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Trente ans de lutte contre l’onchocercose en Afrique de l’Ouest. Traitements larvicides et protection de l’environnement

 | 
Laurent Yaméogo
, 
Christian Levêque
, 
Jean-Marc Hougard

Références des articles présentés sur le cédérom / Papers references presented on CD-ROM

Effects of larvicide treatment on invertebrate communities of Guinean rivers, West Africa

Giuseppe Crosa, Laurent Yaméogo, Davide Calamari, Fafondé Kondé y Kélétigui Nabé

Resumen

Biological and hydrological data collected from 1984 to 1998 in three Guinean rivers were analysed to evaluate adverse effects of biological and Chemical larvicides applied for the control of blackfly Simulium damnosum, vector of the parasitic digenean worm Onchocerca volvulus. Although most of the variation in invertebrate populations were flow-related, larvicide applications affect community structure reducing the abundance of the most sensible taxa. In spite of these results, in the long term the rarefaction of some invertebrate taxa (i.e. Tricorythidae) does not cause a significant reduction of total invertebrate densities because of the corresponding increase of other taxa (i.e. Hydropsychidae and Philopotamidae). The functional structure of the communities is also not affected.

Texto completo

Introduction

1From 1974 to 1998, up to 50 000 km of West African rivers located in an area of approximately 1 300 000 km2 were treated with larvicides to eliminate the aquatic stage of the blackfly Simulium damnosum, vector of the human parasite Onchocerca volvulus (Zimmerman et al., 1992). The control agents were aerial sprayed weekly, on the basis that the development of the aquatic stage of the vector, from egg to pupae, is around 1 week.

2At the beginning of the programme, the biological control agent. Bacillus thuringiensis serotype H-14, and temephos, an organophosphorus compound, were the only insecticides applied. From 1979, the appearance of certain forest cytotypes of the vector resistant to temephos (Guillet et al., 1980) enforced a search for new compounds and the implementation of a renewed strategy based on the rotational application of the larvicides, with intervening periods during which application was suspended. The new compounds applied were: chlorphoxim and pyraclophos (organophosphorus compounds), permethrin (pyrethroid), carbosulfan (carbamate) and etofenprox (pseudopyrethroid) (Hougard et al., 1997). A comprehensive review on the environmental assessment of the applied larvicides has been published (Calamari et al., 1998) and the environmental behaviour and mode of action of the various substances applied are discussed in Dejoux et al. (1985) and Yaméogo et al. (1991).

3The strategy for larvicide application within the programme (Onchocerciasis Control Programme – OCP), both in term of compounds and frequency of spraying, has been carefully planned and, to control the possible effects on the non-target fauna, monitoring has been undertaken applying the criteria and the advice of an independent Ecological Group. An aquatic environmental monitoring programme was established and operationally applied before the application of larvicides to monitor their possible side-effects on aquatic communities. Two biological components were identified and regularly sampled during all periods of larvicides spraying: benthic invertebrates and fish. Among the principles that define the acceptability of new insecticides is one relating to evaluation of induced modifications in aquatic communities. This is indicated within the mandate of the Ecological Group: “temporary and seasonal variation in invertebrate populations, beside the Simulium, could be accepted”.

Figure 1. Schematic representation of the analysed data. The number of the weekly applications of larvicides plus the number of invertebrates samples are detailed for each year.

4A number of studies were published to evaluate the possible side-effects on the fish and non-target insect populations in various areas and during different periods (i.e. Lévêque et al., 1988; Yaméogo et al., 1988).

5This paper presents and discusses the taxonomie and trophic structure variation of benthic invertebrate communities collected from 1984 to 1998 in three Guinean rivers. The objective of the study was to verify whether any short-, medium-or long-term biological variations can be related to the larvicides application.

6The time periods to which these relate are: (1) short-term: any change in the biological structures recovering within a season (wet or dry season); (2) medium term: any change in the biological structures recovering within one complete hydrological cycle (wet and dry season); (3) long-term: any permanent change in the biological structures.

7The rationale we adopted to analysis the data collected in rivers located within a limited spatial range (one country) was intended to avoid possible bias due to the ecological differences that characterise water courses flowing in dissimilar regions. Moreover, the rivers were selected according to the types of treatment and, among the other Guinean rivers, because of their detailed series of biological and hydrological data.

