e c o l o g i c a l m o d e l l i n g 1 9 8 ( 2 0 0 6 ) 53–70

avai lab le at www.sc iencedi rec t .com

journa l homepage: www.e lsev ier .com/ locate /eco lmodel

Comparing trophic flows and fishing impacts of a NWMediterranean ecosystem with coastal upwelling systemsby means of standardized models and indicators

Marta Coll a,∗, Lynne J. Shannonb, Coleen L. Moloneyc,Isabel Palomeraa, Sergi Tudelad

a Institute of Marine Science (CMIMA-CSIC), Passeig Marıtim de la Barceloneta 37-49, 08003 Barcelona, Spainb Marine and Coastal Management, Private Bag X2, Rogge Bay 8012, Cape Town, South Africac Marine Biology Research Institute, Zoology Department, University of Cape Town, Rondebosch 7701, Cape Town, South Africad WWF Mediterranean Programme Office, Canuda 37, 08002 Barcelona, Spain

a r t i c l e i n f o

Article history:

Received 1 April 2005

Received in revised form 6 April

2006

Accepted 12 April 2006

Published on line 13 June 2006

Keywords:

Mediterranean

Upwelling ecosystems

Ecological modelling

Trophic flows

Ecosystem indicators

Fishing impact

a b s t r a c t

The NW Mediterranean has a number of structural features in common with upwelling

ecosystems. Therefore, an ecological model representing a NW Mediterranean exploited

ecosystem was standardized and compared with four previously standardized models

from coastal upwelling ecosystems: the Northern and Southern Humboldt (Chile and Peru

upwelling systems) and the Northern and Southern Benguela (Namibia and South Africa

upwelling systems). Results from biomasses, flows and trophic levels indicated important

differences between ecosystems, mainly caused by differences in primary production, which

was smallest in the NW Mediterranean Sea. However, principal component analysis (PCA)

of biomasses and flows suggested a similar pattern between the NW Mediterranean and the

South African systems due to the inclusion of an important fraction of the continental shelf

in both ecological models representing these areas. At the same time, diets of commercial

species from the NW Mediterranean were more similar to Benguela than Humboldt species.

However, the relatively heavy fishing pressure in the NW Mediterranean ecosystem was

highlighted relative to its primary production, and was evident from the large catches and

small primary production, largest flows from TL 1 required to sustain the fishery (%PPR),

the low trophic level of the catch (TLc), high exploitation rates (F/Z), largest values in the

trophic spectra portraying catch: biomass ratio, the FIB index and the demersal: total catch

ration. Comparisons of %PPR, the trophic level of the community (TLco), the biomass of

consumers and F/Z ratios seemed to capture the ecosystem effects of fishing: large in the

NW Mediterranean, Namibia and Peru upwelling systems. Small pelagic fish were the most

important component of the fisheries in the NW Mediterranean and Peruvian systems.

However, the smaller production and biomass ratios from the NW Mediterranean could

be an indirect indicator of intense fishing pressure on small pelagic fish, also in line with

0d

results from consumption of small pelagic fish by the fishery, F/Z ratios and trophic spectra.

Moreover, similarities bet

mainly related to the dem

zooplankton in the consu

∗ Corresponding author. Tel.: +34 93 230 95 43.E-mail address: mcoll@icm.csic.es (M. Coll).

304-3800/$ – see front matter © 2006 Elsevier B.V. All rights reserved.oi:10.1016/j.ecolmodel.2006.04.009

ween the NW Mediterranean and Namibian systems were found,

ersal: total catch ratios, the FIB index, the relevance of gelatinous

mption of production and the importance of pelagic-demersal

54 e c o l o g i c a l m o d e l l i n g 1 9 8 ( 2 0 0 6 ) 53–70

coupling, in remarkable contrast to the other ecosystems. These similarities should be inter-

preted in terms of dynamic trajectories that the Namibian system has shown due to the

collapse of its pelagic ecosystem, partly due to fishing intensity, and the signs that the NW

follow suit in the future.

Mediterranean could

1. Introduction

1.1. The NW Mediterranean Sea ecosystem

The Mediterranean region has been inhabited for millenniaand human settlements have been spreading continuouslyalong its coastal areas (Margalef, 1985). As a consequence,marine ecosystems of the Mediterranean have been alteredin many ways over the centuries (Bianchi and Morri, 2000;Papaconstantinou and Farrugio, 2000). Fishing activity hasbeen proposed as the first major human disturbance to coastalareas (Jackson et al., 2001) and evidence of fishing activitygoing back to ancient times can be found throughout theMediterranean Sea (Bas et al., 1985). Moreover, the develop-ment of fishing technologies and overcapitalization in recentdecades, with an increasing demand for marine resources,is placing intensive pressure on the exploited ecosystem.The current assessment from the NW Mediterranean sug-gests that demersal stocks are fully exploited or overexploited,whilst some pelagic stocks also show signs of overexploitation(Farrugio et al., 1993; Papaconstantinou and Farrugio, 2000; Baset al., 2003; Lleonart and Maynou, 2003; Lleonart, 2005).

In order to describe the structure and functioning of a rel-atively productive exploited ecosystem from the NW Mediter-ranean and assess the ecosystem effects of fishing, an Eco-path mass-balanced model (Pauly et al., 2000; Christensen andWalters, 2004) was constructed. The model represents the con-tinental shelf and upper slope area associated with the EbroRiver Delta (South Catalan Sea, NW Mediterranean) (Coll et al.,2005) in 1994, when official landings were at their highest levelsince the 1970s. Results from the ecological model showedthat the ecosystem was dominated by the pelagic compart-ment, with which main flows and biomasses were associated.Small pelagic fish, mainly European sardine (Sardina pilchardus)and European anchovy (Engraulis encrasicolus), were identifiedas important components of the ecosystem, dominating thepelagic fraction in terms of biomasses and catches. A calibra-tion process of the model with available time series of data(Coll et al., 2006) suggested that sardine would be involvedin wasp-waist trophic control situations (as defined by Rice,1995 and Cury et al., 2000). Moreover, European hake (Merluc-cius merluccius) and medium-sized pelagic fish (mainly horsemackerel Trachurus spp. and mackerel Scomber spp.) were alsoimportant in terms of biomasses and trophic interactions. Themodel also showed that the NW Mediterranean ecosystemwas highly impacted by fishing activity.

The studied NW Mediterranean ecosystem had a numberof structural features in common with upwelling ecosystems,

more so than with other known ecosystems that have beenmodelled (e.g. Christensen and Pauly, 1993; Jarre-Teichman,1998; Cury et al., 2000; Shannon et al., 2003; Heymans etal., 2004; Sanchez and Olaso, 2004). These features include

© 2006 Elsevier B.V. All rights reserved.

the dominance of the pelagic compartment, the importanceof small pelagic fish in terms of catch and biomass andtheir implication for wasp-waist flow control situations, thekey role of other pelagic fish, such as horse mackerel, theimportance of hake and the low development stage of theecosystem sensu Odum (1969) (Christensen, 1995). Moreover,oceanographic conditions and local upwelling events in theNW Mediterranean, mainly related to wind conditions, ver-tical mixing and stratification of water, fresh water inputs,shelf-slope exchanges and density fronts (Estrada, 1996; Salat,1996; Agostini and Bakun, 2002), greatly influence the produc-tivity and fishing activity in the area. Nutrient enrichmentand relatively high concentrations of small pelagic fish occur(Palomera, 1992; Estrada, 1996; Sabates and Olivar, 1996; Salat,1996; Lloret et al., 2004).

