ecosystem to environmental forcing.

In the face of severe environmental perturbations, it may simply not be sufficient to

ensure exploitation rates are well below critical levels. According to the guidelines

discussed above in terms of exploitation rates (Fig. 9), the Northern Benguela would

not have been classified as over exploited in the 1980s, despite the collapse of the

small pelagic fishery in the 1990s, pointing to the importance of taking into account

synergistic effects of environmental conditions and fishing pressure. Sardine in the

Catalan Sea would rightfully be considered overexploited in the 1990s (Lleonart and

Maynou, 2003), whereas in the Adriatic, exploitation rates of small pelagic fish

appear to have been within sustainable levels but large stock declines were observed

at the end of 1980s (Azzali et al., 2002; Santojanni et al, 2003, 2005).

6.3. Disruption of trophic pathways

Monitoring of pelagic:demersal fish biomass ratios over time shows the general trend

in recent decades to have been a shift towards more demersally-dominated

ecosystems (Fig. 3) as pelagic fisheries have expanded and small pelagic fish stocks

have undergone large declines. Proliferation of non-commercial species such as

jellyfish, and changes in diet and populations of predators in ecosystems where small

pelagic fish are heavily exploited could be seen as signs of disruption of the trophic

structure. Snapshot model results and dynamic model simulations of severely altered

fishing on small pelagic fish in the different ecosystems examined support these

hypotheses. Changes in energy transfer can be quantified in terms of increased energy

flowing to detritus when pelagic fish are heavily exploited (see sections 4.5) and a

higher coupling between pelagic and demersal compartments (sections 4.6 and 5.5).

No important changes were found in the Southern Humboldt models in terms of the

impact of the detritus on the pelagic and demersal components. This could be likely

attributed to a decrease in the biomass of the demersal fish (i.e. hake) and benthic

detritivorous crustaceans in recent years, and thus full advantage is not being taken of

the observed increased flow to detritus. On the other hand, large increases in the

summed mixed trophic impacts of detritus on both the pelagic and demersal food

webs were observed over time in the Southern Benguela, and small increases were

observed in the South Catalan Sea, further supporting the hypothesis that detritus can

become increasingly more important as ecosystems are fished and/or degraded.

However, in the Northern Benguela, the near-total collapse of the pelagic ecosystem

has weakened detritus-pelagic food web linkages, whereas detritus-demersal linkages

have strengthened. The dominant small pelagic fish is now the non-commercial

bearded goby Sufflogobius bibarbatus, which, by virtue of being able to feed

benthically as well as pelagically, appears to have been able to survive the frequent

low oxygen events that have been detrimental to the pelagic food web off the coast of

Namibia. In the Adriatic, the decline in the impact of detritus on the demersal

compartment could be due to the high rates of exploitation of commercial scallops

and other invertebrates after the decrease of fish catches (Coll et al. 2007) and the

lower biomasses of these groups in the ecosystem during the 1990s compared to the

1980s.

Comparison of snapshot models also suggests an increase in the pelagic-benthic

coupling through stronger overall mixed trophic interactions of the pelagic component

on the demersal component in more recent periods (usually when fishing has

increased), and often reduced summed impacts of the demersal compartment on the

pelagic food web (sections 4.6 and 5.5). Although this needs further investigation and

more careful quantification, and recognizing that results would depend on whether

certain omnivorous groups are categorised as pelagic or demersal, changes in flows

between benthic and pelagic compartments may be considered a measure of the

impacts of fishing.

Figure captions:

Fig. 1: Number of species (on a logarithmic scale) in the Southern Humboldt and

Southern Benguela in the main taxa represented in these ecosystems, to show the

wasp-waist at the level of small pelagic fish.

Fig. 2: Schematic plot showing expected changes across different trophic levels when

the typical wasp-waist ecosystem is disrupted by fishing.

Fig. 3 Ratios of pelagic:demersal fish in catches in a) the Benguela, b) the Southern

Humboldt, c) South Catalan Sea and North and Central Adriatic Sea. Figures aii) and

bii) show pelagic:demersal biomass ratios from research surveys for the Southern

Benguela and Southern Humboldt respectively. The ratio of demersal:total fish in

catches in the Northern Benguela is plotted in Fig. 3a (iiii).

Fig. 4 i) Trophic level (TL) of the catch and ii) Fishing in balance (FiB) index

calculated from catches in the a) Southern and Northern Benguela (after Cury et al.,

2005a; van der Lingen et al., 2006), b) Southern Humboldt (plotted with and without

horse mackerel, see text for reason), and c) South Catalan Sea and North and Central

Adriatic Sea.

Fig. 5 i) Simulation 1: closure of the purse seine fishery i) Projected modelled

biomass trajectories (biomass plotted relative to biomass at start of simulation) and ii)

ratio of the biomasses of small pelagic fish to demersal fish (including hake), for the

a) Southern Benguela (small pelagic fish include anchovy, sardine, round herring and

other small pelagic fish), b) Southern Humboldt (small pelagic fish include only

anchovy and sardine), c) South Catalan Sea (small pelagic fish include anchovy,

sardine and other small pelagic fish), and d) North and Central Adriatic (small pelagic

fish include anchovy, sardine and other small pelagic fish).

