The Moroccan Upwelling-Related Resources Case. ICES CM 2005/BB

ICES CM 2005/BB: 14

The need of an ecosystem approach to fisheries management: The Moroccan upwelling-related resources case.

Souad Kifani1, Hicham Masski1 and Abdelmalek Faraj1

1 INRH, 2 Rue Tiznit, Casablanca, Morocco.

Abstract

The Canary current ecosystem is one of the four major eastern boundary upwelling systems of the world oceans. The Moroccan Atlantic continental shelf is part of the Canary current ecosystem, and constitutes an area of high biological productivity and intensive fisheries activity. Like most fisheries worldwide, Moroccan marine fisheries are presently managed following a mono- species approach. The research and stock assessment effort has mainly focused on the commercially targeted species. However, the mono-species approach has gradually revealed its limits: it is inadequate to address ecosystem-fisheries interactions, whereas fisheries operate within a complex array of species interactions and commercial fish stocks are only a part of the complex web of life in the oceans. Catches and distribution of numerous species have undergone decadal changes since the exploitation begun. Huge fluctuations of abundance have been observed for sardines, sardinellas and others pelagic and bottom fishes during the last five decades. Times series of catches show signs of replacement of longer-lived bottom fish species by short lived ones (small pelagics and cephalopods) in the commercial fisheries. The central scientific question that these observations raise is whether the (top down) effects of harvesting or (bottom up) changes in the physical environment are responsible for those changes. The challenge is to understand the critical factors that impact the ecosystem and its resources, and then use this understanding to improve the management of Moroccan fisheries.

Keywords: Canary current ecosystem - catches fluctuation - Ecosystem approach to fisheries - Moroccan fisheries

Contact author: Souad Kifani: INRH, 2 Rue Tiznit, Casablanca, Morocco [tel: +212 22 02 45, fax: +212 22 26 69 67, e-mail: [email protected]].

Introduction Morocco has an extensive Atlantic coastline from 36°N to 21°N that lies alongside the northernmost part of the Canary Current, one of the major eastern boundary systems which is classified as a Class I, highly productive (> 300gC.m-222.yr-1) ecosystem (Carr, 2002; Carr and Kearns 2003). This high biological productivity is stimulated by nutrient-rich upwelling waters. This productive area sustains an important fishing industry which represents an essential economic activity for the bordering countries. It has been stated that marine resources of Eastern Central Atlantic regions are fully or over-exploited, like the majority of the fisheries around the world (Garcia and Grainger, 2004). During the last 50 years, the fisheries moved from a situation where 90% of them were classified as “undeveloped” in the 1950s to one where 34% of them are “mature” and 34% shows declining yields in the 1990s (Garibaldi and Grainger, 2002). As the demographic pressure and the international demand for Þsh and Þsh products will increase, an amplification of the fishing pressure on the living marine resources is expected that might significantly weaken this valuable activity and play an important socio-economic role.

More than 60% of the total Canary current commercial fish landings comes actually from the Northern Canary current sub-system and are actually mostly harvested by the Moroccan fleets after had been heavily exploited by distant water fleets (DWFs). Accordingly, fishing industry represent an important economic branch in the Moroccan agro industry, representing some 2.5% of GDP and accounts for around 15% of total

1 exports. This sector of activity provides close to 400 000 employment opportunities, representing 4% of the Moroccan active population. Fishing activities in Morocco target one or several species. Given the complex array of species interactions on which fisheries operate, the rising complexity implied by the multiplication of fleet interactions (exploitation of new resources, by-catch of non targeted species, discards), and the depletion of some resource stocks, the objective must be the sustainable use of the whole system, not just the targeted species. This implies that the nowadays “Target Resources-Oriented Management” (TROM) approach of Moroccan fisheries has to move beyond simple consideration of fishing pressure on a target species towards a more integrative approach that considers a fishing activity within an ecosystem as embodied in the Ecosystem Approach to Fishery management (EAF) purpose.

As emphasize by Cury et al. (2003), the success of fisheries management in the future depends on research directed at mechanisms underlying ecosystem dynamics and fisheries interactions. The first objective of this study is therefore to investigate the ecosystem changes over the last five decades and whether the ecological footprint of fishing activity has driven changes in the ecosystem. The second objective is to see if the legislative and regulating measures that were implemented in Morocco during the 1990s and the early 2000s answer the need of an EAF and if not how this situation can be improved.