1.2. Comparing ecosystem models

The Ecopath with Ecosim approach (EwE) has been widelyused to quantitatively improve the knowledge on struc-ture and functioning of different marine ecosystems and, byanalysing ecological indicators provided directly from thesemodels, it has been possible to contextualize the fishingimpact and quantify its ecosystem effects (e.g. Christensenand Pauly, 1993; Christensen, 1995; Roux and Shannon, 2004;Sanchez and Olaso, 2004). In addition, this methodology hasbeen intensively applied to upwelling regions, enabling theimprovement of descriptions of ecosystem functioning and ofthe importance of fishing activities and environmental fac-tors in ecosystem dynamics (e.g. Jarre-Teichmann et al., 1998;Heymans et al., 2004; Shannon and Cury, 2003; Neira andArancibia, 2004; Shannon et al., 2004a,b).

Among the analyses of exploited ecosystems undertakenusing the EwE approach, the comparison of ecological modelsrepresenting different situations of a given ecosystem throughtime has been shown to be a useful exercise (e.g. Libralato etal., 2002; Shannon et al., 2003; Heymans et al., 2004; Neira etal., 2004). Furthermore, by standardizing models of differentecosystems to achieve a common structure separating bio-logical features from modelling artefacts, these comparisonshave been successfully applied to four different upwellingecosystems of the Humboldt and Benguela. These models rep-resented different areas and periods (Moloney et al., 2005):the Southern Humboldt upwelling ecosystem (Chilean sys-tem), the Northern Humboldt upwelling ecosystem (Peruviansystem), the Southern Benguela upwelling ecosystem (SouthAfrican system) and the Northern Benguela upwelling ecosys-tem (Namibian system).

In this study, and because of the similarities found betweenthe NW Mediterranean and upwelling ecosystems, the avail-able ecological model from the South Catalan Sea, NWMediterranean, was reformulated to conform to the same

n g

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tandardized model as used for the upwelling ecosystemsnd compared with those models presented in Moloney et al.2005). This comparison is especially relevant in the case of the

editerranean Sea, where there are few available time seriesf data and where ecological modelling of exploited ecosys-ems it is still scarce (e.g. Libralato et al., 2002; Pinnegar andolunin, 2004; Coll et al., 2005).

The principal aims of the comparison were: (a) to assessifferences and similarities in the structure and functioningf the NW Mediterranean ecosystem and the four upwellingystems related to their intrinsic features and exploitation his-ory; (b) to analyse the trophic information and ecological rolesf common important species in terms of biomasses, trophic

nformation and consumption; (c) to compare a selected groupf ecological indicators to assess differences in the ecosystem

mpacts of fishing.Taking into account the exploitation history of the five

cosystems, selected indicators were analysed to test thenitial hypothesis that the NW Mediterranean model woulde ranked within the high impacted areas of the Namibiannd Peruvian systems, which were differentiated in terms ofcosystem impact from the moderately impacted regions ofhe Chilean and South African systems (Moloney et al., 2005).

. Methods

.1. Ecological models and standardization process

he standardized upwelling models in Moloney et al. (2005)rom the Humboldt and Benguela ecosystems represented

Table 1 – Input and output parameters of the standardized Ecop

Functional groups B P/B

Phytoplankton 10.20 37.91Microzooplankton 2.10 24.18Mesozooplankton 7.79 20.87Macrozooplankton 0.54 20.41Gelatinous zooplankton 0.39 25.00Macrobenthos 24.71 1.55European anchovy 2.64 1.33Special small pelagic 3.58 1.50Benthopelagic fishes 0.22 1.37Cephalopods 0.41 2.18Other small pelagics 0.92 0.52Horse mackerel 1.55 0.39Characteristic large pelagics 0.61 0.46Tunas and swordfish 0.40 0.37Juvenile hake 0.04 1.30Adult hake 0.35 0.60Demersal benthic feeders 0.73 1.33Demersal pelagic feeders 1.37 0.67Demersal chondrichthyans 0.06 0.42Seabirds 0.002 4.60Marine turtles 0.03 0.15Cetaceans 0.39 0.04Detritus + discards 70.38 –

B = biomass (t km−2); P/B = production/biomass ratio; Q/B = consumptionTL = trophic level.

1 9 8 ( 2 0 0 6 ) 53–70 55

the Chilean system in 1992 (Neira and Arancibia, 2004),the Peruvian system in 1973–1981 (Jarre-Teichmann et al.,1998), the South African system in 1980–1989 (Shannon etal., 2003) and the Namibian system in 1995–2000 (Roux andShannon, 2004). These models represent exploited ecosys-tems from where information on temporal dynamics oftheir marine resources is available (e.g. Neira et al., 2004;Heymans, 2004; Heymans et al., 2004; Shannon et al., 2003,2004a,b).

The model of the Chilean system (1992) represented theecosystem under a moderate ENSO event, where main fishstocks were described as not fully exploited and the ecosystemwas dominated by medium-sized pelagic fish (mainly Pacificjack mackerel Trachurus symmetricus and hoki Macruronusmagellanicus), with medium to high abundance of small-sized pelagic fish (common sardine Strangomera bentincki andanchovy Engraulis ringens) and Chilean hake (Merluccius gayi)(Neira and Arancibia, 2004). The model of the Peruvian sys-tem (1973–1981) represented the period following the collapseof the anchoveta (E. ringens) fishery, when sardine (Sardinopssagax) biomass was increasing and no major ENSO eventswere recorded (Jarre-Teichmann et al., 1998). The model of theSouth African system (1980–1989) represented a period whenthe ecosystem was dominated by Cape anchovy (E. encrasi-colus) with reduced biomass of sardine (S. sagax), and whenstocks of round herring or redeye (Etrumeus whiteheadi), horsemackerel (Trachurus trachurus capensis) and Cape hakes (Mer-

luccius capensis and M. paradoxus) were believed to be healthy,whilst the pelagic resources were well utilized (Shannon et al.,2003). The model of the Namibian system (1995–2000) repre-sented a period in which pelagic gobies (Sufflogobius bibarba-

ath model for the NW Mediterranean ecosystem (1994)

Q/B Catch EE TL

– 0.94 1.0073.24 – 0.95 2.0548.85 – 0.76 2.1550.94 – 0.91 2.8450.48 – 0.12 2.908.53 0.22 0.36 2.01

13.91 0.94 0.96 3.158.86 2.83 0.97 3.069.03 0.07 0.97 3.55

15.63 0.27 0.97 3.617.39 0.01 0.98 3.095.13 0.02 0.30 3.274.88 0.05 0.51 3.623.52 0.05 0.34 4.167.37 0.02 0.98 3.362.52 0.21 0.98 4.166.66 0.44 0.98 3.145.86 0.22 0.97 3.525.43 0.01 0.90 3.75

