© 2003 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Biology of Ethmalosa fimbriata (Bowdich) and fish diversity in the Ebrie Lagoon (Ivory Coast), a multipolluted environment
a Université Montpellier II, Laboratoire Ecosystèmes Lagunaires (UMR CNRS-UMII 5119) Case 093, Place E. Bataillon, 34095 Montpellier Cedex 5, France
b Centre IRD BP 1386, Dakar, Senegal
c Faculté de Pharmacie, Dept. Sciences de l'Environnement et Sante Publique Av. Charles Flahault, 34060 Montpellier, France
*Correspondence to C. Aliaume; tel: +33-467-144765; fax: +33-467-143719. e-mail: aliaume{at}crit.univ-montp2.fr.
The biology of the clupeid Ethmalosa fimbriata (Bowdich) was studied as a potential bio-indicator of pollution in three bays of the Ebrie Lagoon, an inter-tropical lagoon in the Ivory Coast (western Africa). Bietri Bay was the most impacted by Abidjan's industrial and urban waste, Cocody Bay was characterized by the presence of eutrophic water, and Sud Boulay Bay, located in a rural zone, was least impacted. Sizes at first maturity (fork length) of E. fimbriata were lowest in the most polluted bay (Bietri: 80.8 and 83.5 mm for males and females, respectively), higher in the intermediately polluted bay (Cocody: 125 and 137.5 mm, respectively), and highest in the unpolluted bay (Sud Boulay: 135 and 145 mm, respectively). Owing to its hardiness, E. fimbriata is the dominant species in polluted water, constituting more than 75% of the total number of fish caught. As a consequence, fish diversity decreased and the community was less structured in the polluted environment than in the unpolluted one.
Keywords: bio-indicator, DIMO model, Ethmalosa fimbriata, fish community, inter-tropical lagoon, pollution impact, size at first maturity
Received 5 July 2002; accepted 16 January 2003.
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Introduction |
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Estuaries and lagoons represent about 13% of coastal areas worldwide and exhibit very diverse characteristics in terms of surface area (a few km2 to 800 km2), shape, freshwater input, connections to sea, and anthropogenic impact (Blaber, 2000). Lagoons are usually shallow and confined areas at the interface of continental and marine waters, and characteristically have large salinity gradients and variable environmental conditions. Tidal influence and exchange with seawater may be limited. Evaporation, by contrast, is usually high and salinities can range from 5 to 50 (Hodgkin and Birch, 1982; Blaber, 2000). In addition to a high degree of natural variability, coastal areas are exposed to increasing anthropogenic pressure, both industrial and urban, that is not always well evaluated. Appropriate biological indicators of ecosystem health are therefore needed to protect and, where necessary, restore natural environments, as recommended by, inter alia, the FAO (1995, 1996).
Rapid demographic growth in the city of Abidjan and associated burgeoning industrial activity are responsible for the increase in urban and industrial discharges into the Ebrie Lagoon, the Ivory Coast's largest lagoon. Discharged water is largely untreated (Chantraine and Dufour, 1983; Durand et al., 1994). As a consequence, coastal waters and the living resources adjacent to Abidjan are heavily impacted (Pages et al., 1980; Zabi, 1982; Carmouze and Caumette, 1985; Kouassi and Guiral, 1990). Several studies have demonstrated the impact of increasing pollution on the environment itself, as well as on benthic macrofauna, heterotrophic bacteria, phytoplankton, and primary production (Pages et al., 1980; Zabi, 1982; Carmouze and Caumette, 1985; Kouassi and Guiral, 1990; Durand et al., 1994). Although significant research effort has been directed towards studies of the fish community (Daget and Durand, 1968; Durand et al., 1982; Albaret and Ecoutin, 1989, 1990), very little work has focused on the potential impact pollution can have on fish diversity and the population dynamics of the resources (Albaret and Charles-Dominique, 1982).