Evidence of Ecosystem Changes Source of data and methods

The ecosystem is taken as wide as the continental shelf areas and extends along the Atlantic coast of Morocco from Cape Spartel (36°N) to Cape Blanc (20°N), Canary Islands area included. Here we refer to this part of the Canary Current Large Marine Ecosystem as the Northern Canary Current Subsystem.

A set of trophodynamic indicators (primary production required to sustain the fisheries, mean trophic level in catches, FIB index) are tested to capture the effect of fishing on the energy transfer in the food web. Owing to technical hitches that make it difficult to compile a collection of long term time series catches record from the various fisheries that have operated or are still operating in the area; as is it also the case for a routine scientific surveys dataset, catches statistics in the SAUP database, extracts from the Sea Around Us project website - http://seaaroundus.org/eez/eez.aspx, were used to tackle this problem. Fuctional Groups partitioning and Trophic levels of species were extracted both from the FishBase website (Froese, R. and D. Pauly. Editors. 2005. FishBase. World Wide Web electronic publication. www.fishbase.org, version (06/2005)) and the Sea Around Us Project Website. A normalized principal component analysis (PCA) was applied on the catch time-series using SPlus software in order to pick-up the relationships between species through time.

A specific study of south Moroccan continental shelf biodiversity and its relationship with trawling was based on datasets from a scientific bottom trawl survey and on a one-year geo-referenced catch statistics. Bottom trawl survey data used is from April 2004 and made up of 80 sampling stations of 20 min trawling randomly distributed on the continental shelf in the Southern Morocco (21°N to 26°N). Biomass and frequencies data are spatially re-allocated (2’ squares), and macrofauna Biodiversity Indexes are computed:

Species Richness (SR) = (1)

Simpson diversity index = (2)

Shannon diversity index = (3)

Hil ½ diversity index = (4)

where “s” is the number of species with the proportions (p1, p2,….., ps) in the sample.

Statistics database is from boarded observers reports from 1993 (Moroccan fisheries Department) and

2 concerns the same geographic area; it includes information (spatial reference, biomass of major species, trawling duration, etc.) about 18 360 fishing records (hauls) from 83 fishing vessels. Fishing effort pattern is built by re-allocating the spatial distribution of trawling duration (2’ squares), and is assumed to depict fishing areas for trawlers.

A normalized principal component analysis (PCA) was applied to explore relationships between fishing effort, biomass and ecological indexes using SPlus software.

The method used to estimate the primary production required (PPR) to support catches in a system is based on the equation of Pauly and Christensen (1995):

C PPR = α ⋅ i ∑ TLi −1 i TE (5)

Where C is the annual catch per km2 of continental shelf surface area for a group of species i. Surface area within the continental shelf boundaries is obtained from the Sea Around Us project website (http://seaaroundus.org/eez/eez.aspx. TL represents the mean trophic level of catch and TE is the mean energy transfer efficiency between trophic levels, generally taken as equal to 10% (Pauly and Christensen, 1995). PPR was converted from wet weight to carbon by a conversion factor α equal to 1:9 (Pauly and Christensen, 1995). PPR is then expressed in ton C. km-2. yr-1.

The Fishing in Balance (FiB) Index was proposed by Pauly et al. (2000) to attempt to capture the effect of fishing on the energy transfer in the food web. The justification is that biological production is amplified by a factor of 1/TE (where TE is the trophic efficiency) when moving one trophic level down in the food web. If fishing reduces the mean trophic level by one, we would expect that this would produce 1/TE increase in landings. A FiB index increase indicates a situation of expanding fishery within ecosystem capacity (exploitation development on stocks lightly or not previously exploited or increasing carrying capacity, i.e. primary productivity enhanced). Conversely, a FiB index decrease occurs when a decline in TLs is not ecologically outweighed by corresponding increase in catch, defined here as a tenfold increase of catch for a decline of one trophic level (Pauly et al, 2000). A FiB index decrease indicates that ecosystem functioning is impaired by fishing. The FiB index will stay constant if a decrease in the average trophic level is matched by a corresponding increase in catches. The FiB index of a given year k, is calculated relative to the FiB index in the first year (1), of a time-series of catch data from the equation:

TL TL ⎡ ⎛ 1 ⎞ ik ⎤ ⎡ ⎛ 1 ⎞ i 0 ⎤ FiB = log⎢∑Cik ⋅⎜ ⎟ ⎥ − log⎢∑Ci0 ⋅⎜ ⎟ ⎥ ⎢ ⎝ TE ⎠ ⎥ ⎢ ⎝ TE ⎠ ⎥ ⎣ ⎦ ⎣ ⎦ (6) where Cik is the landings of species i in year k and TLik is the average trophic level and TE is the mean energy-transfer efficiency between trophic levels.