71.58 0.0001 0.18 2.952.54 0.0006 0.12 2.544.73 0.002 0.10 4.03– – 0.77 1.00

/biomass ratio; catch (t km−2 year−1); EE = ecotrophic efficiency;

56e

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lo

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al

mo

de

ll

ing

19

8(2

00

6)

53–70

Table 2 – Diet composition matrix of the standardized Ecopath model for the NW Mediterranean ecosystem (1994) (predators are located by columns, prey by rows)

2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22

1 Phytoplankton 0.700 0.650 0.150 0.100 0.076 0.0522 Microzooplankton 0.050 0.090 0.050 0.050 0.001 0.050 0.066 0.010 0.010 0.0103 Mesozooplankton 0.050 0.600 0.650 0.001 1.000 0.874 0.248 0.926 0.687 0.269 0.0274 Macrozooplankton 0.050 0.001 0.611 0.165 0.618 0.001 0.011 0.006 0.006 0.406 0.142 0.002 0.3735 Gelatinous zooplankton 0.050 0.038 0.0136 Macrobenthos 0.006 0.075 0.479 0.012 0.114 0.049 0.002 0.751 0.015 0.844 0.450 0.424 0.294 0.0017 European anchovy 0.264 0.018 0.092 0.002 0.044 0.104 0.077 0.0368 Special small pelagic 0.176 0.049 0.198 0.566 0.001 0.038 0.156 0.0019 Benthopelagic fishes 0.002 0.005 0.141 0.53 0.005 0.006 0.063 0.01010 Cephalopods 0.045 0.003 0.020 0.001 0.010 0.152 0.003 0.07411 Other small pelagics 0.001 0.215 0.001 0.003 0.067 0.05912 Horse mackerel 0.009 0.066 0.011 0.002 0.00113 Characteristic large pelagics 0.06314 Tunas and swordfish15 Juvenile hake 0.013 0.004 0.00116 Adult hake17 Demersal benthic feeders 0.005 0.002 0.059 0.153 0.039 0.012 0.021 0.00518 Demersal pelagic feeders 0.022 0.001 0.037 0.128 0.013 0.030 0.093 0.03219 Demersal chondrichthyans 0.00220 Seabirds 0.01021 Marine turtles22 Cetaceans23 Detritus + discards 0.250 0.210 0.150 0.150 0.992 0.002 0.010 0.002 0.371 0.29324 Import 0.400 0.312 0.400 0.406

Total 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0

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od

el

lin

g1

98

(20

06

)53–70

57

Table 3 – Comparative trophic regimes of small and medium-sized pelagic fish and hake species for the five models

Chile Peru South Africa Namibia NW Mediterranean

Anchovy Engraulis ringens:Phytoplankton (TL = 2.1)

Engraulis ringens:Phytoplankton,mesozooplankton (TL = 2.7)

Engraulis encrasicolus:Mesozooplankton,macrozooplankton(TL = 3.54)

Engraulis encrasicolus:Phytoplankton, meso- andmacrozooplankton (TL = 3.0)

Engraulis encrasicolus:Mesozooplankton,macrozooplankton (TL = 3.15)

Sardine Sardinops sagax:Mesozooplankton,phytoplankton (TL = 3.2)

Sardinops sagax:Phytoplankton, micro- andmesozooplankton(TL = 2.99)

Sardinops sagax:Phytoplankton, meso- andmacrozooplankton (TL = 2.7)

Special small pelagic Strangomera bentincki:Phytoplankton (TL = 2.1)

Etrumeus whiteheadi:Mesozooplankton,macrozooplankton(TL = 3.64)

Sufflogobius bibarbatus:Macrozooplankton,macrobenthos,mesozooplankton (TL = 3.2)

Sardina pilchardus:Mesozooplankton,phytoplankton (TL = 3.6)

Horse mackerel Trachurus symmetricus:Macrozooplankton (TL = 4)

Trachurus murphyi: Anchovy,macrozooplankton (TL = 3.7)

Trachurus t. capensis:Macrozooplankton,mesozooplankton, smallpelagics (TL = 3.72)

Trachurus t. capensis:Macrozooplankton,mesozooplankton,macrobenthos (TL = 3.6)

Trachurus spp.:Meso- and macrozooplankton,macrobenthos, small pelagics(TL = 3.27)

Characteristhic largepelagic

Macruronus magellanicus:Macrozooplankton,mesozooplankton (TL = 4.2)

Scomber japonicus:Macrozooplankton,anchovy (TL = 3.7)

Scomber scombrus:Macrozooplankton,mesopelagic fishes (TL = 3.8)

Scomber spp.:Macro- and mesozooplankton,small pelagics, macrobenthos(TL = 3.55

Adult hake (1) Merluccius gayi: Smallpelagics, juv. hake,macrobenthos (TL = 3.5)

Merluccius gayi: Smallpelagics, Macrozooplankton(TL = 4.0)

Merluccius capensis:Medium-sized pelagics, juv.hake (1–2), small pelagics,macrozooplankton(TL = 4.66)

Merluccius capensis: Smallpelagics, medium-sizedpelagics, juv. hake (1),macrozooplankton (TL = 4.5)

Merluccius merluccius: Smallpelagics, mesopelagics,demersal fishes (TL = 4.10)

Adult hake (2) Merluccius paradoxus:mesopelagics,macrozooplankton, juv.hake (2), cephalopods(TL = 4.49)

Merluccius paradoxus:Macrozooplankton,mesopelagics, smallpelagics (TL = 4.3)

Juvenile hake Merluccius gayi: Smallpelagics, juv. hake (1),macrobenthos (TL = 3.4)

Merluccius gayi:Macrozooplankton, smallpelagics, mesozooplankton(TL = 3.7)

M. paradoxus and capensis:Macrozooplankton,mesopelagics, smallpelagics (TL = 3.9 – 4.0)

Merluccius capensis: Smallpelagics, macrozo oplankton (TL = 4.03)

Merluccius merluccius:Macrobenthos, mesopelagics,small demersal fishes(TL = 3.45)

l i n g

58 e c o l o g i c a l m o d e l

tus), jellyfish (mainly Chrysaora sp.) and horse mackerel (Tra-churus t. capensis) dominated the ecosystem and sardine (S.sagax) and anchovy (E. encrasicolus) were at low biomass levelsafter the collapse of pelagic fisheries (1960–1970s) (Roux andShannon, 2004).

