Arch Environ Contam Toxicol 53, 371–378 (2007) DOI 10.1007/s00244-006-0209-x
Survival and Growth of Palaemonetes argentinus (Decapoda; Caridea) Exposed to Insecticides with Chlorpyrifos and Endosulfan as Active Element M. C. Montagna Æ P. A. Collins
Received: 6 October 2006 / Accepted: 25 February 2007 Ó Springer Science+Business Media, LLC 2007
Abstract Pesticides with chlorpyrifos and endosulfan as active element are used for pest control on agricultural lands and are high-risk inputs in aquatic systems. The acute toxicity of these insecticides in the freshwater prawn Palaemonetes argentinus was evaluated. The results were used to determine the lowest observed–effect and no observed–effect concentrations. Individual growth of prawns in relation to chlorpyrifos and endosulfan exposure was analyzed. LC50 values to chlorpyrifos and endosulfan exposure were 2.98 lg L–1 and 14.10 at 24 hours and 0.49 lg L–1 and 6.28 lg L–1 at 96 hours of exposure, respectively. The size increment of prawns was the same in all treatments; cephalothorax length increased linearly per molt. The intermolt period was influenced by the toxic effect of pesticides during rearing time, and this decreased with the molt cycles compared with the normal growth pattern. The results suggest that juveniles of P. argentinus are sensitive to chlorpyrifos and endosulfan pollution. The family Palaemonidae (Decapoda; Caridea) contains a vast assemblage of species inhabiting all types of aquatic habitats: fresh, marine, and brackish waters. They are important organisms for aquaculture and candidates for crustacean research (Jayachandran 2001). Palaemonetes argentinus (Nobili 1901) is a species of ecologic interest because of its abundance in the north and centre of Argentina, in Uruguay, and in southern Brazil (Boschi M. C. Montagna P. A. Collins (&) Instituto Nacional de Limnologı´a (CONICET-UNL), Jose´ Macia´ 1933, (3016) Santo Tome´, Santa Fe, Argentina e-mail:
[email protected] P. A. Collins Facultad de Bioquı´mica y Ciencias Biolo´gicas, Escuela Superior de Sanidad, UNL Pje El Pozo s/n, (3000) Santa Fe, Argentina
1981; Lopretto 1995; Morrone & Lopretto 1995; Magalha˜es et al. 2003). P. argentinus in all life cycle stages were found in ponds, lakes, rivers, and brackish-water systems (Spivak 1997), where agricultural activity is intensive. Moreover, juveniles and adults form part of the aquatic trophic web; they are preyed on by several fish and bird species (Oliva et al. 1981; Beltzer 1983; Collins et al. in press). Aquatic ecosystems integrate agricultural areas by providing water and drainage channels. Pesticide application in farmlands increases the risk of insecticide input into lotic and lentic environments. Entry routes of pesticides into adjacent bodies of water resulting from normal agricultural use include spray drift and runoff (Cushing & Allan 2001; Walker et al. 2001; Newman & Unger 2003; Jergentz et al. 2005). In lands with agricultural activities, two common pesticides extensively used in pest control are the organophosphate insecticide chlorpyrifos (0,0-diethyl phosphorotioate of 0-3,5,6-trichloro- 2-pyridyl) and the organochlorine insecticide endosulfan (6,7,8,9,10,10-hexachloro-1,5,5a, 6,9,9a-hexahydro-6,9-methano-2,4,3-benzodioxathiopin-3oxide). Their concentrations are highly toxic to aquatic macroinvertebrates and fish; therefore, the concentrations of insecticides found in this country’s streams may pose a risk to aquatic life. The highest values of chlorpyrifos were 0.45 lg L–1 in water and 225.8 lg Kg–1 for suspended particles in streams; the endosulfan concentration was >318 lg Kg–1 in suspended particles (Jergentz et al. 2005). To evaluate the tolerance of P. argentinus to chlorpyrifos and endosulfan, two bioassays were conducted under laboratory conditions. In the first, the acute toxicity of each insecticide to P. argentinus juveniles was established by exposing them to different pesticide concentrations. The results were used to determine the lowest
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observed–effect (LOEC) and the no observed–effect concentrations (NOEC). In the second, the individual growth of the prawns exposed to different insecticides at sublethal concentrations was measured.