Global trends in Catch

Removal level from the northern Canary Current subsystem increased roughly sevenfold between the 1950s and the 1970s to reach a more or less constant value kept until the late 90s. Total removal of DWFs from the region has largely affected the catch pattern between the late 1960s and the late 1980s; sustainable increasing trend is however observed for the Moroccan catch that represents actually the bulk of removals from this area (Figure 1- a and b)

3 3 2 Canary Current LME 1,8 Ohers 2,5 Spain Canary Current North 1,6 Morocco Sub-System 1,4 2 1,2

Catches millions Tons millions Tons Catches 1,5 1

0,8 1 tons x Millions Landings 0,6

0,4 0,5 0,2

0 0 1950 1960 1970 1980 1990 2000 1950 1960 1970 1980 1990 2000

(a) (b)

Figure 1: Total landings time-series (1950-2001) in studied ecosystem (a) compared with the whole Canary Current LME total landing (Iberian LME excluded), and (b) Northern Canary current landings allocated to fishing countries.

Other groups 100% Large pelagics (>=90 Large pelagics (>=90 cm) cm) Large demersals Large benthopelagics Large bathydemersals (>=90 cm) (>=90 cm) (>=90 cm) Large demersals (>=90 cm) Medium demersals Large sharks (>=90 cm) 80% (30 - 89 cm) Large benthopelagics (>=90 cm) Medium Medium bathypelagics (30 - 89 cm) Medium pelagics (30 - benthopelagics (30 - Large rays (>=90 cm) 89 cm) 89 cm) Large reef assoc. fish (>=90 cm) 60% Small to medium rays (<90 cm) Small demersals (<30 Small bathypelagics (<30 cm) Cephalopods cm) Medium demersals (30 - 89 cm) Medium benthopelagics (30 - 89 cm) 40% Small to medium Medium pelagics (30 - 89 cm) Medium reef assoc. flatfishes (<90 cm) Cephalopods fish (30 - 89 cm) Medium reef assoc. fish (30 - 89 cm) Small reef assoc. fish (<30 cm) 20% Small demersals (<30 cm) Small pelagics (<30 Small to medium flatfishes (<90 cm) cm) Large flatfishes (>=90 cm) Shrimps Small pelagics (<30 cm) 0% Lobsters crabs Shrimps 1950 1960 1970 1980 1990 2000 Other demersal invertebrates

Figure 2: Trends of relative proportions of functional groups in landings from 1950 to 2001 in the Northern Canary Current subsystem.

A very high percentage of catches is represented by small and medium pelagic fish (Sardina pilchardus, Scomber sp., Trachurus sp., Sardinella sp). (Figure 2). The medium pelagic fish catches increased in the 1970s and show a downwards trend from the 90s concurrently with the small pelagic catches. The landings of large and medium demersal fish, medium reef associated fish, large pelagics fish and medium benthopelagics fish were significant in the 1950s and 1960s, but their contribution declined afterwards, remaining at low levels at present. As global catches grew, small demersal fish, shrimps, cephalopods and small to medium flattfishes have increased their contribution to landings (Figure 2).

Catch data analysis (normalized PCA) reveals clear differentiations in the exploitation of marine resources

4 between decades in the 1950-2001 time-series (Figure 3). The main inertia is due to the production level, separating low level landing years (1950s and 1960s) from high level ones (Figure. 3); the industrialization of exploitation added to a significant increase of the fishing effort in the 1970s produced a real leap in landing values. The second PCA component issued from the analysis differentiates groups for which production levels went down in the 1990s from groups which show an increase during the same decade, illustrated by the groups presenting the highest relative contribution to the second PCA component (Medium benthopelagics [MBT] and large bathydemersals [LBD]).

The overall pattern shows a shift in the exploitation profile in the 1960s, which was maintained in the 1970s, and is characterized by a significant increase in landings. Theses two decades are highly correlated with Medium benthopelagic species, medium reef associated ones, and to a lesser extend, with medium and large demersal fish. The 1980s exhibit a pattern close to the mean and correspond to high production levels. The 1990s are fist strongly correlated with large bathy-demersal species, with a predominant contribution of silver scabbardfish witch was not targeted before the 1980s, secondly come small to medium flatfishes, others groups and then shrimps and small demersal fishes.