The ecological model representing the 1994 annual sit-uation of the continental shelf and upper slope ecosystemof the South Catalan Sea, NW Mediterranean (Coll et al.,2005) was standardized following the generic model struc-ture proposed by Moloney et al. (2005). The standardiza-tion process required aggregation of the initial 40 func-tional groups and splitting of the initially combined micro-

and mesozooplankton group into two groups according todata from Calbet et al. (2001). New data of P/B and Q/Bratios for zooplankton were adapted from Sanchez and Olaso(2004), whilst trophic information was modified to account

Fig. 1 – Integrated biomass and flows for the five models: (a) totaexcluding detritus and all plankton groups (t km−2); (c) primary pexcluding all plankton groups (t km−2 year−1); (e) total consumptcatches (t km−2 year−1). Values from the NW Mediterranean are h

1 9 8 ( 2 0 0 6 ) 53–70

for the split zooplankton groups (Demirhindi, 1961; Bell andHarmelin-Vivien, 1983; Ben Salem, 1988; Tudela and Palomera,1997; Stergiou and Karpouzi, 2002). The resulting functionalgroups and the input parameters for the model are listed inTables 1 and 2.

The European sardine was allocated to the “special smallpelagic” group following the comparison criteria, the “othersmall pelagic fish” group included the bogue (Boops boops) andthe sardinella (Sardinella aurita), whilst the “characteristic largepelagic” group included the mackerel (Scomber scombrus and S.japonicus). Unlike the other four ecosystems previously exam-ined, three species were included within the horse mackerel

group: Trachurus trachurus, T. mediterraneus and T. picturatus.Atlantic bonito (Sarda sarda), swordfish (Xiphias gladius) andbluefin tuna (Thunnus thynnus) were included in the “tunas andswordfish” group.

l biomass, excluding detritus (t km−2); (b) total biomass,roducer standing stock (t km−2); (d) total production,

ion, excluding all plankton groups (t km−2 year−1); (f) totalighlighted.

e c o l o g i c a l m o d e l l i n g 1 9 8 ( 2 0 0 6 ) 53–70 59

Table 4 – Eigenvalues and cumulative percent varianceexplained by axes of the principal component analysis(PCA) from Figs. 1, 7, 11 and 13

Axes 1 2 3 4

PCA1 (Fig. 1)Eigenvalues proportion 0.62 0.31 0.06 0.003Cumulative % variance 62.5 93.8 99.7 100.0

PCA2 (Fig. 7)Eigenvalues proportion 0.72 0.19 0.07 0.03Cumulative % variance 71.8 90.6 97.5 100.0

PCA3 (Fig. 11)Eigenvalues proportion 0.42 0.29 0.25 0.05Cumulative % variance 41.7 70.6 95.2 100.0

2i

AsppMam

FbaT

PCA4 (Fig. 12)Eigenvalues proportion 0.33 0.28 0.22 0.17Cumulative % variance 33.05 61.5 83.4 100.0

.2. Comparison of trophic information and ecologicalndicators

fter standardization, diet information of small and mediumized pelagic fish and juvenile and adult hake were com-ared across ecosystems. The trophic behaviour of the Euro-ean anchovy and European hake is well known from the NW

editerranean Sea (Tudela and Palomera, 1997; Bozzano et

l., 1997, 2005), however the information on other small andedium-sized pelagic fish from this area is qualitative and

ig. 2 – Principal component analysis applied to integratediomass and flows for the five models (Fig. 1). Eigenvaluesnd percent variance explained by axes are shown inable 4.

Fig. 3 – Discrete trophic level spectra of biomass (t km−2) forthe five models.

outdated (Massutı and Oliver, 1948; Andreu and Rodriguez-Roda, 1951; Demirhindi, 1961; Bell and Harmelin-Vivien, 1983;Ben Salem, 1988). Therefore, the quantitative diet informa-tion used for the comparison was that from the mass-balancemodel for the NW Mediterranean Sea (Coll et al., 2005).

For various ecological groups, the trophic level (TL),which identifies the position of organisms in the food chain(Lindeman, 1942; Odum and Heald, 1975), was also analysed.By convention, primary producers and detritus have TL = 1;values for other groups are determined using mass-balancemodels, gut content analysis or isotope data (Stergiou andKarpouzi, 2002). The TL can be formulated as following:

TLj = 1 +n∑

i=1

DCjiTLi

where j is the predator of prey i, DCji the fraction of prey i inthe diet of predator j and TLi is the trophic level of prey i.

In addition, a similar procedure to that followed by Moloneyet al. (2005) was applied to compare various population andecosystem indicators derived from the NW Mediterraneanmodel with the four previously standardized models fromupwelling ecosystems (Rochet and Trenkel, 2003; Christensenand Walters, 2004; Cury et al., 2005; Moloney et al., 2005).Integrated biomasses and flows included in the comparisonwere total biomass (t km−2), excluding detritus and exclud-ing detritus and plankton groups to avoid assessment prob-lems, primary production (t km−2 year−1), total production(t km−2 year−1), total consumption (t km−2 year−1) and totalcatches (t km−2 year−1). Moreover, ratios of biomass, produc-tion and catch of small pelagics: large hake and large pelagics(Bsp/Blp, Psp/Plp, Csp/Clp), of planktivores: piscivores (Bpl/Bpc,Ppl/Ppc, Cpl/Cpc) and of planktivores: total consumers (Bpl/Bt,Ppl/Pt, Cpl/Ct) were analysed. At the same time, consumptionof total production (t km−2 year−1) by predator groups exclud-ing zooplankton and benthos, consumption of small pelagic

fish production (t km−2 year−1) by their predators (includingthe fishery) and total biomass (t km−2) per integer trophic levelwere also included in the comparison. For an overall interpre-tation of these results, principal component analyses (PCA)

l i n g 1 9 8 ( 2 0 0 6 ) 53–70

60 e c o l o g i c a l m o d e l

were performed on these data. Input data was centered andscaled by columns to give similar importance to all biomassesand flows. In addition, the trophic spectra for biomass, catchand the catch: biomass ratio following Gascuel et al. (2005)

Fig. 4 – Trophic spectra of (a) biomass; (b) catches; (c) catch:biomass ratios for the five models excluding the gelatinouszooplankton and macrobenthos groups.

Fig. 5 – Trophic level of the community TLco (excludingTL = 1) and total catches TLc.

Fig. 6 – Flows from TL 1 required to sustain the catches for

the five models in terms of flows (t km−2 year−1) and inpercentage. Data of the NW Mediterranean is highlighted.

was also analysed and compared between the five ecosystemmodels.

The average trophic level of the catch (TLc) and the aver-age trophic level of the community (TLco) excluding TL = 1were also included. The former reflects the strategy of a fish-ery in terms of food web components selected and is calcu-lated as the weighted average of the TL of harvested species(Pauly et al., 1998; Christensen and Walters, 2004), whilst thelater reflects the structure of the community and is calcu-lated as the weighted average of the TL of all the specieswithin the ecosystem (Rochet and Trenkel, 2003). Both indi-cators have been shown to decrease when fishing impactincreases because large predators are removed from ecosys-tems whilst lower trophic level organisms prevail (Pauly et al.,1998; Jennings et al., 2002; Pauly and Palomares, 2005).