Materials and Methods Study Organism and Acclimation Conditions Freshwater prawns P. argentinus (mean ± SD 7.03 ± 1.052 mm cephalothorax length [CL]) were collected from the Salado River (latitude 31°39´S; longitude 60°41´W) near the Parana´ River floodplain (Santa Fe, Argentina), which has a mean discharge varying between 16,000 and 60,000 m3s–1 (Iriondo 2004). Juveniles from the same cohort were acclimated in glass aquaria with groundwater (artificial pond water [APW] pH 7.8, conductivity 900 lS L–1, dissolved oxygen 6 ± 0.50 mg L–1, and hardness 383 mg CaCo3 L–1) to laboratory temperature (25°C ± 1°C) and photoperiod (14 hours light to 10 hours dark) for 15 days. They were then they were placed in isolated containers for 1 molt cycle. The prawns were fed ad libitum with a pelletized diet prepared in the laboratory (36% proteins and 10% lipids) (Collins & Petriella 1996). Chemicals The insecticides used were Terminator Ciagro, containing 48% chlorpyrifos, and Zebra Ciagro, containing 35% endosulfan (Ciagro SA, Buenos Aires, Argentina), as active ingredient. The products, which were in liquid form, were diluted with double-distilled water to prepare solutions of the required concentrations. These insecticides are widely used in pampean agroecosystems (Argentina). Terminator Ciagro and Zebra Ciagro products, with all of their components, were used in the experiments. The concentrations used were considered nominal for these commercial products. Acute Assays Insecticide toxicity was evaluated by acute test (96 hours) according to standard static bioassay procedures outlined by the United States Environmental Protection Agency (USEPA 1975). In all assays, glass containers (26 cm diameter and 11 cm high) filled with 3 L APW were used. Ten juvenile prawns in the intermolt stage, previously collected and acclimated, were placed in each container. The tested nominal concentrations for chlorpyrifos were 0.011 to 5.760 lg L–1 and for endosulfan were 0.976 to 15.625 lg L–1; the dilution factor was 0.5. Before this stage, we performed a preliminary test to evaluate potential
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background exposure concentrations. This test was carried out in triplicate and included the control. Control tests were conducted in APW without pesticide during the same period. Mortality was recorded every 24 hours, and dead animals were removed from the glass containers. Effects on prawn behaviour and locomotion activity were observed at the different concentrations. These elements were evaluated by three direct observations. Each one took 10 minutes and these activities were considered when they were not interrupted by a time lapse. Chronic Assays: Individual Growth Chronic assays were conducted to evaluate the individual growth effects on prawns exposed to sublethal concentrations of chlorpyrifos and endosulfan. Before the experiments, prawn CLs were measured (6.85 ± 1.180 mm), and the first ecdysis was discarded. Four days after this molt, during the intermolt stage, the experimental prawns were placed into the glass containers to test the different insecticide concentrations; the control group was tested in APW without the insecticides. Each test and control group consisted of 20 juveniles, each housed individually in one of 20 glass containers (180 ± 1.5 ml capacity). The nominal pesticide concentrations used were 0.005, 0.011, and 0.022 lg L–1 chlorpyrifos and 0.122, 0.244, and 0.488 lg L–1 endosulfan. Water, with and without pesticide, in each container was renewed (70%) with newly made air-saturated solutions every 2 days. Molting and mortality were checked and recorded daily. Before feeding prawns with the pelletized diet, exuviae were collected, and dead prawns were recorded and removed and excess food removed to preserve medium quality. To decrease stress from handling, CLs were determined by measuring the exuviae. The duration of chronic assays corresponded to the