Cephalopods C Gastropoda G Large bathydemersals (>=90 cm) LBD Large benthopelagics (>=90 cm) LBT Large demersals (>=90 cm) LD Large flatfishes (>=90 cm) LF Large pelagics (>=90 cm) LP Large rays (>=90 cm) LR Large sharks (>=90 cm) LS Lobsters, crabs LOB Medium benthopelagics (30 - 89 cm) MBT Medium demersals (30 - 89 cm) MD Medium pelagics (30 - 89 cm) MP Medium reef assoc. fish (30 - 89 cm) MRF Shrimps S Small demersals (<30 cm) SD Small pelagics (<30 cm) SP Small reef assoc. fish (<30 cm) SRF Small to medium flatfishes (<90 cm) SMF Small to medium rays (<90 cm) SMR Others DIV

Figure 3: Normalized PCA on landings data in the Northern Canary Current sub-system: Functional groups as variables and years as individuals.

Habitat alteration

Despite the fact that how trawling on one species impacts the other species is not fully understood, there is some evidence from the Saharan bank that the community dominance shift which occurred in the 1960s- 1970s is a consequence of a reallocation in the trophic flow that resulted from both bottom trawling (as indiscriminate method of fishing) and subsequent discarding practices of non-marketable species (Gulland and Garcia, 1984; Caddy and Roudhouse, 1998; Balguerias et al, 2000). The introduction of bottom trawling gears in the 1960s and resulting discard increase may have affected the benthic ecosystem over the Saharan Bank by reducing the predator populations and increasing the food availability for scavengers, many of which are important prey items in the diet of cephalopods, particularly crustaceans (Balguerõas et al., 2000).

5 Around 114 000 tons per year of organic matter is estimated by Balguerõas (1996) to be discarded over the Saharan Bank by solely Spanish trawlers fleet (without taking into account other fleet discards).

The PCA analysis shows that Biomass and specific Risheness (SR) are correlated, and both of them have a negative correlation with fishing effort pattern. Very little to no correlation exists between Species Diversity indexes and the three other variables. This means that both Biomass and SR decrease where trawling increases. Furthermore, the absence of correlation between Fishing Effort and Species Diversity indices indicates that trawling does not produce the same affect on fishing grounds communities; high and low Species Diversity values can be found in areas submitted to intensive trawling.

(a)

Figure 4: (a) Cartography of re-allocated data (2’) of Biomass and Species Richness from 2004 bottom trawl (b) survey, and fishing effort data from 1993 catch statistics.

(b) Normalized PCA on variables (Biomass (BIOMASS), Fishing effort (EFFORT), biodiversity indices: Species Richness (Richness), Shannon, Simpson and Hil ½ (Hil1.1.2) diversity indexes) affected to square spatial units presented in (a).

Piscivorous:planktivorours ratio

Populations of large, slow-growing, late-maturing species are expected to decline in response to fishing more than does small, early-maturing species. Fisheries have a tendency first to remove large, slow-growing predatory fish, so reducing the trophic level of the fish community remaining in the ecosystem (Meyers and Worm, 2003) and consequently impact on their biodiversity, both in terms of within-species abundance and, in the longer term, in term of number of species. The piscivorous:planktivorours ratio (Figure. 5) shows a long-term trend that seems to be consistent with this statement. Fisheries were initially dominated by piscivorous species but have been slowly replaced by planktivorous species in the catches. 6 On other hand, it can be assumed that the intensification of the fishing pressure on small pelagic fish during the three last decades have an implication for the other components of the ecosystem. Small pelagic species form the most abundant fish population in upwelling ecosystems and these forage species seem to exert a major control on energy flows in the ecosystem (Cury et al, 2003, Fréon et al., 2004). Thus it appears useful to track the impact of intensive small pelagic fish removals on the components of the ecosystem at different trophic levels. Indeed, many predatory fish feed primarily on those species which are now being intensively harvested by the fishery.

1,4

1,2 y = -0,0125x + 0,8991 2 1 R = 0,6109

0,8

0,6

0,4

0,2 Piscivorous:planktivorous ratio 0 1950 1960 1970 1980 1990 2000

Figure 5: Northern Canary Current subsystem Piscivorous versus Planktivorous catches ratio from 1950-2001.

Primary production required (PPR) to sustain global catches

The primary production required to sustain fisheries is considered as an ecological footprint that capture the impact of fishing as conveyor of marine trophic flows towards human use (Pauly and Christensen, 1995).

