Ecotoxicology (2010) 19:196–206 DOI 10.1007/s10646-009-0405-3
The mysid Siriella armata as a model organism in marine ecotoxicology: comparative acute toxicity sensitivity with Daphnia magna Sara Pe´rez Æ Ricardo Beiras
Accepted: 18 August 2009 / Published online: 16 September 2009 Ó Springer Science+Business Media, LLC 2009
Abstract Siriella armata (Crustacea, Mysidacea) is a component of the coastal zooplankton that lives in swarms in the shallow waters of the European neritic zone, from the North Sea to the Mediterranean. Juveniles of this species were examined as standard test organisms for use in marine acute toxicity tests. The effects of reference toxicants, three trace metals (Copper, Cadmium and Zinc), and one surfactant, sodium dodecyl sulfate (SDS) were studied on S. armata neonates (\24 h) reared in the laboratory. Acute toxicity tests were carried out with filtered sea water on individual chambers (microplate wells for metals or glass vials for SDS) incubated in an isothermal room at 20°C, with 16 h light: 8 h dark photoperiod for 96 h. Each neonate was fed daily with 10–15 nauplii of Artemia salina. Acute (96 h) LC50 values, in increasing order, were 46.9 lg/L for Cu, 99.3 lg/L for Cd, 466.7 lg/L for Zn and 8.5 mg/L for SDS. The LC10, NOEC and LOEC values were also calculated. Results were compared with Daphnia magna, a freshwater cladoceran widely used as a standard ecotoxicological test organism. Acute (48 h) LC50 values were 56.2 lg/L for Cu, 571.5 lg/L for Cd, 1.3 mg/L for Zn and 27.3 mg/L for SDS. For all the reference toxicants studied, the marine mysid Siriella armata showed higher sensitivity than the freshwater model organism Daphnia magna, validating the use of Siriella mysids as model organisms in marine acute toxicity tests. Keywords Mysidacea Siriella armata Daphnia magna Ecotoxicology Metals SDS
S. Pe´rez (&) R. Beiras Laboratorio de Ecoloxı´a Marin˜a (LEM), Facultade de Ciencias do Mar, Universidade de Vigo, As Lagoas Marcosende s/n, 36310 Vigo, Galicia, Spain e-mail:
[email protected]
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Introduction In marine ecotoxicology, early life stages of sea-urchins and bivalves are frequent biological models, and their high sensitivity to trace metals and other pollutants is well documented. (e.g. Beiras and His 1995; Bellas et al. 2005). However, those authors have pointed the necessity of increasing the number of taxonomic groups used in ecotoxicology, and analyze cases of selective toxicity. Crustaceans, with a more cephalic nervous system, are in fact more sensitive than echinoderms or bivalves to insecticides (His et al. 2000; Bellas et al. 2005), PAHs (Bellas and Thor 2007) and Cadmium (Marin˜o-Balsa et al. 2000). The cladoceran Daphnia magna is a well known standard test species in freshwater ecotoxicological studies, and detailed protocols for their use in both ecological risk assessment and prenormative tests with chemicals are available (UNE-EN ISO 6341: 1996). This is due to their small size, easy handling and laboratory culture, wide distribution, availability throughout the year, predominantly parthenogenetic reproduction, ecological relevance in food chains and high sensitivity (Adema 1978; Sarma and Nandini 2006). Mysids are crustaceans with a wide distribution in aquatic environments. Their short life cycle, easy maintenance in aquaria, and ecological relevance as a food source for bottom-feeding fish (Lussier et al. 1985; Sardo et al. 2005), support their use in marine ecotoxicological studies. Standard procedures are available for toxicity tests with the North American species Americamysis (formerly Mysidopsis) bahia (USEPA 2002a, b; Widdows 1993). In Europe some work has been done with the brackish water species Neomysis integer and the salt water species Praunus flexuosus (McLusky and Hagerman 1987; Emson and
The mysid Siriella armata as a model organism in marine ecotoxicology