time for four molt cycles. Statistical Analysis Three parameters (LC50, LOEC, and NOEC) were calculated to measure variations in insecticide toxicity. LC50 values and their 95% confidence limits for 24-hour intervals were estimated with the standard method of probit analysis as described by Finney (1971). Statistical comparison of LC50 values was carried out using one-way analysis of variance (ANOVA), and differences in the slopes between two insecticides were tested with Student t test. Pairwise comparisons of means were performed using Tukey’s posttest (Zar 1996). The LOEC was the lowest concentration that produced a significant toxic response, and the NOEC was the highest concentration that did not produce a significant toxic response. LOEC and NOEC were determined by testing the response in each concen-
P. argentinus Exposed to Chlorpyrifos and Endosulfan
CLt+1 (postmolt) = a + b CLt (premolt),
8
A 7 6 5
-0.025 4x
y = 4.8232e 2 R = 0.9609
-1
LC50 (µg L )
tration group and comparing responses with those of the control group (Dunnett test) (Zar 1996). Statistical analysis between treatments was carried out to determine differences in growth parameters (intermolt period and increase in size) during the experimental period using ANOVA and Tukey’s posttest (Zar 1996). Insecticide effect on size increment was examined by linear regression:
373
4 3 2
where a is the CLt+1 intercept, and b is the constant of growth (Collins & Cappello 2006).
1 0 0
Results
24
48
72
96
120
Time (hours)
Acute Assays
40
No prawns died in the control groups during the experiment, but mortality started at 48-hour 0.045 lg L–1 chlorpyrifos exposure; there was no survival at 96-hour 2.880 and 5.760 lg L–1 chlorpyrifos exposure. In endosulfan assays, the animals showed mortalities at 48-hour 1.953 lg L–1 endosulfan exposure, and all of them died at the highest concentration at 72 hours. For the effects of chlorpyrifos, significantly decreased survival was observed at concentrations 2.880 lg L–1 at 24 hours (ANOVA F(0.05 2 5) = 17.62; p < 0.0001, Tukey’s p < 0.05). At 96 hours, statistical significance for survival occurred at chlorpyrifos concentrations between 0.180 and 0.360 lg L–1 (ANOVA F(0.05,2,5) = 14.88; p < 0.0001, Tukey’s p < 0.05). For endosulfan, a significant difference (ANOVA F(0.05,2,5) = 45.36; p < 0.0001, Tukey’s p < 0.05) was found between the lowest (0.976 to 3.906 lg L–1) and highest (7.812 and 15.625 lg L–1) concentrations at 24 hours, and endosulfan (3.906 to 15.625 lg L–1) was responsible for the greatest mortality at the end of the experiment (ANOVA F(0.05,2,5) = 32.42; p < 0.0001, Tukey’s p < 0.05). The variation between LC50 values at 24 and 96 hours was 83.5% and 55.5% in chlorpyrifos and endosulfan assays, respectively; the difference in LC50 values was significant in all cases (chlorpyrifos ANOVA F(0.05,2,5) = 208.43; p = 0.0001; endosulfan ANOVA F(0.05,2,5) = 21.77; p = 0.0095) (Fig. 1 and Table 1). Their slopes values were similar (t(0.05,2,20) = 0.457), but chlorpyrifos exerted significantly greater toxicity (ANOVA F(0.05,2,5) = 25.04; p = 0.0075). In addition to mortality, parameters observed in these tests included some effects on behaviour, namely excitation and jerky movements of the prawns exposed to chlorpyrifos, especially when gently stimulated. In contrast, prawns in endosulfan solutions showed impaired mobility, loss of
35
B
-1
LC50 (µg L )
30 25
-0.0 10 8x
y = 16.274e 2 R = 0.8809
20 15 10 5 0
0
24
48
72
96
120
Time (hours)
Fig. 1 LC50 mean values, standard deviations (bars) and 95% confidence limits for P. argentinus juveniles exposed for 24 to 96 hours to chlorpyrifos (A) and endosulfan (B) solutions