The ratio of harvested biomass to net phytoplankton production is used to determine the level of exploitation rate. Relative PPR is displayed as a percentage of the total primary production available in the system. Despite subsequent limitations inherent to primary production variability, we used average primary production values estimated by Carr (2002) for the Canary Current upwelling ecosystem. The use of default value was necessary because no locally derived long term estimates were available, knowing that relative PPR estimate is strongly dependent on a reasonable assessment of actual primary production that is, unfortunately, not often available on a recurrent base for the whole ecosystem.

The global average energy transfer efficiency between trophic levels in marine ecosystems is considered to be 10% (Pauly and Christensen; 1995), upwelling ecosystems are however in general highly inefficient in transferring energy up the food web (Jarre-Teichmann and Christensen, 1998; Jarre-Teichmann et al., 1998; Carr, 2002). The average transfer efficiency computed by Jarre-Teichmann and Christensen (1998) and Jarre-Teichmann et al., (1998) for the four major Eastern Boundary Current Upwelling systems is slightly above 5%. The transfer efficiency obtained by Jarre-Teichmann and Christensen (1998) and Jarre- Teichmann et al., (1998) for the NW Africa upwelling is slightly higher than average (around 6%). We have consequently used transfer efficiency with value of 10% and 6% in the calculation of PPR.

Furthermore, as stressed by Carr (2002), fish in upwelling areas is expected to be food limited as not all primary production is accessible in time and space to its consumers. Some fraction of primary production biomass will sink or be transported off-shore before it can be consumed (Binet, 1988; Binet et al., 1998; Hutchings, 1992, Mitcheli, 1999; Bakun and Weeks, 2004). Moreover, only a portion of remaining primary production is appropriate for feeding (Binet, 1988). These limitations are thought to lead to an effective environmental accessibility for consumers smaller than the whole primary production generated by the system (Carr, 2002). Effective environmental accessibility is assumed to vary between 10% and 20%. Shannon and Field (1985; cited by Carr, 2002) estimated an effective environmental accessibility of 12% in the Benguela Current region. We applied a somewhat arbitrary effective environmental accessibility of 20% in the Northern Canary Current Subsystem.

The primary production required to sustain catches in the Northern Canary Current Subsystem fisheries uses 7 a relatively large proportion of productive capacity of the shelf ecosystem. Relative PPR calculated by taking into account the smallest energy transfer efficiency in upwelling system leads to a heavier ecological footprint than that calculated by assuming an average trophic efficiency of 10% and a potential use of the whole primary production by primary consumers (Figure 6). The Relative PPR varied from less than 5% of average shelf primary production in the 1950s to around 20% in the late 1990s. Maximum fisheries ecological footprint is reached in the 1970s, when fisheries utilize more than 20% of the primary production. These results indicate that the impact of the fisheries in the Northern Canary Current Subsystem is comparable to the one obtained by Pauly and Christensen (1995) for the intensively exploited temperate shelf ecosystems (where about one third of the primary production is used by fishing), especially for the 1970s. However, it must be underlined that discards were not taken into account in our PPR computation, resulting in a conservative PPR estimates and then an underestimated ecological footprint of the fisheries.

Furthermore, PPR vs catch ratio plot shows a steady downward trend that reflects the ecological cost of the catches (Figure 7). This means that harvested biomasses were more expensive in terms of primary production requirements in the 1950s and 1960s than it was in the 1990s when the fishery withdraws increased and tended to take place progressively lower in the food web. Although fishing at lower trophic levels is not necessarily problematic per se, and results in total yield increase, it would lead to a shortage of energy flow that is transferred to higher trophic levels.

700 50% PPR (Tons C. Km-2.Year-1) %PPR 1 600 %PPR 2 40% 500

400 30%

300 20% Relative PPR 200 10% 100

PPRfrom (Flow primary producers) 0 0% 1950 1960 1970 1980 1990 2000

Figure 6: Primary production required (PPR) to sustain yields removed by fisheries from the Northern Canary Current sub-system between 1950 and 2001 .

50 y = -0,204x + 44,793 R2 = 0,4857 45

PPR:Catch ratio 30

20 1950 1960 1970 1980 1990 2000

Figure 7: Northern Canary Current subsystem primary production required (PPR):Catches ratio evolution from 1950 to 2001.

8 Mean trophic level of catch

The Mean trophic level of the catch (TLs), used as an index of sustainability, reflects the strategy of a fishery in terms of food web components selected (Pauly et al., 2000).

