Hydrobiologia 232 : 157-168, 1992 .© 1992 Kluwer Academic Publishers . Printed in Belgium .

Effects of lindane and deltamethrin on zooplankton communities ofexperimental ponds

Abiba S . Tidou, Jean-Claude Moreteau & Francois RamadeLaboratoire d'Ecologie et de Zoologie, Bat . 442, Universite Paris-Sud, 91405, Orsay, France

Received 18 July 1990 ; in revised form 25 April 1991 ; accepted 31 July 1991

Key words: zooplankton, mesocosms, pollution, direct and indirect effects

Abstract

Two insecticides, lindane (321 tg 1 - ') and deltamethrin (13 tg 1 -1 ) were employed in a four mesocosmexperiment (two ponds of 10 m3 and two of 16 m 3 ) to asses the impact of water pollution by pesticides .Resistance of the different zooplankton species was variable and depended upon both the group andthe insecticide concentration . No effect of lindane was observed on macrozooplancton such as Cladoceraand Copepoda . In the deltamethrin-treated pond, all species of zooplankton were found dead a day afterthe treatment. The microzooplankton (Rotifera and copepod nauplii) were highly susceptible to bothinsecticides . Although the larvae of Chaoborus were present in the ponds after the treatments, their densitydecreased (less than 1 individual 1 - ') . The elimination of filter-feeding zooplankton by deltamethrin wasfollowed by an increase of the concentration of chlorophyll a in the post-treatment period . Two monthslater the original zooplankton population recovered, with the addition of a new and dominant species :Ceriodaphnia reticulata .

Introduction

The use of various pesticides in intensive agricul-ture can cause significant changes in the equilib-rium of non target organisms . In highly intensiveagricultural regions, the products used are oftenwashed out by rains and may pollute surface andground waters . Ramade et al. 1984; 1985) showedthat the benthic invertebrate populations of pondswere significantly altered in intensive agriculturalzones of Ile-de-France . The major effects ob-served were the decrease in density of some spe-cies and changes in community composition .

The evaluation of the ecological consequencesof pesticide use, is currently one of the major

157

preoccupations of ecotoxicological studies . Dueto the complexity of biotic interactions it is diffi-cult to assess the impact of insecticides, or otherpesticides on aquatic ecosystems, without effi-cient evaluation methods . The use of mesocosmsis a step to surmounting the difficulty since con-ditions in artificial ponds and enclosures are closeto those of natural environment (Solomon et al.,1980), yet a number of parameters may still becontrolled . Mesocosms are thus an intermediatestep between laboratory microcosms nd thenatural aquatic ecosystems (Lay, 1987) . Whilemost ecotoxicological research is concerned withthe acute toxicity of pesticides, their indirect anddirect effects have scarcely been studied (Hurlbert

1 58

et al., 1972; Kaushik et al., 1985; Lay et al., 1985,1987) .As a follow up of the work on natural ponds

(Ramade, loc . cit .) and ecotoxicological labora-tory studies on the effects of lindane and delta-methrin on aquatic invertebrates (Thybaud, 1987)we employed mesocosms presenting semi naturalcondition in order to study the effects of these twoinsecticides on aquatic communities. The presentstudy is a report on the impact of the two insec-ticides on the population dynamics of herbivouszooplankton communities which are an impor-tant trophic level in freshwaters (Pourriot &Champ, 1982) . The dynamics of some preda-tors (Chaoborus larvae) and of phytoplankton(as estimated by chlorophyll a concentration :Lorenzen, 1967) were also reported .

Among the microcrustacea collected in the me-socosms, cladocera were studied in detail becauseof their importance in the evaluation of aquaticpollution (Adema, 1978; Macrioroswki & Clarke,1980) .

Material and methods

Mesocosms

Four outdoor concrete ponds located on theCampus of the University of Paris-Sud (France)were used . The ponds were lined with blackpolyane plastic film 50 pm thick to avoid leakage .The volume of the two smallest ponds was ofapproximately 10 m 3 (2.5 m x 10 m x 0 .4 m) andthe others 16 m 3 (4 m x 10 m x 0 .4 m). The twosmaller ponds were used for Lindane experiment(pond A: control and pond B: lindane treatment)and the two largest for Deltamethrin (pond D :control and pond C : deltamethrin treatment) .

The bottom of mesocosms was covered with asandy sediment layer, 15 cm thick .

The mesocosms were filled with tape drinkablewater from the city water adduction system . Thiswater is neutral and slightly calcic .