The clupeid Ethmalosa fimbriata is abundant along the coast of western Africa. It is estuary-dependent and tropical, distributed from Mauritania to Angola (Charles-Dominique, 1982; Lévêque et al., 1990). In the Ebrie Lagoon, it is the most abundant fish species by both number and biomass, and it is heavily exploited by a small-scale fishery (Durand et al., 1982). Studies of larvae, growth, and migratory behaviour have been documented (Scheffers et al., 1972; Albaret and Gerlotto, 1976; Scheffers and Conand, 1976; Gerlotto, 1979; Albaret and Charles-Dominique, 1982). It is very adaptable to environmental change and tolerates wide variation in salinity (Charles-Dominique, 1982). Observations within the Ebrie Lagoon have revealed that the species spawns and spends its first year of life inside the lagoon, before migrating offshore during its second year (Gerlotto, 1976; Charles-Dominique, 1982).
Albaret and Charles-Dominique (1982) documented a notably small size at first maturity of E. fimbriata in Bietri Bay, a highly polluted area of the Ebrie Lagoon. Study of such a species able to tolerate great environmental disturbance, both natural and anthropogenic, may be revealing. The objectives of the current paper are therefore to study its biology, in particular its size at first maturity, in polluted and unpolluted environments, and to evaluate the impact of polluted environments on the structure of the overall fish community in the lagoon.
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Material and methods |
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The Ebrie Lagoon is part of the inter-tropical estuarine system of the Ivory Coast (4–11°N, 2–9°W), and lies between the Grand Lahou and the Aby Lagoons (Figure 1). With an average depth of 4.5 m and a surface area of 566 km2, the lagoon (which is narrow, only 4–5 km wide) extends more than 130 km parallel to the coast (Carmouze and Caumette, 1985; Durand et al., 1994). Durand et al. (1994) divided the lagoon into six homogeneous zones on the basis of morphological features and location, the relative influence of the Vridi Canal, and the input of freshwater. The only permanent connection with the sea is through the Vridi Canal, a channel 300 m wide and 15 m deep constructed during the 1950s. Freshwater input is mainly by the Comoe River, located on the eastern side of the lagoon.
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The present study was located in zone III of the lagoon, where a non-polluted bay, Sud Boulay, can be compared with two multipolluted bays, Cocody and Bietri (Figure 2). The three bays, all with similar relative environmental conditions (Durand et al., 1994), were selected according to their degree of pollution. Sud Boulay Bay (10 km2) is in a rural area and therefore can be considered as the unpolluted reference point. Cocody Bay is 1.4 km2 in area and has a depth of only a few metres (Daget and Durand, 1968). It is located in an urban area, between Abidjan and the Cocody township, and is eutrophic (Dufour and Slepoukha, 1975). Finally, Bietri Bay (5.5 km2) is located in the centre of the Abidjan metropolis. It is a virtually closed system that opens on its western side into the main lagoon through a very narrow channel. It is extremely eutrophic and is the most polluted bay of the Ebrie Lagoon. The three bays are described in more detail by Chantraine and Dufour (1983) and Durand et al. (1994).
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Sources of pollution
There are three main sources of pollution: chemical, organic, and bacterial. Chemical pollution, mainly hydrocarbons, organochlorides, and heavy metals, is derived from agricultural and industrial activity in the adjacent watershed. Fertilizers and phytosanitary chemicals drain out during runoffs (especially during the wet season), and subsequently impact the quality of coastal waters. The use of chemicals in farming has increased during the past few years as a direct result of burgeoning agricultural development. In addition, industrial chemicals, including soda ash, pigments from the textile industry, heavy metals from metallurgical enterprises, and arsenic from leather tanning, are discharged in the area of Abidjan (Chantraine and Dufour, 1983; Durand et al., 1994). Contributing to this output of pollutants are slaughterhouses and an oil factory near Cocody Bay, and municipal slaughterhouses and dyeing plants near Bietri Bay. Marchand and Martin (1985) recorded total concentrations of hydrocarbons exceeding 1000 µg g–1 of dry sediment in urban bays, and none at all in rural bays. The same authors also noted much higher concentrations (>100 ng g–1) of polychlorinated biphenyls (PCBs) in urban bays than in rural ones.
Organic pollution originates from farm produce and includes malt, yeast, and plant oil. In 1980, these three components alone accounted for 47% of the total organic pollution near Abidjan, a city then in which the homes of only one in five of its citizens were connected to waste-water treatment plants. The situation is different outside the city where, for example, Sud Boulay Bay shows no clear sign of organic pollution (Chantraine and Dufour, 1983; Durand et al., 1994).