Materials and methods

8Since 1987. the studied rivers were treated with the biological control agent B.t. H14, the organophosphates temephos and pyraclophos, and the pyrethroid permethrin. The time extern of the treatments, the available discharge data and the number of invertebrate samples for each of the monitored year are shown in Figure 1. Invertebrate sampling started 3 years before the beginning of larvicide treatment in the Milo and Niandan rivers. No pre-treatment samples are available for the Dion river for which invertebrate collection started in 1990, 3 years after the first larvicide application.

9The invertebrates were collected in shallow riffles over rock substrate using a modified 25x25 Surber sampler (Dejoux et al., 1979), the sampling stations were chosen because, being the breeding sites of S. damnosum, these areas were subject of direct application of the larvicide compounds. For each site, 5 samples were replicated and the mean number of individuals were calculated.

10All the sampled invertebrates were classified at family level and to their trophic role: predators, shredders, scrapers and filtering or gathering collectors. This second classification method is based on the association between a limited set of feeding adaptations found in freshwater invertebrates and their basic nutritional resource categories (Cummins, 1973).

11Since the invertebrates collected were classified with respect to their taxonomie level as well as to their functional feeding group (trophic role), the analysis of the biological variation focused on both structural and functional attributes. Whereas the first aspect of concern, beside the faunistic interest over loss of global biodiversity. is related to the quality of the biomass available for the upper trophic levels, the second one is related to the quantity and stability of energetic flows. On account of the position of invertebrates in the first levels of river food webs, changes in energy flows can be an alarm signal about greater detrimental effects upon the ecological characteristics of the whole river system.

12The variables used for the analyses were the total number of invertebrates collected in each Surber sample (individuals/625 cm–2) and the percentage of each trophic guild.

13For detecting any change in the taxonomie composition or in the relative abundance of each taxonomie unit. Principal Component Analysis (PCA) was applied to the relative log-transformed invertebrate abundance expressed in term of the number of individuals for each taxa. The resulting first two axes were then opportunely rotated (45°) to facilitate the description of variation in the scores for each axis.

Figure 2. Samples ordination scores resulting from the Principal Component Analysis of invertebrate data collected in the three Guinean rivers studied: dotted line = Milo; unbroken line = Niandan; bold dotted line = Dion. In the upper graph, the relationship between the first axes ordination scores and the densities of the total classified invertebrates are shown and the arrow marks the beginning of the larvicides application.

14An invertebrate data matrix was created by assembling all the samples classified according sampling date and river location.

15Sample ordination scores of the first two components resulting from the analysis are separately illustrated along with sampling time in order to outline any time-related biological variation.

16The water regime of the selected rivers shows a defined seasonal pattern with high discharges from June-July to December followed by low discharges during the dry season (January to May–une); details of hydrological and Chemical characteristics of the rivers and of the flowing waters are reported in Iltis & Lévêque (1982) and in Moniod et al. (1977).

Results

17Ordination scores of the log-transformed invertebrates data on the first two axes are shown in Figure 2. In the upper part of the graphs, the arrow marks the beginning of the larvicide treatments, and each point in the figure represent a samples ordination score plotted in correspondence of the sampling day (x-axis).

18The ordination diagrams account for 35% of the total invertebrates variance: 28% 1st axis, 7% 2nd axis. As discussed in the following, the ordination scores represent mean invertebrate densities (1st axis) and the relative abundance changes of the sampled taxonomic groups (2nd axis).

Figure 3. Long-term lime related variation of the average invertebrates densities (individuals 625 cm-2) sampled in the studied Guinean rivers. Boxes represenl the standard errors of the calculated means values.

19The two axes’ ordination scores present different time-related patterns. The first one results from the seasonal variation of the sample ordination scores and shows no evidence of any long-term trend in invertebrate community structures. Medium-term variation is evident for all the three sampled rivers, and reflects seasonal changes in invertebrate densities as demonstrated by the significant correlation between the first axis samples ordination scores and mean invertebrate densities (r=0.8, P<0.001) shown within the upper graph of Figure 2.

20With respect the 2nd ordination axis, a long-term trend in ordination scores for the sample is evident from the corresponding graph. Although the maximum values resulting during the pre-treatment period still occur throughout the sampling period, soon after the beginning of the treatments the samples scores for the 2nd axis reduce their variation range. Considering that this trend can not be reasonably related to natural factors presenting such a continuous change as the river hydrology, a detailed analysis of the taxonomic units showing significant time related trends are provided in Figure 3.