In order to compare the ecological footprint of fishing

activities, the primary production and detritus (flows fromTL 1) required to sustain fisheries (PPR; typically expressedas t km−2 year−1) was included in the comparison. The PPR isobtained by back calculating the flows, expressed in primary

n g

pca1l

P

wppEdoittbiT

apfsf

Fcm

e c o l o g i c a l m o d e l l i

roduction and detritus equivalents, for all pathways from theaught species down to the primary producers and detritusnd increases with fishing intensity (Pauly and Christensen,995; Christensen and Walters, 2004). The PPR can be formu-ated as:

PR =∑paths

⎡⎣Yi

Pi×

∏j,i

Qj

Pj × EEj× DCj,i

⎤⎦

here Yi is the catch of a given group i, P the production ofredator j, Q the consumption of predator j, DC the diet com-osition of each predator j/prey i interaction in each path andE is the ecotrophic efficiency, or the proportion of the pro-uction that it is used within the system due to consumptionr is exported from the system (e.g. in terms of catches). This

ndex can also be expressed relative to the primary produc-ion and detritus of the ecosystem (%PPR). At the same time,he exploitation rates (F/Z, fishing mortality to total mortality)y ecological group were also considered. These indexs alsoncrease with fishing (Pauly and Christensen, 1995; Rochet andrenkel, 2003).

Finally, the demersal: total catch ratio, the Fishing in Bal-nce (FIB) index (Christensen, 2000; Pauly et al., 2000) and the

lot of TLc and total catch (Pauly et al., 1998) were calculatedor the NW Mediterranean case study from an available timeeries of catches (from 1976 to 2003) and compared resultsrom Benguela ecosystems (Cury et al., 2005). The catch series

ig. 7 – Ratios of small pelagic fish: large hake and large pelagiconsumers (excluding plankton, macrobenthos and detritus) forodels. Values for the NW Mediterranean are highlighted.

1 9 8 ( 2 0 0 6 ) 53–70 61

of the NW Mediterranean was obtained from the Institute ofMarine Science (CMIMA-CSIC, Barcelona, Spain) through thefishermen associations of the area and from the regional gov-ernment of Catalonia.

The FIB index is formulated as following:

FIB = log

[∑iYik10TLi∑

iYi010TLi

]

where Yik is the catch of species i during the year k, Yi0 thecatch of species i during the year at the start of a time seriesand which serves as an anchor and TLi is the trophic levelof species i. Values of FIB = 0 indicate that a decrease in thetrophic level of the catch is matched by an increase in catchbecause of higher production at low trophic levels. In contrast,when the FIB index increases (>0) this indicates that there isan expansion of the fishery or bottom-up effects occur. TheFIB index decreases (<0) when discarding occurs and is notconsidered in the analysis or when the fisheries impact onthe ecosystem is so high that its functioning is impaired (Paulyand Watson, 2005).

The demersal: total catch ratio informs of the origin ofcatches (whether they come from the demersal or the pelagic

habitat) and it can increase with fishing intensity (Rochetand Trenkel, 2003), although it has also been related to nutri-ent availability and eutrophication (De Leiva Moreno et al.,2000).

fish, of planktivores: piscivores and of planktivores: totalcatches (a–c), biomass (d–f) and production (g–i) for the five

l i n g 1 9 8 ( 2 0 0 6 ) 53–70

62 e c o l o g i c a l m o d e l

3. Results

3.1. Trophic information on key species

The principal prey groups of small and medium-sized pelagicfish and hake species from the different ecosystems are sum-marized in Table 3. European anchovy feed mainly on meso-zooplankton, being trophically more similar to Cape anchovyin the South African system, and to a lesser extent in theNamibian system, than to anchoveta in the Humboldt ecosys-tem, which feed mainly on phytoplankton. This was also inline with the trophic levels of anchovy in the different ecosys-tems (Table 3). The European sardine, feeding on micro- andmesozooplankton, and to lesser extent on phytoplankton, wastrophically similar to sardine and round herring in the SouthAfrican system and to sardine in the Peruvian systems, whilstsardine in the Namibian system and common sardine in theChilean one were considered to be more dependent on phyto-plankton.

Medium-sized pelagic fish in the NW Mediterranean Seashowed some trophic differences from upwelling ecosystems,where the TL of horse mackerel was the lowest (Table 3). Dif-ferences in trophic data of horse mackerel (Trachurus spp.)

Fig. 8 – Principal component analysis applied to catch,biomass and production rations of small pelagic fish: largehake and large pelagic fish, of planktivores: piscivores andof planktivores: total consumers (excluding plankton,macrobenthos and detritus) for the five models (Fig. 7).Eigenvalues and percent variance explained by axes areshown in Table 4.

Fig. 9 – Exploitation rates (F/Z) of (a) anchovy, Sardinops andthe special small pelagic and (b) adult hake and juvenilehake for the five models (see Table 3 for species scientific

name by ecosystem).

were mainly due to the higher intake of mesozooplanktonand the importance of macrobenthos in the NW Mediter-ranean diet, also observed to a lesser degree in the Namib-ian system, whereas the diet of horse mackerel in the otherecosystems examined consisted mainly of macrozooplank-ton. The trophic behaviour of mackerel (Scomber spp.) from theNW Mediterranean also showed some differences due to theoccurrence of macrobenthos in the diet of the Mediterraneangroup.

The diet of adult European hake was similar to hake inthe Namibian system and to a lesser extent in the Chileanone; however, lower rates of cannibalism were displayed. Thetrophic behaviour of juvenile European hake was differentfrom that in the upwelling systems, with some similaritiesto the Chilean species, because its main prey were macroben-thos and mesopelagic fish. Zooplankton and small pelagic fishwere more important in the diet of juvenile hake species in theother systems. Juvenile hake in upwelling areas are mainlypelagic-feeders and show high rates of cannibalism by adulthake (e.g. Payne et al., 1987; Punt and Leslie, 1995). The juvenileEuropean hake in the NW Mediterranean seems to under-

take nocturnal vertical movements through the water columnto prey on mesopelagic fish, whilst it preys on macroben-thos and small demersal fish during the day (Larraneta, 1970;Bozzano et al., 2005). The juvenile Cape hake have been found

n g

tcehrhb2ot

MHisecmdAot

Frdts

e c o l o g i c a l m o d e l l i

o remain high in the water column, possibly in order to avoidannibalism from adult hake (Pillar and Barange, 1995; Huset al., 1998). The vertical movements displayed by Europeanake cannot be explained by cannibalism because of the lowerates, although they could be related to the fact that juvenileake is escaping from other potential predators or could alsoe related to differences in prey availability (Bozzano et al.,005). However, it could be argued that the lower incidencesf cannibalism that are observed are due to the vertical migra-ion (successfully reducing cannibalism).

The TL of small pelagic fish and adult hake from the NWediterranean fell between those for these species in theumboldt and Benguela ecosystems (Table 3). However, diet

nformation and TLs of small and medium sized pelagic fishhowed more similarities with the Benguela than Humboldtcosystems. Moreover, these results emphasized the signifi-ance of pelagic-demersal coupling in the NW Mediterraneanodel, reflected by the importance of macrobenthos in the

iets of horse mackerel, mackerel and juvenile European hake.strong pelagic-demersal link has also been noted in the case

f the pelagic goby and horse mackerel in the Namibian sys-em (Roux and Shannon, 2004).

ig. 10 – (a) Fishing-in-balance and demersal: total catchatio (D/T); dotted lines indicate the seven fishing periodsiscussed in the text and (b) plot of mean trophic level ofhe catch and total catch for the NW Mediterranean casetudy (1976–2003).