The planctonic and insects macroinvertebrateshave spontaneously colonized the mesocosms .However some macrophytes and with them eggs

from invertebrates carried with the soil wereintroduced a few weeks after the mesocosmshad been filled. Three species were chosen :Ranunculus aquatilis L., Typha langustifolia L. andScirpus palustris L . ; a fourth demersal species,Ceratophyllum submersum L . was introduced tothe deeper parts of the mesocosm .

Treatment

The ponds were treated with a low concentrationof insecticide comparable to the doses applied byfarmers to their fields (ACTA, 1986) . Pond Breceived 321µg1-' of lindane and pond C13 pg 1 -1 of deltamethrin . Lindane (99,99%yisomer of hexachlorocyclohexane) is an old syn-thetic insecticide supplied by Pepro and stillemployed in France (Picot, 1983) .

Deltamethrin or (1R, 3R)-3 (2,2 dibromovinyl)-2,2 dimethylcyclo propane carboxylate of (S)-alpha cyano-3 phenoxy-benzyle, is one of the newsynthetic pyrethroid insecticide supplied by Rous-sel Uclaf in France (Tessier, 1982) .

Sampling

The organisms were collected with a 1 .5-literhorizontal dipper bottle, from November 1987 toJuly 1988 . Two samples of three liters were ran-domly collected from four predeterminedtransects in each pond . Sample water was filteredon a 63 µm sieve before fixation in 4% formal-dehyde. Thus all microcrustacea, Chaoborus lar-vae and small rotifers were recorded .

The physico chemical characteristics of thewater such as minimum and maximum tempera-ture, dissolved oxygen and pH, were measuredon each sampling occasion . All Crustacea werecounted, but copepod nauplii and rotifers weresubsampled and counted with a counting cell(Dollfus) using the method described byEdmondson & Winberg (1971) and Bottrell et al.(1976). The organisms were identified using keysby Scourfield et Harding (1958), Pontin (1978)and Amoros (1984) .

Acute toxicity in Daphnia pulex population

To study the immediate effect of the applicationof the insecticides on the zooplankton popula-tion, a number of D. pulex at different stages ofdevelopment were isolated in small plastic boxeswhich were submerged in each pond, one dayprior to treatments . Each box of 150 yl equippedwith a 250 ym mesh net, contained 15 similarsized daphnids . The number of individuals perbox was limited to 15 to avoid overcrowding . Thedead animals were counted in each box 24 hoursafter treatment .

Results

Due to their geometric similarity, the ponds pre-sented the same physico-chemical characteristics .The water temperature varied from 3 ° C in thewinter to 25 ° C in the summer . They ponds werenot deep (40 cm) and the water was continuallymixed by the wind . Consequently the temperaturevaried little between the surface and the bottom(about 1 'C) and the ponds were usually oversa-tured in dissolved oxygen . The water was slightlyalkaline (ph 8.2-8.5) . According to Caquet et al.(1989) deltamethrin disappeared four days afterthe treatment and only 10% of lindane still re-mained in the water seven weeks later (Thybaud,pers. com .) .

Rotifers

In the control ponds, the maximum densities ofrotifers were observed in April (see Fig . 1). Thesemaximum densities were followed by an impor-tant population decrease (90%) in May . How-ever, all rotifers disappeared immediately afterboth lindane and deltamethrin treatments, follow-ing which they remained rare throughout thecourse of the experiments .

Nauplii

In mid-April, the populations of nauplii were im-portant in the controls with a stable population in

1 59

pond A and a slightly declining population incontrol D (see Fig. 2). In spite of this differencein seasonal cycles in the control ponds, the acutelytoxic effects of lindane and deltamethrin wereclear since both nauplii populations were elimi-nated. By mid-June, two months after the treat-ment, they slowly began to reappear .

Copepodites and adult copepod populations

The abundance of adult copepod and copepoditepopulations were different in the controls (seeFig. 3). Both before and after treatment, the fluc-tuations of densities observed in the lindane-treated pond were parallel to those in control Abut on a slightly lower scale . Meanwhile, in thedeltamethrin treated pond, all instars of copepodsdisappeared and they recovered in the ponds twomonth later . Deltamethrin was more toxic thanlindane. The concentration of lindane employedwas not high enough to have an effect oncopepodite and adult copepod populations .

Cladocera

D. pulex was the most important species Clado-cera in the mesocosms . In the control pond A thepopulation increased progressively from Febru-ary to July while in the control pond D, it wasstable from the end of April to July . Similar vari-ations in population density were observed in thelindane-treated pond and in the control pond A .At the concentration used, lindane had no effecton cladoceran populations . Sanders & Cope(1966) showed that the EC 50 (the concentrationproducing a response in 50% of the population)of D. pulex for lindane was 460 pg 1 - ' (a higherconcentration than that used in the present study) .The density of Cladocera was important after thelindane treatment. However, the concentration ofdeltamethrin applied, killed all species of Clado-cera as well as rotifers and copepods (see Fig . 4) .