It is assumed that a decreasing in Mean TLs trends indicates that fisheries tend to switch from species with high trophic levels to species with low trophic levels in response to changes of their relative abundances (Pauly et al., 1998). The Mean TLs pattern must however be analysed by taking into account that Mean TLs trends may reflect:

i. A fisheries-induced changes in the food webs from which the landings were extracted.

ii. A fishing taking place low in the food web as a deliberate policy choice to allow more of an ecosystem’s biological production to be harvested, or

iii. A bottom-up effect resulting from an enhancement of the primary production.

Estimated Mean TLs (Figures 8, 9) shows a steady upward trend from 1950 to the early 1970s in parallel with catch. Mean TLs picked up in 1972 and shows a somewhat decline after this year. The decrease became more noticeable in the 1980s, which indicates that fishery seems to have switched from high trophic level species to low trophic level species; probably in response to changes of their relative abundances in the ecosystem.

3,55

3,5

3,45

3,4 TLs 3,35

3,3 1950 2001 3,25 00,511,52 Landings (Millions Tons)

Figure 8: Mean Trophic Level versus landings evolution from 1950 to 2001

3,55 3,5 3,45 3,4 3,35 TLs 3,3 3,25 3,2 3,15 1950 1960 1970 1980 1990 2000

Figure 9: Trend in Mean TLs of the Northern Canary Current subsystem global landings (1950-2001)

This decreasing Mean TLs trend from the 1970s cannot however be entirely imputed to a ‘‘fishing down the food web’’ effect (sensus Pauly et al, 1998a), since it could be also due to bottom-up effect that have 9 enhanced low trophic levels’ fish production as it is often the case in upwelling systems. Increase of small pelagic catches, would lead, through a decline of computed Mean TLs, to a misleading impression of a decline in high individual TLs, even though the corresponding species may not have reduced their abundance in absolute terms (Caddy et al, 1998; Pauly and Watson, 2005). Massive quantities of forage species, especially sardine, were extracted from the Northern Canary Current Subsystem since the late 1970s. Meanwhile, an increase in the sardine biomass, related to an enhanced upwelling intensity, was observed during the 1970s (Sedykh, 1978; Holzlohner, 1975; Binet, 1988, Binet et al., 1998). The Northern Atlantic Oscillation (NAO) is a large scale climatic forcing (Hurrell, 1995, Dickson et al., 2003; Stenseth et al., 2003), which has a significant influence on the Canary Current ecosystem productivity north of 20°N (Roy and Cury, 2003; Aristegui et al, 2005). The NAO index, taken here as a proxy for environmental forcing (Stenseth et al., 2003), is plotted against mean TLs of the catches (Figure 10). Long term variability of mean TLs and the NAO index appear to exhibit patterns in opposite phase. Correlation between those two indexes is negative (r=-0.45, p=0.001). This result is in agreement with the assumption that observed average TLs trend would reflect a “bottom up” effect of primary productivity on abundance of planktivores small pelagic fish, especially the dominant one, i.e. sardine.

6 3,55 3,5 4 3,45 2 3,4 0 3,35

3,3 Mean TLs NAO index -2 3,25 -4 3,2 -6 3,15 1950 1960 1970 1980 1990 2000

Figure 10: Comparative pattern of DJFM NAO index (http://www.cgd.ucar.edu/~jhurrell/nao.stat.winter.html#winter) and Mean TLs global catches of Northern Canary Current subsystem. ( Mean TLs, NAO index, solid lines are smoothed (span 3)) .

Furthermore, increasing fisheries landings originating from the lower part of the food webmay also be due to a deliberate policy aiming to increase fish production by orientating the fishing effort towards more abundant and more productive species presenting low trophic levels (Pauly et al, 1998b). The demand increase for canning and fish-meal industries since the 1970s in Morocco and Canary Islands as well as the significant development of Eastern countries (DWFs) fishing effort targeting small pelagic fishes fall probably under the same logic. This implies that a growing pressure on forage species, as a key element of the food web, might lead to an alteration of the flow transfer efficiency towards the higher trophic levels of the food web, and hence could result in a collapse of ecosystem. Fishing down the food web must then be balanced by an ecologically suitable increase of the catch, which takes into consideration the transfer efficiency (TE) between trophic levels (Pauly and Watson, 2005). At the opposite, the decline of the average trophic level of fished species can be associated with by stagnation or decrease in global catches. When lower trophic levels removals reach risky limits that impair bottom-up production transfer, the mean TLs versus catch curve could bend backwards (Pauly et al, 2000; Pauly and Watson, 2005).