1 9 8 ( 2 0 0 6 ) 53–70 63

3.2. Integrated biomasses, flows and trophic levels

The NW Mediterranean ecosystem was characterised bysmaller biomasses of consumers (t km−2, both excludingdetritus, and excluding detritus and plankton groups) thanHumboldt and Benguela ecosystems (Fig. 1(a) and (b)). TheNW Mediterranean also had the lowest primary production(t km−2 year−1), total production (t km−2 year−1) and total con-sumption (t km−2 year−1) that reflected the small dimensionsof the ecosystem in terms of flows per unit of area com-pared to upwelling ecosystems (Fig. 1(c–e)). However, the NWMediterranean showed the third highest catch (t km−2 year−1)of the comparison, higher than in the Benguela ecosys-tems (Fig. 1(f)). Results from principal component analysis(PCA) applied to this data showed that the NW Mediter-ranean pattern was similar to that of the South African sys-tem, even though the latter system showed higher flowsand biomasses (Fig. 2(a) and (b)). The high biomass of con-sumers from the Namibian system (excluding detritus andplankton groups) set this model apart from the rest, whichwas related to the benthic biomass necessary to sustain thetrophic requirements of the pelagic goby and could be a modelartefact (Moloney et al., 2005). The Peruvian and Chileansystems showed similar patterns but differ due to primaryproduction. Three factors explained 99.7% of the variance(Table 4).

Analyzing the ecosystem models in terms of biomass(t km−2) by discrete trophic levels (Fig. 3), it was also seen thatthe NW Mediterranean had the smallest biomasses per dis-crete trophic level (TL), where biomass of TL II was higherthan TL I, as in the Namibian and Peruvian systems. Thetrophic spectra by trophic levels II–V, excluding the gelatinouszooplankton and macrobenthos groups, are shown in Fig. 4;the NW Mediterranean biomass spectra being the smallest inamplitude of all the cases examined (Fig. 4(a)). Moreover, it issimilar to Chilean system with the exception being that theNW Mediterranean biomass spectrum lacked the marked sec-ond peak at TL 4 that resulted from characteristic large pelag-ics and large horse mackerel in the Chilean region. In addition,some similarities were found when comparing the trophicspectra of catches from the NW Mediterranean case studyand Benguela ecosystems, where the catch is mainly basedon organisms with TL 3 and TL 3.5, respectively (Fig. 4(b)).It is important to highlight the similar shape of the trophicspectrum of biomass and catch in the NW Mediterranean casestudy (as in the Peruvian system). This is related to the multi-specificity of the fishery, where fishing activity mainly targetsall that can be fished in the ecosystem (excluding plank-ton and benthic invertebrates) (Coll et al., 2005). The trophicspectra of catch: biomass ratios for the NW Mediterraneanshowed the highest values between TLs 3 and 3.7 (Fig. 4(c)).The two distinguished peaks within this range highlight theintense fishing pressure on organisms with TLs ≈ 3.1 (mainlysmall pelagic fish) and TL ≈ 3.5 (mainly demersal fish andcephalopods).

The mean trophic level of the community (TL ) exclud-

co

ing TL = 1 ranged from 2.40 to 3.08 and was smallest in theNW Mediterranean ecosystem, followed by the Namibian andPeruvian systems (Fig. 5). The mean trophic level of the catch(TLc) for the NW Mediterranean was higher than the values

l i n g

64 e c o l o g i c a l m o d e l

obtained for Humboldt ecosystems and lower than those inBenguela (Fig. 5).

Comparing the flows from TL = 1 required to sustainthe fishery (PPR) (Fig. 6) it was seen that the total flow(t km−2 year−1) was the smallest in the NW Mediterranean,whilst the percentage of the PPR (%PPR) was the high-est (39%), followed by the Peruvian and the Namibian sys-tems.

The importance of small pelagic fish in the NW Mediter-ranean and Peruvian systems can be observed from the anal-ysis of the catch ratio of small pelagics: adult hake andlarge pelagic fish (Csp/Clp), of planktivores: piscivorous fish(Cpl/Cpc) and of planktivores: total consumers (excl. plankton,

macrobenthos and detritus) (Cpl/Ct) (Fig. 7(a–c)). The biomassratio of small pelagics: adult hake and large pelagics (Bsp/Blp)and of planktivores: piscivores fish (Bpl/Bpc) was low in theNW Mediterranean and similar to the Chilean and Namibian

Fig. 11 – Main partitioning (%) of total consumption of productionfive models (a–e). Total consumption is reflected in the relative s

1 9 8 ( 2 0 0 6 ) 53–70

systems (Fig. 7(d) and (e)). On the other hand, the biomassratio of planktivores: total consumers (Bpl/Bt) was higher inthe NW Mediterranean than in the Peruvian and Namibiansystems, but lower than in the South African and Chileanupwellings (Fig. 7(f)). The production ratio of small pelagics:adult hake and large pelagic fish (Psp/Plp) and of planktivores:piscivores fish (Ppl/Ppc) was also low in the NW Mediterraneancase study, similar to the Namibian and Chilean systems(Fig. 7(g) and (h)), whilst the production ratio of planktivores:total consumers (Ppl/Pt) was higher than for the Benguelaecosystems but lower than those in the Humboldt ecosys-tems (Fig. 7(i)). Results from PCA applied to these indicatorsshow that NW Mediterranean pattern is similar to that of the

South African and Chilean systems, and to a lesser extendto the Namibian one, mainly due to similar values of Bpl/Bt

(Fig. 8(a) and (b)). Three factors explained 97.5% of the vari-ance (Table 4).

by predators (excluding zooplankton and benthos) for theizes of the portion pies.

e c o l o g i c a l m o d e l l i n g

Fig. 12 – Principal component analysis applied topartitioning (%) of total consumption of production bypredators (excluding zooplankton and benthos) for the fivemodels (Fig. 11). Eigenvalues and percent variancee

tCNtS

cc2fF(atfd1awtiws

xplained by axes are shown in Table 4.

The exploitation rates (F/Z) (Fig. 9) had higher values inhe NW Mediterranean ecosystem, followed by the Peruvian,hilean and South African systems, and were zero for theamibian system in the case of the small pelagic fish due to

he collapse of the fisheries (Heymans et al., 2004; Roux andhannon, 2004).

The analysis of time series of demersal catches: totalatches, the FIB index and the plot of mean TLc and totalatches calculated for the NW Mediterranean from 1976 to003 (Fig. 10(a) and (b)) showed an increase of the demersalraction in the catch (from 22% to 46%) and of the mean TLc.ig. 10(a) and (b) can be interpreted in seven different periodsdotted lines) corresponding with expansions of the fisherynd the intense exploitation of available resources, mainly ofhe pelagic fraction. In this context, the FIB index decreasedrom 1976 to 1978 and increased from 1978 to 1983. The valueecreased again from 1989 to 1990, increased from 1990 to994 (the year modelled in this study, and for which FIB wast its maximum), and decreased from 1994 to 1998, duringhich period small pelagic fish decreased in their contribu-

ion to total catches. From 1998 to 2000, there was a moderatencrease in the FIB index, followed again by a decrease till 2003,

here negative values have been shown for the last part of theeries.