The elimination of zooplancton by deltamethrinwas followed by an increase in chlorophyll a con-tent (Fig . 5). Recovery of the cladoceran popula-

1 60

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tions started about two months after the treat-ment with the colonization of the pond by a newspecies Ceriodaphnia reticulata (85.6% of thepopulation) . C. reticulata occurred only in thetreated ponds (see Fig . 6) with higher numbers inpond C (92 individuals 1 -1 ) than in pond B (lessthan 1 individual l -1 .

3013188 2914188 2915188 2816/88

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Fig . 1 . Seasonal abundance of Rotifera in the ponds (N = individuals per liter ; BAC A and BAC D = ControlBAC B = Lindane treated pond, BAC C = deltamethrin treated pond) . .

Other invertebrate : Chaoborus larvae

Larvae of Chaoborus were present in all ponds,but more numerous in the controls . In spite oftheir low densities in both of the treated ponds,they were less susceptible to lindane than to del-tamethrin, the latter reduced their numbers by98% (see Fig . 7) .

ponds,

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Acute toxicity test on D . pulex

Table 1 represents the acute toxicity of the twoinsecticides . At the concentration used, delta-methrin eliminated all daphnids isolated inpond C, regardless of size . Lindane however,affected J2 and J3 juveniles more than J1 juve-

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161

Fig. 2 . Seasonal abundances of Copepods nauplii in the ponds (N = individuals per liter ; BAC A and BAC D = Control ponds,BAC B = Lindane treated pond, BAC C = deltamethrin treated pond)

niles whose numbers were not significantlyreduced . Egg bearing females were more tolerantthan non reproductive females . These results arein agreement with Gliwick and Sieniawaska(1986) and confirm the resistance of egg bearingdaphnids to lindane .

1 62

Discussion

Many laboratory tests and field surveys haveshown the toxicity of lindane on aquatic inverte-brates (Sanders & Cope, 1966 ; Bodenstein, 1972 ;Edward, 1977 ; Lay et al ., 1987) . Despite the scar-city of tests on deltamethrin (Dejoux, 1983 ;Lhoste & L'Hotellier, 1982), synthetic pyrethroidshave been shown to be very toxic to aquatic or-

log (N + 0,01)

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Fig . 3 . Seasonal abundances of Copepodites and adult copepod in the ponds (N : Individuals per liter ; BAC A andBAC D = Control ponds, BAC B = Lindane treated pond, BAC C = deltamethrin treated pond) .

ganisms (Coasts & O'Donnell-Jeffrey, 1979 ;Mulla et al ., 1981 ; Stephenson, 1982) . Althoughthere was a natural decline in the population ofthe microzooplankton (especially rotifers), it isobvious that the application of lindane and del-tamethrin to the mesocosms was lethal to filter-feeding microzooplankton . These results are inagreement with those of Lay et al. (1987) on thetoxicity of low concentrations of lindane on roti-

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Fig. 4 . Seasonal abundances of Cladocera in the ponds (N : Individuals per liter; BAC A and BAC D = ControlBAC B = Lindane treated pond, BAC C = deltamethrin treated pond) .

fers and copepod nauplii . It appears that naupliiare particularly sensitive to organochloride insec-ticides, as been shown in Ramade & Thybaud(1986). DDT is known to arrest metamorphosisof Pseudodiaptomus cornatus nauplii at dose of0.01 ag 1 -1. An indirect affect of the eliminationof filter feeding zooplankton by deltamethrin wasthe phytoplankton bloom . This demonstrates the

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163

ponds,

impact a pesticide may have through it's effect ofthe herbivorous zooplankton which graze on phy-toplankton (Hurlbert, 1975; Papst & Boyer, 1980 ;Parson et al ., 1986) .

Due to the complex nature of the mesocosms,the insecticides may not have been the only fac-tors causing the elimination of the microzoo-plankton population . The interspecific compe-

164

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tition which may have been responsable forthe decrease in microzooplankton density in thecontrol, may have added itself to the effect oflindane in the treated pond, resulting in thecomplete elimination of microzooplankton .Larger filter-feeding zooplankton (Cladocera andcopepodites) were not affected by lindane, theycould have competitively eliminated the rotifers

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Fig . 5 . Evolution of Chlorophyll a content in pond. Log (Chla) =Log of chlorophyll a concentration (in pg 1 - 1 ), Zoo .herb. = Zooplancton herbivore.