21Tricorythidae and Leptoceridae show extremely low abundance since, respectively, the first and the fifth year from the beginning of the larvicides applications; Tricorythidae in particular were absent from 1990 and for the remainder of the sampling period (until 1998). Conversely, Hydropsychidae and Philopotamidae show slightly higher abundance values during the treated years compared to the densities measured during the pre-treatment period. As a result of the density increase of the above taxonomic units, total invertebrate abundance does not show a significant reduction during the final years of the monitoring period or any other related long-term trend.

Figure 4. Total invertebrates densities after pyraclofos applications measured in Niandan river during 1993–1995.

22To analyse of the short-term effects of larvicide applications on invertebrate communities, and to provide a description of their resistance and resilience, we selected the data sampled in the Niandan river during the years 1993–1995. This period was chosen because of the low invertebrate density measured during 1995, and also due to the fact that, during these years, invertebrate communities in the Niandan river were sampled after pyraclophos applications with different time lags; from a minimum of 11 days after pyraclofos treatments up to 79, with intermediate lags. In addition, previous studies provided experimental evidence of the severity of this Chemical in relation on the nontarget aquatic fauna. Finally, the hydrological cycles within the selected years do not present in Niandan river any significant difference.

23The invertebrate density measured during the above selected period is shown in Figure 4. In the graph, each abundance value is plotted with respect to the number of days elapsed since pyraclofos treatment and the maximum and mean invertebrate densities measured during the pre-treatment period are marked as reference values.

24Although the invertebrates sampled within a short period of time after pyraclofos application (11–13 days) show low densities, in all probability induced by the Chemical, as the time elapsed since treatment increases, the communities recover their original densities. After a period of 3–8 weeks, invertebrate abundance recovers to within the range of variation measured during the pre-treatment years.

25To address the last question of this study, regarding the possible side-effects of larvicide applications on invertebrate trophic structure, the time-related variation of the relative abundance of the principal functional groups sampled in Milo river are presented as representatives of the situation typical response of the studied Guinean rivets (Fig. 5). To facilitate the interpretation of the seasonal biological variation, the hydrograph is plotted on the same graph of analysed trophic guilds and the missing flow values of the period 1984–98 are replaced by the average monthly discharges calculated using the available data.

26The most abundant trophic guilds are the gathering and the filtering collectors that show seasonal and, consequently, flow-related variations similar to those of the other two sampled rivers: a dominance of the gathering collectors at the end of the wet season that decreases during the dry season.

27Although the data preceding the commencement of applications of larvicide are themselves poorly correlated with seasonality, this cyclic pattern is described, with narrower variation ranges, by the communities sampled during the pre-treatment period

28The graphs indicate that the larvicide applications affect the trophic structure of the invertebrate communities, reducing the gathering collectors abundance during the dry season. However, after each wet season, the two trophic guilds show percentages similar to those calculated for the pre-treatment samples. For example, the low proportion of gathering collectors during March 1995 fell to 10%, a value very different from the percentages measured for the pre-treatment samples although, by November of the same year, the gathering collectors abundance was more than 90%. This finding suggests that the larvicides effect on the relative abundance of the trophic guilds of the invertebrate communities is not permanent: no more than 7–8 months after the first sign of alteration.

Discussion

29The data collected provide experimental evidence of the variation in invertebrate communities during the Onchocerciasis Control Programme in Guinea. These allow an evaluation of the biological response to larvicide applications, with reference to short-, medium- and long-term trends addressed in the present study.

Figure 5. Milo flow rates (solid lines) and relative percentages of the two mos abundant invertebrate functional groups (dotted lines). The missing flow values of the period 1984–98 are replaced by the average monthly discharges calculated using the available data. In the graphs, the first year of treatment is marked by an arrow.

30Most of the biological variation measured during the monitored period in the three studied Guinean rivers is flow and medium-term related. The variability of the total invertebrate density, showing higher values during the dry season, results mainly regulated by the natural hydrological cycle and does not shows any significant trend within the monitored period.

31Also, trophic structure appears not to be permanently affected by larvicide applications; unfortunately, the 1988 year-class is missing and this make more difficult the interpretation of recovery following treatment.