Fig. 6 Simulation 2: collapse of the purse seine fishery i) Projected modelled

biomass trajectories (biomass plotted relative to biomass at start of simulation) and ii)

ratio of the biomasses of small pelagic fish to demersal fish (including hake), for the

a) Southern Benguela (small pelagic fish include anchovy, sardine, round herring and

other small pelagic fish), b) Southern Humboldt (small pelagic fish includes only

anchovy and sardine), c) South Catalan Sea (small pelagic fish include anchovy,

sardine and other small pelagic fish), and d) North and Central Adriatic (small pelagic

fish include anchovy, sardine and other small pelagic fish).

Fig. 7 Modelled catch:biomass ratios (equivalent to fishing mortality, F) for anchovy,

sardine and all the main small pelagic fish in a) Southern and Northern Benguela, b)

Southern Humboldt, and c) South Catalan Sea, and North and Central Adriatic.

Fig. 8 Estimated predation mortality rates of small pelagic fish in a) Southern

Benguela, b) Southern Humboldt and c) South Catalan Sea and (from models fitted to

time series data).

Fig. 9 Exploitation rates (E=F/Z) for main fish species in the a) Southern Benguela,

and b) Northern Benguela, estimated using models for three periods in each system; c)

Northern Humboldt, estimated using models of three periods; d) South Catalan,

estimated using a model for 1978 (blue) and the 1990s (red); and e) North and Central

Adriatic Sea, estimated using a model for the 1980s (blue) and the 1990s (red).

Fig. 10 Estimated biomass trajectories (t.km-2.y-1) of main groups from a) Southern

Benguela trophic model fitted to time series data (Shannon et al., 2004), b) Southern

Humboldt trophic model fitted to time series data (Neira et al., in prep.), and c) South

Catalan trophic model fitted to time series data (Coll et al., in prep.). Because the

relative increase in sardine in the Southern Benguela was so large, the plot including

sardine is presented as an insert in Fig. 10 a. For the South Catalan Sea, species are

grouped according to their scale of relative biomass change over time in Fig. 10 c.

Fig. 11 Sum of all modelled flows to detritus in different periods for the a) Southern

and Northern Benguela, b) Southern Humboldt, and c) South Catalan Sea, and North

and Central Adriatic Sea.

Acknowledgements

Authors would like to thank all researchers involved in ecological models used in this

work: Isabel Palmera, Enrico Arneri, Alberto Santojanni, Sergi Tudela, and Frances

Sardà (South Catalan Sea and North and Central Adriatic Sea), Astrid Jarre and

Coleen Moloney (Southern Benguela upwelling), Hugo Arancibia and Luis Cubillos

(Southern Humboldt upwelling).

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Following is to be placed in a ‘box’ separate from the text:

Quick look at Ecopath with Ecosim (EwE)! • ECOPATH

Mass balance Ecopath models provide a quantitative representation, or snapshots, of marine ecosystems in terms of trophic flows and biomasses for a defined time period, usually a year. Model parameters are expressed in terms of nutrient or energy related currency per unit of surface (frequently expressed as t·km-2·yr-1 for fisheries applications) (Pauly et al. 2000, Christensen and Walters 2004).

The ecosystem is represented by functional groups, which can be composed of species, groups of species with ecological similarities or ontogenetic fractions of a species. The model is based on two linear equations that represent the energy balance among groups (production equation) and the energy balance within a group (consumption equation). For each group, the model describes a mass balance situation, where the energy removed from the ecosystem due to, for example, predation or fishing, is balanced by consumption.

(1) The production (P) of each functional group (i) is divided into predation mortality (M2ij) caused by the biomass of the other predators (Bj), exports from the system via fishing activity (Yi) and other exports (Ei), biomass accumulation in the ecosystem (BAi) and a baseline mortality or other mortality (1-EEi), where EE is the ecotrophic efficiency, or the proportion of the production of group (i) that is exported out of the ecosystem (e.g. by fishing) or consumed by predators:

∑ −++++=j

iiiiiijji EE1PBAEY2MBP )·(·

(1)

(2) The energy balance within each group is then ensured when consumption by group (i) equals the sum of production by (i), respiration by (i) and food that is unassimilated by (i).

Ecological analyses integrated in Ecopath can be used to examine many ecosystem features based on trophic flows and network analyses, thermodynamic concepts and information theory (Christensen and Walters, 2004; Cury et al., 2005).

• ECOSIM

The trophodynamic simulation module Ecosim (Walters et al., 1997) re-expresses the linear equations of the Ecopath model as difference and differential equations that dynamically respond to changes in fishing mortality and biomass. This enables the performance of dynamic simulations at the ecosystem level from the initial parameters of a baseline Ecopath model as follow:

( ) iiiiijii

i BeFMIQijQQP

dtdB

⋅++−+−⋅⎟⎟⎠

⎞⎜⎜⎝

⎛= ∑∑

(2)

where dBi/dt is the growth rate of (i) during the time interval dt in terms of Bi, (P/Q)i is the gross efficiency, Mi is the non-predation natural mortality rate, Fi is the fishing mortality rate, ei is the emigration rate, Ii is the immigration rate, and ei · Bi –Ii is the net migration rate. Consumption rates (Q) are calculated based upon the “foraging arena” theory where the biomass of (i) is divided into a vulnerable and a non-vulnerable fraction and the transfer rate υ between the two fractions is what determines the flow control (Walters et al. 1997, Christensen and Walters 2004). Default values of υ represent mixed flow control, whilst these values can be modified to represent bottom-up flow control and top-down flow control.