1 9 8 ( 2 0 0 6 ) 53–70 65

3.3. Consumers of production

The largest consumers of production, after excluding zoo-plankton and benthic invertebrates, were the small pelagicfish in all the case studies (Fig. 11). Results from PCA showedthat NW Mediterranean pattern are more similar to Benguelaecosystems, mainly due to similar values of consumption bymammals and turtles, cephalopods and demersal fish andchondrichthyans (Fig. 12(a)). However, the NW Mediterraneanand Peruvian systems show similar patterns of consump-tion of production by small pelagic fish. In addition, the NWMediterranean shows similarities with the Namibian systemdue to the relatively high proportion of consumption by jelly-fish (Fig. 12(b)). Three factors explained 95.2% of the variance(Table 4).

When analysing the impact of consumption of the produc-tion of small pelagic fish (Fig. 13), the fisheries were by farthe most important group in the NW Mediterranean, whichwas set apart from the other ecosystems when a PCA wasperformed (Fig. 14(a)). Three factors explained 83.36% of thevariance (Table 4). Moreover, consumption of production byfisheries was also important in the Chilean and Peruvian sys-tems, but had collapsed off the Namibian one by the late1990s. Cephalopods, apex fish predators and other demersalfish also played an important role in the NW Mediterraneanregion, whilst cephalopods were also important in Benguelaecosystems. As in the Peruvian system, marine mammals andseabirds showed low impact in terms of consumption in theNW Mediterranean, whilst the importance of these groups inBenguela ecosystems, and to a lesser extent in the Chileansystem, was higher.

4. Discussion and conclusions

Results from comparisons of biomasses, flows and trophic lev-els showed expected important differences between ecosys-tems resulting from differences in primary production, beinglower in the NW Mediterranean Sea, followed by the Benguelaand Humboldt ecosystems. This is in line with productionfrom the Mediterranean Sea (Bosc et al., 2004) and with dif-ferences in transfer efficiencies, which are higher in the NWMediterranean than in the other models included in the com-parison (Jarre-Teichmann et al., 1998; Neira and Arancibia,2004; Shannon et al., 2003; Heymans et al., 2004; Coll et al.,2005) and indicates that the NW Mediterranean ecosystemis food limited. This relates to previous observations sug-gesting that transfer efficiencies from primary and secondaryproduction decrease with increasing primary production sothat oligotrophic areas can be more efficient than highly pro-ductive ones (Cushing, 1975). Moreover, Alcaraz et al. (1985)reported that the ratio between zooplankton and phytoplank-ton biomass was higher in the Western Mediterranean thanin the NW African upwelling regions, suggesting a relativelyhigh ecological efficiency in the Mediterranean Sea.

On the other hand, results from the trophic spectra analy-

sis, total catches and trophic levels highlighted structural dif-ferences among Benguela, Humboldt and NW Mediterraneanfood webs. This is in line with results from diets of commercialspecies that reflect intrinsic ecosystem features. Differences

66 e c o l o g i c a l m o d e l l i n g 1 9 8 ( 2 0 0 6 ) 53–70

Fig. 13 – Main partitioning (%) of total consumption of small pelagic fish production by their predators (including the fishery)e re

for the five models (a–e). Total consumption is reflected in th

in the diet of medium-sized pelagic fish may be also due tolimited availability of data for these species in the Mediter-ranean Sea (Stergiou and Karpouzi, 2002). In the case of horsemackerel this may be due also to the fact that the diet for theNW Mediterranean case study has been assumed applicableto both small and large horse mackerel due to lack of detailedinformation, whilst ontogenetic information is available forthe upwelling ecosystems.

Results from biomasses, flows and consumption of pro-duction also showed that NW Mediterranean had similar pat-terns to the South African system. This could be related to

the fact that both models from NW Mediterranean and SouthAfrican systems include a part of shelf habitat in compari-son with the other ecosystems compared. The South Africanmodel includes the Agulhas Bank, which is important in terms

lative sizes of the portion pies.

of shelf habitat (Shannon and Jarre-Teichmann, 1998) andthe NW Mediterranean model includes the continental shelfecosystem associated with the Ebro River Delta (Coll et al.,2005).

From the analysis of consumption of production it is alsoshown that the role of benthopelagic fish in the NW Mediter-ranean was smaller than in the other models. This could berelated to the large proportion of continental shelf withinthe NW Mediterranean model or to the general problems ofbiomass estimation of these daily migratory species.

Results from this comparison also underlined the higher

impact of fishing within the NW Mediterranean ecosystemrelative to the primary production, reflecting the high fishingpressure in that area. This was highlighted by high catches andlow primary production, low total biomass and low total sec-

e c o l o g i c a l m o d e l l i n g

Fig. 14 – Principal component analysis applied topartitioning (%) of total consumption of small pelagic fishproduction by their predators (including the fishery) for thefie

ot1olfito

tEe(2vatg2

oeeNai

ve models (Fig. 13). Eigenvalues and percent variancexplained by axes are shown in Table 4.

ndary production, high %PPR, low TLc and large values for therophic spectra of catch: biomass ratio (Pauly and Christensen,995; Pauly et al., 1998; Rochet and Trenkel, 2003). In the casef the NW Mediterranean, total biomasses and flows were also

ower and these indicators are expected to decrease with highshing pressure, although they can also be related to ecosys-em size and might be difficult to predict due to indirect effectsf fishing through food webs (Rochet and Trenkel, 2003).

In addition, the NW Mediterranean showed high exploita-ion rates (F/Z for small pelagics and hake) and in the case ofuropean sardine the value was higher than 0.5, the limit ref-rence point above which overexploitation is likely to occurPatterson, 1992; Mertz and Myers, 1998; Rochet and Trenkel,003) and similar to the F/Z ratios for sardine in the Peru-ian system. Moreover, the exploitation rate for juvenile anddult hake was the highest, and in the case of the adult hakehe value was higher than the recommended rate of 0.8 forroundfish stocks (Mertz and Myers, 1998; Rochet and Trenkel,003).

Furthermore, the comparison of %PPR, TLco, total biomassf consumers (excluding plankton and macrobenthos) andxploitation rates (F/Z) seemed to capture the ecosystem

ffects of fishing (Rochet and Trenkel, 2003), larger in theamibian, Peruvian and NW Mediterranean systems. Thenalysis of biomass by discrete trophic level also showed sim-larities between these ecosystems.