32Although the amplification of the variation in invertebrates trophic guilds occurring during the treatment period may be induced by the applied larvicides, the trophic structures show a complete recovery at the end of each high water period. It has to be noted that the recovery of population may be due to in-section resilience as well to recolonisation, from unaffected reaches upstream and in tributary, between wet cycles.

33Both of these two aspects of the invertebrate communities, total density and trophic structure, suggest they are highly resilient with respect to natural driving forces (hydrology) or to induced stresses (larvicide application).

34Examining the present data in the context of published papers on the same subject, the results of the analysis of the invertebrates sampled during the Onchocerciasis Control Programme show that, with reference to the pre-treatment observations, and during B.t. applications, the relative abundance of the gathering collectors decrease. Conversely, during the application of Chemicals such as permethrin and phoxim, the filtering collectors are strongly affected (Crosa et al., 1988). This differing response between invertebrate trophic structures can be partially justified by the larvicide properties and the feeding habits of the invertebrates; for example the gathering collectors feed on surface deposit and thus can be more affected by B.t. because to its rapid adsorption to soil particles (Tuosignant et al., 1993). Since the biological control agent was applied only during the low water periods (up to 1 m3 s–1), the above consideration can partly explain the density reduction of the gathering collectors measured during the low water periods, and suggests a direct effect of B.t. application on invertebrate trophic structures.

35As for short-term biological variation induced by larvicide application, the data collected in the Niandan river during the period 1993–95 suggest that the Chemical shock, although affecting the invertebrate communities and reducing their total density, are short-lasting and in the quoted example result completely overcome after a period of 3–8 weeks.

36Analysis of long-term trends in changes in invertebrate taxa demonstrates that the rarefaction of Tricorythidae and Leptoceridae in the studied rivers may be induced by the application of larvicides. Considering the above discussed short-term recovery capabilities of the invertebrate communities, recolonization of river habitats by the above quoted taxa will probably be accomplished within a short period after the conclusion of the programme.

Conclusion

37In evaluating biological variations, we adopted the concept of “significant ecological change” used by Onchocerciasis Control Programme in assessing the ecological impact of larvicide application (Lévêque et al., 1977). Within the mandate of the Ecological Group, two criteria were indicated: “the vector control activities should not reduce the number of invertebrate species, nor cause a marked shift in the relative abundance of species”; and “temporary and seasonal variations in invertebrate populations other then Simulium could be accepted.” With reference to these criteria, the biological variation we have measured in the regional contest of Guinea can be considered ecologically acceptable.

Acknowledgements

38We thank the anonymous reviewers for helpful comments and suggestions on improving the manuscript.

Bibliografía

References

Calamari. D., L. Yaméogo, J. M. Hougard & C. Lévêque, 1998. Environmental Assessment of Larvicide Use in the Onchocerciasis Control Programme. Parassitology Today 14: 485–489.

Crosa, G., L. Yaméogo, D. Calamari & J. M. Hougard, 1998. Long term quantitative ecological assessment of insectides treatments in four African rivers: a methodological approach. Chemosphere 37: 2847–2858.

Cummins. K. W., 1973. Trophic relations of aquatic insects. Annts Rev. Ent. 18: 183–206.

Dejoux, C., F. M. Gibon & L. Yaméogo, 1985. Toxicité pour la faune non-cible de quelques insecticides nouveaux utilisés en milieu aquatique tropical. Rev. Hydrobiol. trop. 18 : 31–49.

Dejoux, C., J. M. Elouard, C. Lévêque & J. J. Troubat, 1979. La lutte contre Simulium damnosum en Afrique de l’ouest et la protection du milieu aquatique. C. R. du Congrès de Marseille sur la lutte contre les insectes en milieu tropical 2 : 873–883.

Guillet, P., H. Escaifre, M. Ouedraogo & D. Quillevere. 1980. Mise en èvidence d’une rèsistence au tèmèphos dans le complexe Shuulium daninosum (S. sanctipauli et S. soubrense) en Cote d’Ivoire dans la Zone du Programme de Lutte contre l’Onchocercose dans la Règion du Bassin de la Volta. Cah. O.R.S.T.O.M. Sèr. Ent. Mèd. Parasitol. 17: 291–299.