Bacterial pollution attributable to sewage is characterized by high levels of enteric bacteria, Escherischia coli and Clostridium perfringens, both of which are known to be a danger to human health. Concentrations measured close to Abidjan in the 1970s and subsequently revealed a real sanitary risk (Pages, 1975; Pages and Citeau, 1978). In waters adjacent to urban areas, E. coli and enteric bacteria are, respectively, 500 and 70 times higher than off rural areas (Kouassi and Guiral, 1990). As a consequence, swimming is forbidden near Abidjan, according to the OMS/PNUE (1977) standards (Kouassi and Guiral, 1990).
Sampling
During part of 1980 and 1981, fish were captured every second month in Sud Boulay Bay (nine sampling trips) and monthly in Cocody Bay (16 trips), using a purse-seine 300 m long and 18 m high, with a square mesh of 14 mm. Each sampling trip consisted of five hauls. A further 11 hauls were made in Bietri Bay between February and May 1980 (Albaret and Charles-Dominique, 1982). However, to compare the population dynamics of the fish resources, only data on E. fimbriata collected from the three bays during 1980 were used, i.e. 628 fish caught in Sud Boulay Bay, 1018 in Cocody Bay, and 510 in Bietri Bay.
Analyses
The proportion of male E. fimbriata in the total number of fish sexed was calculated for each of the three bays. Size distributions by sex were drawn on the basis of fork length (FL, measured to the nearest mm) and summarized by 5 mm size classes.
The stage of maturity was determined macroscopically from the gonads, following the methods and descriptions of Fontana (1969). Size at first maturity (L50), the size at which 50% of the fish caught were mature or at a more advanced state of maturity (stage 3+) was determined graphically as the inflexion point of the curve when plotting cumulative frequencies of mature fish against FL. Data on males and females were processed separately.
The distribution of male and female E. fimbriata inside each of the three bays studied was compared by means of a 
2 test. Fish length was compared by sex and bay using two-way ANOVA, and L50 in each bay was compared using a median test.
To analyse the structure of the fish community, a diversity monitoring (DIMO) model was applied (Qinghong, 1995). This model visualizes species richness (log2 S), the Shannon index (H'; Shannon and Weaver, 1949), evenness (H'/log2 S; Pielou, 1966) and Qinghong's (1995) Q index in a single graph. The Q index is defined as the vector length from origin to sample point. This graphic method evaluates the indices that best characterize change in community structure, and it permits comparison of the fish communities of Sud Boulay and Cocody Bays using seven common sampling dates in 1980 or 1981.
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Results |
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Biology
Of the 1018 E. fimbriata caught in Cocody Bay, 19.5% were male, 23% female, and 57.5% of undetermined sex. In Sud Boulay Bay, 42.5% of the 628 caught were male, 31% female, and 26.5% unsexed. In Bietri Bay, 44.3% of the 510 fish caught were male, 49% female, and 5% of indeterminate sex. The proportions of males caught in the three bays were therefore remarkably similar: 0.58, 0.47, and 0.49 for Sud Boulay, Cocody, and Bietri, respectively. However, a
2 test revealed non-homogeneity in the distributions of males and females in the three bays (2=16.01, d.f.=2, p<0.005). Comparison off the size of the fish sexed in the three bays (Figure 3) by two-way ANOVA showed a significant effect for both sex and bay factors (p<0.0001). Females were always slightly larger than males, indicating that females grow a little faster. Mean sizes were smallest in Bietri Bay (84 and 87.7 mm for males and females, respectively), intermediate in Cocody Bay (122.2 and 130.8 mm), and highest at the unpolluted reference site of Sud Boulay Bay (138.2 and 151.9 mm).
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In terms of the stage of sexual maturity, of the 432 sexed E. fimbriata caught in Cocody Bay, 116 males and 148 females were at or above stage 3. In Sud Boulay Bay, 161 of 194 females and 227 of the 267 males were at that stage of maturity. These data were used to determine the size at first maturity (Figure 4). The L50 for males was 80.8, 125, and 135 mm in Bietri, Cocody, and Sud Boulay Bays, respectively (Figure 4b), and that for females was 83.5, 137.5, and 145 mm for the same bays (Figure 4a). A median test revealed a significant effect of bay (p<0.0001), but no significant effect of sex.