-& Chloro. a

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as been shown by Hurlbert et al . (1972) andGilbert (1985; 1988). The total elimination ofcopepod nauplii clearly demonstrates the hightoxicity of lindane on microzooplankton .

Results from literature show that when themacrozooplankton community is eliminatedby water pollution (Muirhead-Thomsom, 1971 ;Kaushih et al ., 1985; Halbach, 1984) or by

log (N + 0,01)3 .0

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1 65

Fig. 6 . Seasonal abundance of Ceriodaphnia reticulata (Cer. ret) and Daphnia pulex (Dap. pul.) population (N : Individuals per liter) .

predators (Grygierek et al., 1966; Hurlbert &Mull a, 1981) the microzooplankton communitygrows abundantly in the absence of its main com-petitors. In these cases, microzooplankton com-munity is well established by the time the macro-zooplankton recovers . In the present study,however, both micro- and macrozooplanktoncommunities were eliminated, and the first to

recover were the macrozooplankton . The pres-ence of thee effective competitors further mayhave hindered the recovery of the microzoo-plankton. These results show that deltamethrin,in contrast to other insecticides, is extremely toxicand has a wide spectrum of action in aquaticecosystems . The elimination of rotifers from thetreated ponds may in part be attributed to their

1 66

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natural decline which was observed in the con-trols. Therefore the effects of the insecticidesadded themselves to the factors influencing theseasonal variation of the rotifer populations .Laboratory tests by Gliwicz & Sieniawska

(1986) showed that feeding Cladocera with lin-dane treated Chlorella (50 pg l - ') caused a

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Fig . 7 . Seasonal abundances of Chaoborus larvae in the ponds (N : Individuals per liter ; BAC A and BAC D = Control ponds,BAC B = Lindane treated pond, BAC C = deltamethrin treated pond) .

reduction in the frequency of mandibular mouve-ment they suggested a subsequent decrease in fil-tration rate . However, in our case, the possibledisruption of the feeding rate was insufficient toprovoke a decrease in population density . In factthe abundance of cladoceran populations in thelindane-treated pond increased, indicated that

Table 1 . Acute toxicity of lindane and deltamethrin on D. pulex over 24 hours .

Stages

nr. females (> 1 .8 mm)eb . females (> 1 .8 mm)juveniles (stage I)juv . (stage II)juv . (stages III, IV)

Total

other important factors controlling reproduction,such as temperature and food availability wereprobably sufficiently favorable to compensate thepossible decrease of the frequency of mandibularmouvement caused by lindane . Since Cladocerawere unaffected by lindane, there was no changein the chlorophyll a content of the pond (seeTidou, 1989), despite the elimination of rotiferpopulations. The effects of lindane and delta-methrin, demonstrate the impact of insecticideson the zooplankton and phytoplankton relation-ships in aquatic ecosystems . The occurrence ofC. reticulata in the treated ponds appeared to bean indirect effect of the insecticides . The impor-tant reduction of Chaoborus larvae by delta-methrin allowed the development of theirpreferred prey, C. reticulata . C. reticulata compet-itively dominatesD. pulex (Lynch, 1979), thus im-peding the recovery and the development of thelatter .

Conclusion

The impact of insecticides on aquatic environ-ments is complex. It is the result of both theirdirect and indirect effects on organisms as well asthe changes in natural ecological factors . In somecases, as with the rotifers, environmental factorscan mask the effects of pollution by insecticides .

Treated C deltamethrin

nr females : non reproductive females ; eb. females : egg pearling females ; juveniles (stage I) : juveniles < 1 mm ; juv . (stage II) : ju-veniles from 1 to 1 .49 mm ; juv . (stages III, IV): juveniles from 1 .5 to 1 .8 mm; N : number of animals ; D : number of deaths ; %D :percentage of deaths .Binomial test : ns : non significantly different (p>0 .05) ; *: significantly different (p<0 .005 ; ** : significantly different (p<0 .01).

1 67

However, in cases of acute toxicity, the effect ofthe insecticides was extremely clear, resulting ina phytoplankton bloom due to the elimination ofthe grazers . This could have an consequence onthe transfer of the energy through the trophicchain .

This study showed that it is at times impossi-ble to extrapolate the impact of a pollutant on anaquatic ecosystem from single species laboratorytests . Artificial mesocosms remain an efficientmethodological tool in ecotoxicological studiesbut they may be simplified to better emphasize thereal effects of pesticides on aquatic communitiesas been shown by Lay et al. (1987) .

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D

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2480 31 38 .8 ** 120

1680 17 21 .3 * 160

14

349 99 28 .4 ** 625

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