Crane 1994; Garnacho et al. 2000; Verslycke et al. 2003), but their restricted geographical distribution prompts the use of local species, which allow also a more realistic assessment in estuarine environments (Emson and Crane 1994; Verslycke et al. 2003). The saltwater species Siriella armata is a component of the coastal zooplankton that lives in shoals or swarms in the shallow waters of the neritic zone. The broad distribution of this species along the European coast, expanding from the North Sea to the Mediterranean (Cuzin-Roudy et al. 1981), makes it available as a testing model in all Europe. S. armata is characterized by its particularly slender form and by the length of its rostrum (Tattersall and Tattersall 1951), the maximum size of adults is 24 mm. Females bear a marsupium, or brood pouch (hence the common name of opossum shrimps), where embryonic and post-embryonic development of the juveniles occur, until they are released, before the ecdysis of the female. Different stages of embryonic development inside the marsupium are shown in Fig. 1. The aim of the present study was to develop a standard marine acute toxicity test using neonates of the European mysid Siriella armata as a model organism by means of standardising the exposure conditions and measuring the sensitivity of this organism to reference toxicants, in particular Copper (Cu), Cadmium (Cd), Zinc (Zn) and SDS. We have also carried out a comparative toxicology study between S. armata and the standard freshwater model Daphnia magna in order to validate the novel marine mysid test in terms of sensitivity. Ecologically, the estimation of the toxicity threshold for an environmental pollutant is more informative than a parameter predicting a level of effect as high as 50% (Beiras and Bellas 2008). Therefore, LC10, NOEC (no observed effect concentration) and LOEC (lowest observed effect concentration) were also calculated.
197
Materials and methods Experimental solutions The reference toxicants used in this study were three trace metals (Copper, Cadmium and Zinc) and one surfactant, SDS. For each metal, stock solutions were prepared from a 1 g/L stock solution for spectrophotometry (Panreac quı´mica SA Barcelona, Spain) in deionized water. Then selected experimental concentrations were prepared by addition of adequate volumes of the stock solution to 0.22 lm filtered seawater (FSW) in case of mysids, and to reconstituted hard water (RHW) prepared with Milli-Q water in case of daphnids. Metal dilutions in the tests with mysids were calculated to avoid a salinity decrease higher than 10%, and their control concentration was prepared with FSW and deionised water in the same proportion as the highest metal concentration. SDS stock solution was prepared from analytical grade SDS (Merck, Darmstadt) in FSW or in RHW for mysids and daphnids respectively. Experimental concentrations prepared in x2 geometric scale ranged from 10 to 2,400 lg/L for Cu, from 20 to 1,400 lg/L for Cd, from 0.125 to 8 mg/L for Zn, and from 0.5 to 65 mg/L for SDS. The number of concentrations per test were variable because of the availability of neonates, but always higher than six plus control. Siriella armata acute test Swarms of Siriella armata were captured in Rı´a de Vigo (Galicia, NW Iberian Peninsula) by divers, with a hand net, and immediately placed in quarantine facilities at Estacio´n de Ciencias Marin˜as de Toralla (ECIMAT). In the laboratory, mysids were maintained in 100 L plastic tanks with circulating sand-filtered seawater at a rate of 2 L/min, giving a 100% volume exchange every 50 min. The
Fig. 1 Different stages of Siriella armata embryonic development inside the marsupium of the mature females (f.1a–f)
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198