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Differences between the average sizes of males and females varied by sample location, 13.7 mm in Sud Boulay Bay, 8.6 mm in Cocody Bay, but just 3.7 mm in Bietri Bay. Differences in L50 were of the same magnitude, 10, 12.5, and 2.7 mm for the same bays.
Fish communities in Sud Boulay and Cocody Bays
Analysis of catch per unit effort (cpue) revealed a dominance of E. fimbriata in Cocody Bay (Figure 5). In 11 of the 16 samples, E. fimbriata accounted for more than 75% of the total number of fish collected. The species' lowest relative abundances were 32% in January 1981, when Chloroscombus chrysurus was most abundant (42%), and 28% in March 1981, when Sardinella maderensis was abundant (65%).
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In Sud Boulay Bay, more species contributed to the catch (C. chrysurus, S. maderensis, Gerres nigri, Caranx senegalus, and E. fimbriata), so the cpue was not closely related to the abundance of E. fimbriata (Figure 5). However, many more fish were caught in Cocody Bay than in the unpolluted Sud Boulay Bay, except in December 1980, when numerous juvenile S. maderensis were found in the latter bay.
The DIMO model clearly illustrated the decrease in diversity, evenness (
angle) and Q index in the polluted bay (Cocody) compared with the reference bay (Sud Boulay; Figure 6). This can be interpreted as the existence of a better structured community in Sud Boulay Bay, with an evenness that is high and close to maximum (H' = log2 S), than in the polluted Cocody Bay. Only the December 1980 sample from Sud Boulay Bay equated the community structure of Cocody Bay, coincident with the abundance then of S. maderensis.
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Discussion |
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In this paper, biological characteristics of E. fimbriata were compared between urban and non-urban areas of the Ebrie Lagoon. The size at first maturity was inversely related to the extent of pollution, the highest L50 being associated with the unpolluted reference site and the smallest with the most polluted site. The differences demonstrated a high tolerance of the species to polluted environments. Further, differences between male and female L50 decreased also (10, 12.5, and 2.7 mm, respectively), suggesting perhaps that E. fimbriata is reaching its maximum capacity of adaptability in response to the extreme environmental stress within Bietri Bay. As a consequence, the species may be a good bio-indicator of coastal water quality, by way of its L50 and catch rate. The advantages of using it in such a manner are its broad distribution, its relative abundance, and the fact that its early life history is spent inside lagoons and coastal areas.
The differences in L50 between fish caught in Sud Boulay and Cocody Bays were not as noticeable as between fish caught in Cocody (the intermediately polluted environment) and Bietri Bays. This can be taken as confirmation that Bietri Bay is highly polluted whereas Cocody Bay is mainly eutrophic (urban pollution). The L50 of E. fimbriata calculated overall for the Ebrie Lagoon is lower than for the same species in other West African countries. In Senegal for example, the L50 was calculated by Scheffers et al. (1972) to be 160 and 170 mm for males and females, respectively, and in Sine Saloum, a hyperhaline lagoon of Senegal, it was 175 and 180 mm for males and females (Diouf, 1996). In Casamance (also in Senegal), it ranged from 140 to 150 mm for females and from 130 to 140 mm for males (Albaret, 1987). Farther afield, in Rio Ruba (Guinea Bissau), the L50 for males and females, respectively, has been documented as 144 and 150 mm (Kromer et al., 1994), and in Gambia females mature at 185 mm (Scheffers and Conand, 1976).
The robustness of E. fimbriata is probably the reason for its dominance in the polluted Cocody and Bietri Bays, the other fish species clearly being unable to adapt to the changing conditions to the same extent. However, in the unpolluted Sud Boulay Bay, other species can be more abundant, increasing the inter-species competition for food and habitat. Over a longer period than studied for this analysis, the trend in catch rates is the same (Table 1). For the period 1978–1985, the catch of E. fimbriata accounted for 44% of the total number of fish caught in Sud Boulay Bay, 77% in Cocody Bay, and 92% in Bietri Bay (Ecoutin, 1992). Of course, the dominance of a single species leads to lower levels of evenness and diversity, and this is evident in the comparison between Cocody Bay and Sud Boulay Bay: the fish community appeared to be less structured in the more polluted environment of the former bay. A loss in diversity attributable to anthropogenic impact has been shown by many studies (Harrel and Hall, 1991; Grall and Glémarec, 1997; Chow-Fraser et al., 1998; Boêt et al., 1999; Gafny et al., 2000; Martin et al., 2000).