The average trophic level in catches removed from the Northern Canary Current Subsystem has indeed declined during the last two decades with total landings oscillating around 1.5 Million of tons (Figure 8). This cannot however be straightforwardly interpreted as resulting from an expansion of fishery beyond the ecosystem capacity. Small pelagics have been targeted by eastern countries during their intensive exploitation in the 70s until the late 80s. Two major shifts have been subsequently recorded in catches trajectory, respectively the mid-70s and the early 90s (Figure 8). These shifts might be related to geopolitical and fisheries access regimes changes which have influenced the activity of the dominant pelagic fishery operated by the eastern countries DWFs. Reduction in Eastern Countries DWFs catches followed the end of open access status prevailing in the 1970s and the ending of the fisheries access agreement accorded to 10 eastern block countries DWFs in the 1980s and early 1990s. It should be noticed however that the average trophic level of the second maxima of landings was lower than the one recorded during the 1970s.

The reliance of mean TLs on planktivores catches will however masks a top-down effect which should be expected in such heavy exploited area. To highlight alteration in the relative abundance of the more threatened, high-TL fishes, Pauly and Watson (2005) proposed an average trophic level index based on time- series that exclude the low trophic level (e.g planktivores) whose high biomass tends to vary broadly in response to environmental factors and, consequently, masks TLs changes induced by fishing. CutTLs Index, calculated after excluding species groups with trophic level lesser or equal to 3.75 (Christensen et al., 2003), shows evidence of a clear downward trend (Figure 11). This indication would confirm that large and slow growing species in the top of the food chain have been removed from the system or that flow channelled towards the top trophic levels via small pelagics fish were impaired by fishing.

4,35 4,3 4,25 4,2

TLs 4,15 cut 4,1 4,05 4 3,95 1950 1960 1970 1980 1990 2000

Figure 11: Plot of high trophic levels catches of the North Canary Current subsystem mean TLs (1950-2001).

Fishing in Balance (FiB) Index

Figure 12 depicts the profile of FiB index computed with TE taken equal to 10% (computation of FiB index with a transfer efficieny of 6% provides similar results). The index increased greatly as the fishery expanded over the period from 1950 to 1975 reflecting how the fisheries developed steadily to rely onto the productive capacity of the entire ecosystem. FiB plot shows a minor change from 1975 onwards, with marginally non- significant decrease, reflecting the consistent growing of small pelagic fish contribution to the catches.

1,4

1,2

0,8

0,6 FiB 0,4

0,2

0 1950 1960 1970 1980 1990 2000 -0,2

Figure 12: Changes in the Fishing in Balance index (FiB) of the Northern Canary Current global landing (1950-2001).

Discussion The Moroccan fishery industry has gone through a development phase in the 1970s and the 1980s, where enhancing of national harvesting capacity, boosting production and incomes was the major objectives pursued. Within four decades this activity has gone from exclusively artisanal and semi-artisanal fishery, targeting mostly pelagic species used in canning and fishmeal production factories, to a more industrialized 11 activity targeting species of increased export value. Morocco became more concerned with the sustainability of its fishing sector when valuable fisheries, like the cephalopods fishery, began to experience a problem of resource depletion in the 1990s. With this growing concern about long term economic viability of fishing activities, solutions were required. A range of legislative and regulating measures were implemented during the 1990s and the early 2000s. Some of them are listed below:

! ban on catch and trade of threatened species, ! ban on new national fishing capacity investments, control and limitation of access to fisheries to face the problem of overcapacity; ! Enforcing the existing regulations on mesh size, minimum landing sizes; ! ban on destructive fishing gear; ! Setting up of areas and season closures for cephalopods and Sardine stocks, Marine Protected Areas in habitat areas of particular concern; ! Setting up of rights based management plans for octopus and sardine stocks (based on precautionary TACs); ! Enforcing regulation on incidental mortality by setting up a bycatch thresholds of non-targeted species for the most industrialized national fleet and for foreign fleets; ! Increasing the involvement of stakeholders in decision-making management (El Filali and El Ayoubi, 2004).

Theses measures, based on TROM approach, were however essentially implemented to cope with the fishing overcapacity, spatial fleets interaction and growth overexploitation issues, although elements of multispecies interactions and environmental forcing are somewhat taken into account in the management procedures (e.g. ban on catch and trade of threatened species, MPAs, bycatch thresholds, precautionous TACs). Concerns would be expressed therefore about biomass tradeoffs among species in the ecosystem (Link, 2002) and the ability of the TROM approach to maintain critical ecosystem processes and structures (Murawski, 2000; Degnbol, 2001).