response to mechanical stimulus, and lateral positioning. During the test period, there was a greater decrease in LOEC and NOEC values identified in the concentrations chosen for the chlorpyrifos experiment, and a there was less change between concentrations used for the endosulfan assay (Table 1). Individual Growth The size increase of P. argentinus was similar for both the control and the treatment groups during four molt cycles (90 days) (Fig. 2); there was a significant relation between CL premolt and postmolt (ANOVA p < 0.01) (Table 2). The intermolt period increased with the molt cycles in the control groups and treatment groups, except for the
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M. C. Montagna and P. A. Collins
Table 1 LC50, LOEC, and NOEC values for P. argentinus in lethal toxicity tests with chlorpyrifos and endosulfan. Time (hr)
Chlorpyrifos (lg L–1)
24
LC50
2.98 ± 0.155
LC50
LOEC
0.360
LOEC
3.906
NOEC
0.180
NOEC
1.953
96
Endosulfan (lg L–1) 14.10 ± 2.113
LC50
0.49 ± 0.255
LC50
6.28 ± 1.989
LOEC
0.046
LOEC
1.953
NOEC
0.023
NOEC
0.976
groups exposed to the greatest concentrations of the two biocids (Fig. 3). However, the intermolt period diminished in the second aor third molt cycles in groups exposed to the lowest concentrations of chlorpyrifos and endosulfan, respectively (Table 2 and Fig. 3).
9.5 Control 0.005 µg L-1 0.011 µg L-1 0.022 µg L-1 0.122 µg L-1 0.244 µg L-1 0.488 µg L-1
9 8.5 8
Chlorpyrifos
Endosulfan
A wide range of adverse environmental effects—including toxicity to beneficial insects, birds, a variety of plants, soil organisms, domestic animals, freshwater fish, and other aquatic organisms—has been linked to the organophosphate chlorpyrifos and the organchlorine endosulfan (Newman & Unger 2003; Jergentz et al. 2004). In Argentina, the recommended application levels on farmland, according to Camara de Sanidad Agropecuaria y Fertilizantes (2001), ranges from 0.21 to 6 L ha–1 and from 0.6 to 2.5 L ha–1 for chlorpyrifos and endosulfan, respectively. During rainfall and runoff events, insecticides are transported by rainwater and soil particles from the fields into the streams. In the aquatic system, these pesticides are transported by water across varying distances. Moreover, liquid droplets may rise to the surface or may be carried downward by sediment particles (Walker et al. 2001; Newman & Unger 2003). The application method (e.g., aeroplane) also facilitates release of biocids onto water surfaces. The chlorpyrifos and endosulfan values registered in natural environments (chlorpyrifos 0.45 lg L–1 in water and 225.8 lg Kg–1 for suspended particles; endosulfan 318 lg Kg–1 in suspended particles (Jergentz et al. 2005) were greater than LC50 values obtained in the laboratory, with decapods being the most affected. These levels may vary according season, rainfall, and farm culture methods (insecticide application, grain type, and integral use of the land). Many studies dealing with current levels of pesticides in Argentine pampean streams have reported (Jergentz et al. 2005) the highest concentrations of chlorpyrifos and endosulfan in sediment, suspended particles, and water. These investigators suggested that in many cases the concentration of pesticides in runoff and/or floodwater
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CLt+1 (mm)
7.5
Discussion
7 6.5 6 5.5 5 4.5 4 2
4
6
8
10
CLt (mm)
Fig. 2 Relation between CL premolt and postmolt of P. argentinus in control and different treatments of chlorpyrifos and endosulfan during three molt cycles
exceeded the water-quality criteria for freshwater established by the USEPA (1980, 1986a, 1986b) (0.041 and 0.056 lg L–1 for chlorpyrifos and endosulfan, respectively). Such insecticide concentrations were measured in species that were found in streams, that appeared abundantly in the region, and that were sensitive to both insecticides. An in situ bioassay indicated that 100% mortality occurred in the amphipod Hyallela curvispina and the prawn Macrobrachium borellii from insecticide application to farmland (Jergentz et al. 2004). However, information regarding the comprehensive toxic effects of these two pesticides on other inhabitants of the pampean streams, such as prawn P. argentinus, is scarce. Several publications have reported the sensitivity of P. argentinus to pollution in laboratory tests (Rodrigues Capitulo 1984a, 1984b; Montagna & Collins 2005; Collins &