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Adaptive strategies (either behavioural or physiological) usually take the form of reproductive changes, space use, and/or resource use. Indeed, migratory species have to speed up their life cycle to save energy and to counter-balance the loss of energy caused as a result of climatic or anthropogenic stress (Amanieu and Lasserre, 1982). Perhaps E. fimbriata allocates most of its energy to reproduction and metabolism, to the detriment of body growth, as observed for two species of tilapia, Oreochromis niloticus and Oreochromis aureus, in Mariut Lake, Egypt (Bakhoum, 1994). Further, besides its tolerance of pollution, E. fimbriata can reproduce in salinities ranging from 3.5 to 38 (Charles-Dominique, 1982), adding to its robustness to stress. Indeed the same species matures at a salinity >60 in Casamance and Sine Saloum, Senegal (Albaret, 1987). In the Ebrie Lagoon, spawning seemingly only takes place where the salinity is >5 (Gerlotto, 1979). Such a tolerance to salinity by a fish species is an exception. Its adaptability to environmental stress (of natural or anthropogenic origin) suggests that E. fimbriata possesses different ecophysiological responses to various environmental conditions. Other species tolerate toxic substances. For example, Fundulus heteroclitus survives in high concentrations of dioxin (Nacci et al., 1999) and shows a genetic response to pollution (Kirchhoff et al., 1999).
Several questions arise from this analysis. For example, can this particular adaptation be transmitted from generation to generation? Further, are there one or more populations of E. fimbriata in the Ebrie Lagoon? Different L50s could mean that populations evolved separately, as suggested by Albaret and Charles-Dominique (1982). However, the existence of two separate populations in this instance is unlikely, because E. fimbriata is migratory. Exchanges between bays are probable and, even if rare, such exchanges would be sufficient to homogenize the pool of genes. Another hypothesis is that the environment, and specifically the pollution, triggers the adaptive response. Such intra-population plasticity has been observed elsewhere for other species. For example, the tilapia O. niloticus rapidly adapts its age and size at first maturity when local environmental conditions vary (Duponchelle and Panfili, 1998). Also, Stergiou (1999) related significant changes in red bandfish Cepola macrophtalma L50 and age at first maturity to food supply and temperature. Other factors, such as predation pressure or geographic distribution, may trigger phenotypic plasticity and changes in size at first maturity (Belk, 1995; Holopainen et al., 1997; Sampson and Al-Jufaily, 1999).
The question still remains whether E. fimbriata can be used as a bio-indicator species for the coastal system of western Africa. Fish community structure has been used as a stress indicator before (Adams et al., 1990; Fausch et al., 1990; Appelberg et al., 1995; Wichert and Rapport, 1998; Fitzgerald et al., 1999). However, for E. fimbriata, further ecotoxicological, enzymatic, and molecular biological studies are needed to determine its reliability as a biomarker. For instance, a relationship between molecular concentration in fish tissue and environmental pollution can be sought, as done for numerous other fish species (Gopal et al., 1997; Soimasuo et al., 1998; Bresler et al., 1999; Broeg et al., 1999).
More and up-to-date studies are clearly necessary to determine the age at first maturity and the age structure of E. fimbriata. Unfortunately, no otolith analysis has been carried out thus far in the Ebrie Lagoon, and such data are crucial to concluding whether the smaller size at first maturity observed for E. fimbriata in polluted environments is related to the species' precocious maturity, or whether the fish reproduce smaller only because the environment is limiting their growth (i.e. dwarfing).
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Acknowledgements |
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We thank E. Charles-Dominique from IRD, who helped us in providing data, and Gabriella Bianchi and an anonymous reviewer for their valuable comments on the draft text.
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References |
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