temperature in the tanks ranged between 17 and 18°C, salinity from 34.4 to 35.9%, and oxygen was always higher than 6 mg/L. These parameters were checked daily. The organisms were fed daily with nauplii or metanauplii of Artemia salina, ad libitum. Preliminary tests were made to standardize the bioassay in order to obtain maximum survival rates of the neonates in the controls (data not shown). Those tests showed control 96 h survival [90% with no need of water renewal nor aeration. In contrast daily feeding was essential to prevent neonate mortality. Preliminary tests demonstrated that less than 10 nauplii of Artemia was insufficient and mortality in controls increases, but more than 15 nauplii was excessive because degradation of surplus food impaired water quality. One day before the start of the test, mature females bearing embryos in the last stage of development, i.e. in the late post-nauplioid phase (Cuzin-Roudy and Tchernigovtzeff 1985) (Fig. 1e, f) were separated into 0.45 dm3 individual tanks half submerged in the main tank with a 150 lm mesh on the bottom and well aerated. The neonates released within \24 h were used in the tests. The use of new-born individuals not only increases sensitivity, but also allows standardization (Cripe 1994; Whiting et al. 1996; Verslycke et al. 2003). Incubations were conducted in plastic microplate wells in case of metals and in 20 mL glass vials for SDS. To prevent cannibalism among neonates, a single individual per well was used. A total of twenty individuals were used for each concentration. Neonates were delivered by plastic pipette in each compartment of 2 mL. Microplates or glass vials were incubated in an isothermal room at 20°C and 16 h light: 8 h dark photoperiod for 96 h. Neonates were fed daily between 10–15 nauplii of 24–48 h. posthatch Artemia salina. Oxygen concentration, pH and salinity were determined at the beginning and the end of each test. Dead mysids were counted after 24, 48, 72 and 96 h. Figure 2 shows the difference between an alive and a dead mysid inside a microplate well. Exposure time was set to
Fig. 2 Juveniles of Siriella armata inside a microplate well. Figure 2a shows a living mysid, and Fig. 2b shows a dead mysid
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96 h on the basis of preliminary results on background mortality under the same exposure conditions. Daphnia magna acute test Daphnia magna were obtained from the University of Antwerp (Belgium), and cultured in a 20°C isothermal room in aerated 4 L plastic jars of RHW with 50 daphnids per jar. The photoperiod was 16 h light: 8 h dark, and they were fed 3 9 106 cells of Selenastrum capricornutum every second day, after water change. One day before the start of the test mature females were separated in 4 L plastic jars, where new neonates were keeping until the following day. Tests were carried out with \24 h neonates, in 25 mL plastic vials in case of metals, and 25 mL glass vials in case of SDS. Ten daphnids per replicate and four replicates per treatment were used. Neonates were delivered by plastic pipette in each vial. Oxygen concentration, pH and water hardness were determined at the beginning and the end of each test. Vials were incubated in a 20°C isothermal room for 48 h. with a 16 h light: 8 h dark photoperiod, and animals were no fed during the test. Mortality was recorded after 48 h (UNE-EN ISO 6341:1996; USEPA 2002a). Statistical analyses The LC50 and LC10 values (the estimated concentrations causing 50 and 10% mortality), and their 95% confidence intervals were calculated by fitting the survival data to a Weibull dose-response model using Statistica version 6.0 (StatSoft, Inc. 1984–2008, http://www.statsoft.com/). The NOEC and LOEC values were calculated with the Kruskall-Wallis and the Mann-Whitney U-non-parametric test, because data did not meet the requirements for parametric tests, using SPSS version 14.0 for Windows software (SPSS, Inc., Chicago, Illinois, www.spss.com). Differences were considered as significant when P \ 0.05.
The mysid Siriella armata as a model organism in marine ecotoxicology
199
Results
Discussion
LC50 values