P. argentinus Exposed to Chlorpyrifos and Endosulfan
375
Table 2 Growth of P. argentinus at different concentrations of insecticide and control Cephalothorax length (CL) a Control
b
r2
F
P
0.202
0.986
0.997
5738.87
< 0.0001
0.005
0.288
0.973
0.992
2557.43
< 0.0001
0.011
0.488
0.952
0.990
2536.05
< 0.0001
0.022
0.199
0.988
0.994
3427.87
< 0.0001
0.122
0.173
0.991
0.995
3949.11
< 0.0001
0.244
0.237
0.981
0.996
4754.15
< 0.0001
0.488
0.208
0.984
0.996
4960.39
< 0.0001
9.374
0.553
0.361
8.26
0.0057
0.005
9.921
0.357
0.156
1.59
0.2112
0.011
11.681
0.091
0.036
0.09
0.7638
0.022
10.782
–0.153
–0.057
0.21
0.6446
0.122
10.035
0.520
0.191
2.05
0.1576
0.244
10.158
0.459
0.174
1.72
0.1947
0.488
12.291
–0.236
–0.082
0.35
0.5579
Chlorpyrifos lg L–1
Endosulfan lg L–1
Intermolt period Control Chlorpyrifos lg L–1
Endosulfan lg L–1
a is the intercept and b is the constant of growth in the linear regression
Cappello 2006), indicating it to be a species of ecologic relevance for aquatic environments. In the present study, the lethal toxicity of chlorpyrifos to prawns occurred at lower concentrations than those reported for Daphnia magna at 48 hours (0.6 lg L–1) (Moore et al. 1998), and slightly higher than those indicated for several freshwater and marine species, e.g., shrimp Paratya australiensis (0.08 to 0.28 lg L–1 at 96 hours; Olima & Pablo 1997); the amphipod Ampelisca abdita and Korean shrimp Palaemon macrodactylus (0.16 to 0.25 lg L–1, respectively), or the amphipod Gammarus fasciatus and crayfish Orconectes pseudolimnaeus (0.32 to .18 lg L–1, respectively) (USEPA 1986b). The values recorded suggest the tolerance level to chlorpyrifos toxicity of some decapod crustaceans, with P. argentinus having a relative higher resistance and effective detoxification mechanisms. In contrast, this freshwater prawn was affected by endosulfan applications at lower concentrations than the values indicated for D. magna at 48 hours (62.0 lg L–1) (Schoettger 1970). Furthermore, LC50 values at 96 hours were different from those reported by Bhavan et al. (1997), Bhavan and Geraldine (2001), and Selvakumar et al. (2005), who determined values ranging from 0.16 to 0.19 lg L–1 endosulfan in the prawn Macrobrachium malcolmsonii. Scott et al. (1999) reported an LC50 value of 1.01 lg L–1
endosulfan in the adult grass prawn P. pugio. Moreover, adults of this decapod was more sensitive to endosulfan than were larvae and embryos to both biocids (Key et al. 2003), and differences have also been reported between male and female animals (Wirth et al. 2002). Despite the great variability in values reported for crustaceans, all of them indicated high toxic levels, e.g., the LC50 for the freshwater amphipod Gammarus fasciatus was 6 lg L–1 and for the saltwater Korean shrimp Palaemon macrodactylus was between 3.4 and 17.2 lg L–1 in flow-through or static assays (USEPA 1980). Once a toxic chemical enters an organism, several biochemical and physiologic mechanisms attempt to challenge the toxic stress caused by the pollutant. The mode of action of these insecticide compounds is the inhibition of acetylcholinesterase (AchE) activity, which causes death by hindering nerve function and, ultimately, muscle response. This enzymatic system is common to all organisms and is the reason early biocide compounds were nonspecific in their toxicity. Regarding sublethal effects, some important physiologic processes often associated with individual fitness have been recognized as being affected, e.g., reproduction, development, behaviour, and growth, (Newman & Unger 2003). Chorpyrifos inhibited AchE in stage-5 grass shrimp eggs (Lund et al. 2000). Moreover, AchE inhibition
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M. C. Montagna and P. A. Collins 13.5
Cont 0. 00 0. 01 0. 02