There is growing evidence from many fisheries in the world that the ecological consequences of fishing are substantially greater and more complex than the biomass reduction of target species. At first glance, results presented in this work give a rough picture of a system that does not seem to be heavily exploited. However, there are signs of steady erosion of marine resources and food web perturbation. Further increase in yields from this ecosystem is expected to be at low trophic levels in the food web, since small pelagic species or others species with high turnover like cephalopods are presently targetted. Our estimates of the energy transfer through the food web suggest that about 20% of the energy produced by the primary producers in this area is needed to sustain the current fisheries. When such a high fraction of the production is taken out from the system it is expected that species competing with the fisheries for resources will be affected. Consequently, fisheries management has to deal with energy flows within the ecosystem and some of the limitation imposed by trophic transfer (Link, 2005), as it has to cope with climatic driven uncertainty impacting this ecosystem. Species which are primarily concerned are precisely those supporting the bulk of the current fishing activities in the Canary current northern subsystem –i.e. forage fishes and cephalopods. The former species play a major role in channelling the energy flow up in the system but their abundance variability is climatic driven (Cury et al, 2003; Rice, 2001). Caddy and Roudhouse (1998) highlighted that landings of the latter species have already peaked in area where both cephalopods and ground fish have been submitted to intensive trawling. Evidence does exist that cephalopods landings are now varying as a function of fishing effort and environmental variation (Caddy and Roudhouse, 1998).

On the other hand, cumulative impact of the various changes that occurred in the Northern Canary Current subsystem area (geopolitical context, environmental and access regimes, previous removal levels) on marine living resources has little been accounted for in decision making concerning the development and management of marine fisheries in Morocco. Fisheries development or management actions undertaken in this context run the risk to face a situation already influenced by past fishing considered as their baseline. As underlined by Pauly (1995), Pitcher (2001) and Sumaila (2004), past overexploitation (resulting from previous open access regime and overcapacity) implies that many capture fishery resources are now producing below their full potential.

Governments’ commitment at Johannesburg summit enforces to protecting biodiversity and improving ecosystem management to restore fisheries to their maximum sustainable yields by 2015. However, because

12 shifting baselines syndromes (Pauly, 1995) occurs more often in developing countries, management for sustainability might be based on inappropriate reference points for evaluating losses from overexploitation or for setting a target for recovery measures. As a result, management processes under TROM would maintain both marine living resources and their underlying ecosystem in ecologically undesirable state (Willemse and Pauly, 2002).

The above considerations highlight the need to develop a more holistic and integrative approach that addresses more explicitly the effect of fishing on the whole ecosystem. The principle of an ecosystem approach to fisheries states that fisheries have to be “plan, develop and manage in a manner that addresses the multiplicity of societal needs and desires, without jeopardizing the options for future generations to benefit from a full range of goods and services provided by marine ecosystems” (The Reykjavik FAO Expert Consultation-FAO, 2003). However, while it is a major conceptual advance that will make it possible to achieve the goals of resources conservation, the practical problems that such an approach implementation will raise are immense, particularly in the context of developing countries. One related question will be for example: do fisheries management agencies in Morocco have to consider the sustainability of the valuable octopus fishery or to try to restore the ecosystem state prevailing earlier? Cephalopods fishery is mostly an export-oriented activity that constitutes an important product of seafood world trade (Alder and Sumaila, 2004) and provides a significant source of incomes for Morocco. In such a situation, the international pressure context and the short term economic requirements, at both national and local levels, will be too overwhelming for serious consideration of change, even if the long-term benefits on ecosystem level were obvious. This will make it questionable the EAF objectives of conserving ecosystem biodiversity, structure and functioning in the nowadays Moroccan context.

Management objectives are a matter of societal choice. Some ecosystem states, even if desirable, may not be sustainable in the long term (Link, 2005). So, notwithstanding the constraints that will shackle an ecosystem approach implementation in the developing country context, given the stakes that underline their fishing sector, ecosystem functioning constraint has to be accounted for to meet fisheries sustainability. As a result, a fisheries ecosystem plan has to be developed for the Moroccan upwelling ecosystem to increase managers’ and stakeholders’ awareness of how their decisions affect the ecosystem. Such fisheries an ecosystem plan would be the next major step in translating today’s TROM approach efforts into a more holistic approach (Mace, 2001) that seeks to balance conservation and responsible ecosystem use.

Acknowledgments We wish to express our thanks to the Sea Around Us Project Team for providing datasets used in this work, as well as to Pierre Fréon, Eric Machu and Pierre François Baisné for providing useful comments and suggestions on draft version of the paper.

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