1 9 8 ( 2 0 0 6 ) 53–70 67

Small pelagic fish were very important for the NW Mediter-ranean and Peruvian fisheries, with high catch of small pelag-ics: adult hake and large pelagics, of planktivores: total con-sumers and, to a lesser extent, of planktivores: piscivores fish.This was also highlighted with the size spectra and the lowTLc. However, important differences in the production andbiomass of small pelagic fish were seen between these twoareas; the ratios from the NW Mediterranean were more sim-ilar to the Benguela and Chilean systems than to the Peruvianone. This could be an indirect indicator of the intense fishingpressure of small pelagic fish in the NW Mediterranean, also inline with results for consumption of small pelagic fish produc-tion and exploitation rates (F/Z). Therefore, taking into accountthe differences in ecosystem production, present results sug-gest that marine resources in the NW Mediterranean ecosys-tem have been subjected to high fishing pressure in line withColl et al. (2005).

The FIB index and the demersal: total catch ratio appliedto the NW Mediterranean showed various periods of expan-sion of the fishery (increasing values of FIB), but also of intenseimpact of the exploited pelagic food web (decreasing values ofFIB). The expansion periods of the fishery most likely resultedfrom governmental aids to the fishing sector and the imple-mentation of technological advances (Bas et al., 1985; Farrugioet al., 1993; Papaconstantinou and Farrugio, 2000). Due to thefact that demersal: total catch increased, an eutrophicationprocess in the area cannot be identified (De Leiva Moreno etal., 2000). Time periods where the FIB index was decreasingcould be related to periods with high impact of fishing anddecreased stock sizes of targeted species (mainly small pelagicfish). Moreover, the negative values of the index for the lastpart of the time series could be likely related to an impair-ment of the underlying food web and the ecosystem func-tioning. The demersal: total catch ratio reflects the increasingimportance of demersal catches mainly due to reduced pelagiccatches (Coll et al., 2005). These results should be viewed in thecontext of recent decreasing trends in the NW Mediterraneanpelagic landings and biomasses. After 1994, the official land-ings have shown a steady decline, mainly due to the decline ofthe pelagic fraction, whereas demersal catches seem to haveremained relatively stable since 1983. This would also be inline with recent evaluations of high risk of ecosystem over-fishing sensu Murawski (2000) related with the current fishingactivity in the area (Tudela et al., 2005) and with the ecosystemeffects of fishing reported for the Mediterranean Sea (Tudela,2004).

This decrease in the pelagic contribution to the catches(mainly based on organisms with low trophic levels) is alsoseen in the analysis of the mean trophic level of the catchand catches with time, where the TLc increases from 1976 to2004 and landings decrease. This has also been seen in theNamibian system (Cury et al., 2005), where a more demer-sal dominated ecosystem have been observed, resulting fromthe decrease and non-recovery of the pelagic component. InNamibian system the decrease of the FIB index is likely to bereflecting the collapse of the underlying food webs (Cury et

al., 2005; Heymans, 2004; Heymans et al., 2004; Sumaila et al.,2004; Willemse and Pauly, 2004). On the contrary, a decrease inthe TLc was found in the Western Mediterranean from 1972 to1998 (Pinnegar et al., 2003), but when excluding clupeid land-

l i n g

r

68 e c o l o g i c a l m o d e l

ing from the analysis a marginally significant increase in themean trophic level of capture fishery and aquaculture land-ings was described.

Similarities between the NW Mediterranean and theNamibian system are also reflected in the significant con-sumption by gelatinous zooplankton and the importance ofpelagic-demersal coupling, in remarkable contrast to the otherecosystems. The importance of gelatinous zooplankton inboth ecosystems appears to be a key difference from theother ecosystems modelled. The proliferation of jellyfish inNamibia appeared after the collapse of sardine fisheries in the1960–1970s and jellies have been dominating the system withthe pelagic goby and the horse mackerel (Heymans et al., 2004;Roux and Shannon, 2004). The proliferation of jellyfish in theNW Mediterranean from the 1980s has been also described(e.g. Buecher, 1999), whilst concern about ecosystem statusis rising due to the decrease of important pelagic resources,reflected both in biomasses and catches in the system.

The pelagic-benthic coupling is likely to be indicating thechanged state of the Namibian system due to fishing pressureduring the pre-independence period, exacerbated by environ-mental perturbations and changes (Boyer et al., 2001). Thisecosystem experienced a change from a pelagic-dominatedenvironment towards a demersal one due to the collapse ofsmall pelagic fish in the 1960–1970s (Heymans et al., 2004;Moloney et al., 2005; Roux and Shannon, 2004; Sumaila et al.,2004; Willemse and Pauly, 2004; Van der Lingen et al., 2006).The NW Mediterranean could follow suit in the future, whilstat present the demersal assemblage seems to be growing inimportance relative to the pelagic one (Coll et al., 2005). TheNamibian experience is especially relevant in the context ofthe NW Mediterranean because even though Namibia imple-mented a resource management system to rebuild stocks afterindependence in 1990, the small pelagic fish stocks are notshowing clear signs of recovery (Sumaila et al., 2004; Willemseand Pauly, 2004). Therefore, these similarities between the NWMediterranean and Namibian systems should be interpretedin terms of dynamic trajectories that the Namibian upwellinghas shown due to fishing intensity and the signs that the NWMediterranean is showing in that direction.

The present contribution highlights the usefulness ofcross-system comparisons of standardized models. Even ifecological models are unable to fully capture reality and arebuilt with values associated with different levels of uncer-tainty, they are the “best” picture of the ecosystem withthe available information, and the standardization processhelps to minimize the errors associated with the structureof the model so that the features of the ecosystems can berevealed and compared. These results support the conclusionof Moloney et al. (2005) that comparisons of global indices areuseful to generalise ecosystem structure and fishing proper-ties whilst highlighting uncertainties of the model parame-ters. This is especially important in systems where there is adeficit of time series data, as in the case of the MediterraneanSea.

Moreover, these comparisons are particularly valuable.

Firstly, they serve as a basis for developing and test-ing hypotheses using dynamic simulations of fishing andenvironmental effects along the lines of those examinedin upwelling areas. For example, of special relevance are

1 9 8 ( 2 0 0 6 ) 53–70

the findings that high fishing mortality and environmen-tal anomalies could have driven the Namibian ecosystemfrom 1970s till the present and could be related to the col-lapse of small pelagic fish (Heymans, 2004; Heymans et al.,2004; Roux and Shannon, 2004). Secondly, a comparativeapproach, such as that followed in this study, provides a basisfrom which the mechanisms that drive ecosystem changesand/or regime shifts, and the underlying processes and inter-nal controls operating to sustain ecosystem states, can beexplored.

Acknowledgements

The developers of the ecological models included in thecomparison are acknowledged: Sergio Neira (Chile), AstridJarre (Peru) and Jean-Paul Roux (Namibia). The authors wishto thank them for agreeing to the use of their published modelresults. They also wish to acknowledge all the researchersinvolved in the development of the ecological model of theSouth Catalan Sea, especially from the Institute of MarineScience (Barcelona). The Benguela Ecology Programme andthe University of Cape Town are thanked for logistical sup-port and the Spanish Ministry of Education and Science forfinancial assistance. An anonymous reviewer is thanked forsuggesting PCA analysis as a means to strengthen our resultsand conclusions.

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