Hougar, J. M., L Yaméogo, A. Seketeli, B. Boatin & K. Y. Dadzie, 1997. Twenty-two years of blackfly control in the Onchocerciasis Control Programme in West Africa. Parassitology Today 13:425–431.

Iltis, A. & C. Lévêque. 1982. Caractéristiques physico-chimiques des rivières de Cote d’Ivoire. Rev. Hydrobiol. trop. 15 : 115–130.

Lévêque. C., M. Odei & M. Pugh Thomas, 1977. The Onchocerciasis Control Programme and the monitoring of its effects on the riverine biology of the Volta River Basin. In Perring. F. H. & K. Mellanby (edst. Ecological Effects of Insecticides. Linn. Soc. London 133–143.

Lévêque. C., C. P. Fairhurst, K. Abban. D. Paugy, M. C. Curtis & K. Traore. 1988. Onchocerciasis control programme in West Africa: ten years monitoring of fish populations. Chemosphere 17:421–440.

Moniod. F., B. Pouyard & P. Sechet, 1977. Le Bassin du fleuve Volta. Monographies hydrologiques, O.R.S.T.O.M., 5.

Tousignant. M. E., J. L. Boisvert & A. Chalifour, 1993. Loss of Bacillus turingiensis var. israelensis larvicidal activity and its distribution in benthic substrates and hyporheic zone of streams. Can. J. Fish. aquat. Sci. 50: 443–451.

Yaméogo, L., J. M. Tapsoba & D. Calamari. 1991. Laboratory Toxicity of Potential Blackfiy Larvicides on Some African Fish Species in the Onchocerciasis Control Programme Area. Ecotoxicol. Environ. Saf. 21: 248–256.

Yaméogo, L., C. Lévêque, K. Traore & C. P. Fairhurst, 1988. Dix ans de surveillance de la faune aquatique des rivieres d’Afrique de l’ouest traitée contre les simules (Diptera: Simuliidae), agents vecteurs de l’Onchocercose humaine. Nat. can. 115 : 287–298.

Zimmerman, P. A., K. Y. Dadzie, G. De Sole, J. Remme, E. Soumbey Alley & T. R. Unnasch, 1992. Onchocerca volvulus DNA probe classification correlates with epidemiologic patterns of blindness. J. Infectious Diseases 165: 964–968.

Índice de ilustraciones

Leyenda Figure 1. Schematic representation of the analysed data. The number of the weekly applications of larvicides plus the number of invertebrates samples are detailed for each year.
URL http://books.openedition.org/irdeditions/docannexe/image/28806/img-1.jpg
Archivo image/jpeg, 55k
Leyenda Figure 2. Samples ordination scores resulting from the Principal Component Analysis of invertebrate data collected in the three Guinean rivers studied: dotted line = Milo; unbroken line = Niandan; bold dotted line = Dion. In the upper graph, the relationship between the first axes ordination scores and the densities of the total classified invertebrates are shown and the arrow marks the beginning of the larvicides application.
URL http://books.openedition.org/irdeditions/docannexe/image/28806/img-2.jpg
Archivo image/jpeg, 91k
Leyenda Figure 3. Long-term lime related variation of the average invertebrates densities (individuals 625 cm-2) sampled in the studied Guinean rivers. Boxes represenl the standard errors of the calculated means values.
URL http://books.openedition.org/irdeditions/docannexe/image/28806/img-3.jpg
Archivo image/jpeg, 86k
Leyenda Figure 4. Total invertebrates densities after pyraclofos applications measured in Niandan river during 1993–1995.
URL http://books.openedition.org/irdeditions/docannexe/image/28806/img-4.jpg
Archivo image/jpeg, 39k
Leyenda Figure 5. Milo flow rates (solid lines) and relative percentages of the two mos abundant invertebrate functional groups (dotted lines). The missing flow values of the period 1984–98 are replaced by the average monthly discharges calculated using the available data. In the graphs, the first year of treatment is marked by an arrow.
URL http://books.openedition.org/irdeditions/docannexe/image/28806/img-5.jpg
Archivo image/jpeg, 127k

Autores

Department of Landscape and Environmental Sciences, University of Milano-Bicocca, Piazza della Scienza, I-20126 Milano, Italy

Équipe Nationale ONCHO, Kankan, Guineé

Équipe Nationale ONCHO, Kankan, Guineé

© IRD Éditions, 2003

Condiciones de uso: http://www.openedition.org/6540