Mysids, and particulary Americamysis bahia are recommended test organisms by the USEPA for estuarine and marine water toxicity tests (USEPA 2002a, b). Some European mysids such as Neomysis, Praunus and Siriella have also been proposed, although sensitivity intercomparisons are lacking (OSPAR Commission 2006). In this paper, we tried to validate a standard marine acute toxicity test with Siriella armata by comparing the sensitivity of this organism to the standard model in freshwater ecotoxicology Daphnia magna. According to the 96-h LC50 values, the ranking of toxicity of the reference compounds was the same for both test species. Correlation analysis showed a positive Pearson correlation (rp = 0.97; P \ 0.05) between LC50 values for S. armata and D. magna, but for all the reference toxicants studied, the marine mysid S. armata showed more sensitivity than D. magna; therefore, we suggest the use of that mysid as a model organism in marine ecotoxicology in terms of sensitivity. Nevertheless it is important to bear in mind that the period of exposure for D. magna (48 h) is shorter than for S. armata (96 h), and this partly explains the lower LC50 values of the mysids. If necessary for practical reasons, the exposure time of the mysid test could be reduced to 48 h, and its sensitivity still would be similar to that of D. magna; when we compare values of 48 h-LC50 and 48 h-LC10 between both mysids and daphnids (Table 1 and Table 2) S. armata shows more sensitivity for SDS and Cd, and similar toxicity for Cu and Zn. In case of metals the kinetics of toxicity on S. armata showed different patterns. Cu and Zn exerted significant effects from the first day of exposure, whereas for Cd mortality did not exceed 50% until 48 h exposure. This suggests that the mechanisms involved in the uptake, accumulation and excretion for Cd (non-essential metal) are different to those for the essential metals Cu and Zn (Amiard et al. 1987; Smokorowski et al. 1998) and
The LC50 values and their 95% confidence intervals (CI) are summarize in Table 1. The mortality of the mysidacea was recorded every 24 h, but 96 h was selected as standard exposure period. Whereas Cu, Zn and SDS showed mortality at high concentrations since the first 24 h, the effect of Cd was delayed until 48 h exposure, and later on mortality rapidly increased. Control survival was always C90%. Among the metals tested, Cu was the most toxic to S. armata neonates, with a 96 h-LC50 of 46.9 lg/L. Zn LC50 was 466.7 lg/L, the least toxic metal, while the LC50 of Cd was 99.3 lg/L. The SDS, with a LC50 of 8.5 mg/L, was the least toxic compound tested. For S. armata, curves fitted to the toxicity data are shown in Fig. 3(a–d); in each figure, four curves are represented, one each 24 h exposed. Figure 4(a–d) represent curves for D. magna in comparison with curves for S. armata at 96 h. The 48 h-LC50 for daphnids (Table 1) followed the same ranking that mysids; LC50 value of Cu was 56.2 lg/L, 571.5 lg/L for Cd, 1343.9 lg/L for Zn and 27.3 mg/L for SDS. LC10, NOEC and LOEC values The LC10 values and their 95% confidence intervals (CI) are shown in Table 2. As expected, toxicity increased with exposure time, but the pattern was not the same for all toxicants. In case of Cd, before 48 h effects were minimal. Both S. armata and D. magna showed the lowest LC10 value in case of Cu (9.6 lg/L and 31.1 lg/L respectively), and then Cd (62.8 lg/L and 269.6 lg/L), Zn (301.1 lg/L and 1.1 mg/L) and finally SDS with 4.3 mg/L for S. armata and 13.9 mg/L in case of D. magna. NOEC and LOEC values for D. magna (at 48 h) and for S. armata (at 48 and 96 h) are shown in Table 3. The ranking of toxicity, therefore, is independent of the toxicity parameter chosen.
Table 1 LC50 values of Cu, Cd, Zn and SDS for Siriella armata and Daphnia magna Toxic
Values (lg/L)
Siriella armata ( h)
Daphnia magna ( h)
24
48
72
96
48
LC50
315.0
152.0
100.1
46.9
56.2
(CI 95%)
(223.0–444.8)
(111.6–206.9)
(86.8–115.5)
(32.2–68.2)
(53.0-59.3)
Cd
LC50
[1400
344.34
140.4
99.3
571.5
Zn
(CI 95%) LC50
(n.c.) 1776.6
(341.7–347.0) 1341.5
(127.8–154.2) 1260.1
(86.2–114.4) 466.7
(491.7–664.1) 1343.9
(CI 95%)
(1707.1–1849.3)
(1240.1–1451.2)
(1177.9–1348.0)
(462.1–471.4)
(1314.9–1373.4)
LC50
22999.6
11612.1
9445.6
8478.6
27342.6
(CI 95%)
(n.c.)