ro l 5 µg L-1 1 µg L-1 2 µg L-1
A
Intermol period (days)
12.5
11.5
10.5
9.5 1
2
3
4
Molt cycles 13.5
B
Cont r o l 0. 1 22 µg L-1 0. 2 44 µg L-1 0. 4 88 µg L-1
Intermolt period (days)
12.5
11.5
10.5
9.5
1
2
3
4
Molt cycles
Fig. 3 Mean intermolt period of P. argentinus plotted against molt cycles for control and each concentration of chlorpyrifos (A) and endosulfan (B) during the experiment
occurred in natural-environment prawns inhabiting environments in which chlorpyrifos and endosulfan, among mother biocids, are found (Key et al. 2003). Previous works have reported abnormal behaviours—such as fast jerking, frequent jumping, erratic swimming, spiralling, convulsions, tendency to escape from aquaria, secretion of mucus over the gill chamber (Bhavan et al. 1997), and even severely impaired growth potential (Bhavan & Geraldine 2000)—produced by exposure to endosulfan in test prawns and in the freshwater prawn Macrobrachium malcolmsonii. Similar neurotoxic effects were observed in P. argentinus in endosulfan and chlorpyrifos solutions, and these alterations permitted assessment of the impact and lethal effects of contaminants. Furthermore, the NOEC and LOEC values were used to determine sensitivity to the toxic action of these
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insecticides. In contrast, control prawns spent much of their time in an inactive state interrupted by short periods of walking and swimming. In streams, the highest concentrations of both biocids (Jergentz et al. 2005), as well as the NOEC and LOEC values obtained in the current study (Table 1), indicated that decapod populations in these aquatic environments could be affected. This effect could also be increased after rainfall events. This risk has been indicated in P. pugio populations inhabiting natural environments (Wirth et al. 2003; 2004; Arnold et al. 2004). In the sublethal tests, the same growth increment of P. argentinus was observed among experimental and control prawns, in which CL increased linearly during the experimental period. This growth was not different from that reported for the other crustacean species under normal growth conditions (Hartnoll 1982; Collins & Petriella 1999; Renzulli & Collins 2000) or from that indicated for this prawn when exposed to glifosate herbicide (Montagna & Collins 2005). However, the intermolt period was severely affected by both insecticides during the exposure time, and this alteration differed from what was reported for prawns exposed to cypermethrin (Collins & Cappello 2006). Perturbations in the Y-organ and the seno gland may serve as indicators of the toxicity of these pesticides, which affect the production and storage of the inhibitory molt hormone or, more integrally, the neurohormonal system located in the eyestalks. This indicates that despite the fact that concentrations were lower than lethal doses, chlorpyrifos and endosulfan affect the ecdysis cycle, increasing mortality and possibly affecting reproductive events as well. The presence of endosulfan in aquatic environments could affect the reproductive season mainly because of decreased gravity of female prawns. This could affect prawn reproducibility by producing low numbers of individuals and thus higher predation stress in the population during winter (Wirth et al. 2004). Moreover, this risk could become worse after rainfall during periods when biocids are used extensively (Arnold et al. 2004). Data in this study indicate that the freshwater prawn P. argentinus is sensitive to applications of these organochlorine and organophosphorus insecticides and that the species may be used as a bioindicator crustacean to provide information on environmental quality. This evaluation should be validated with macroscale assays to reach true data conclusions (Pennington et al. 2004). Acknowledgment These studies were supported by Grant PICTO UNL N° 01-13232.
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