(10810.8–12467.7)
(9076.0–9828.8)
(7220.5–9929.4)
(22487.7–33201.0)
Cu
SDS
Values are in lg/L, with 95% confidence intervals in parentheses
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200
S. Pe´rez, R. Beiras
Fig. 3 Percentage of dead neonates of Siriella armata at 24 (closed triangle), 48 (open circle), 72 (cross) and 96 h (closed circle) in each concentration, represented as log [concentration (lg/L) ? 1] for Cu (f.3a), Cd (f.3b) and Zn (f.3c), and as log [concentration (mg/L) ? 1] for SDS (f.3d)
mechanisms of regulation of the body burden in marine invertebrates have been described (Lorenzo et al. 2003). Alternatively, Cd may target some compartment or metabolic route in the organism not affected by the other two metals, which would explain its delayed response (Ferrer et al. 2006; Gentile et al. 1982; Rainbow 1995). Instances of selective toxicity of Cd to crustaceans, compared to other marine invertebrates such as molluscs and echinoderms have been demonstrated (Nimmo et al. 1978; Martin et al. 1981), and this is probably due to their specific effects on the development of the exoskeleton in arthropods. This should be especially relevant in the case of the fast-growing neonates used in the present study. By comparing crustaceans to non-crustacean marine organisms (Table 4) we find that, while sensitivity to Cu and Zn is similar in both groups, average Cd LC50 for crustaceans (geometric mean = 168 lg/L) is one order of magnitude lower than that for non-crustacean marine organisms (g.m. 1692 lg/L). This stresses the need to include a crustacean in the battery of marine bioassays for routine water quality assessment. While the rank of acute toxicity of metals in literature varied among the species tested, SDS was consistently less toxic. Whiting et al. (1996) obtained a 48 h LC50 of 9.8 mg/L for S. sapidus, and 34 mg/L for P. pugio. Mariani
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et al. (2006) also found a 96-h LC50 for T. fluvus of 7.4 mg/L. Bellas et al. (2005) obtained a 20-h LC50 of 5.1 mg/L for C. intestinalis. However the same authors observed a high sensitivity of M. squinado to SDS, with a 96-h LC50 value of 0.68 mg/L. Therefore although in general heavy metals are more toxic than SDS, sensitivity to SDS is highly variable among different taxa. Several studies have quantified the acute toxicity of Cu, Cd, Zn and SDS to mysids (Table 5). As Table 5 shows, and once age differences are taken into account, there is an agreement between the range of values found in the literature (15.5–181 lg/L, 12.0–318 lg/L, 145.4–3,000 lg/L and 4,690–17,000 lg/L for Cu, Cd, Zn and SDS respectively) and those reported in the present study. Nevertheless, there is a significant variation among toxicity values reported by different authors that stresses the need for harmonization of the exposure conditions, age and endpoint recorded in a standard acute toxicity test for mysids. Factors such as temperature or salinity, which affect metal availability and therefore its toxicity (e.g. Blust et al. 1992), also vary between experiments, because both marine and estuarine species of mysids are used in ecotoxicology. The use of natural filtered seawater (FSW) instead of artificial seawater (ASW) can be also a source of
The mysid Siriella armata as a model organism in marine ecotoxicology
201
Fig. 4 Percentage of dead neonates of Daphnia magna at 48 h (closed circle) and percentage of dead neonates of Siriella armata at 96 h (open circle) in each concentration, represented as log [concentration(lg/L) ? 1]) for Cu (f.4a), Cd (f.4b) and Zn (f.4c) and as log [concentration (mg/L) ? 1] for SDS (f.4d)
Table 2 LC10 values of Cu, Cd, Zn and SDS for Siriella armata (at 96 h) and Daphnia magna (48 h) Toxic
Values (lg/L)
Siriella armata ( h)
Daphnia magna ( h)
24
48
72
96
48
LC10
84.5
39.0
38.8
9.6
31.1
(CI 95%)
(48.2–147.4)
(22.4–62.9)
(28.8–52.3)
(5.0–18,9)
(27.8–34.9)
LC10
[1400
320.0
92.0
62.8
269.6
(CI 95%)
(n.c.)
(311.8–328.4)
(68.6–123.3)
(54.2–72.8)
(215.3–337.5)
Zn
LC10
1467.6
1047.6
998.1
301.1
1133.1
(CI 95%)
(1345.8–1600.2)
(829.9–1322.5)
(867.3–1148.5)
(294.3–308,0)
(1026.8–1250-3)
SDS
LC10 (CI 95%)
20771.5 (n.c.)
6763.5 (6042.1–7558.7)
4814.1 (4373.6–5290.6)
4339.7 (2894.6–6320.9)
13934.2 (10358.3–18635.8)
Cu Cd
Values are in lg/L with 95% confidence intervals in parentheses n.c. no calculated
variability, because in FSW dissolved organic matter is available to bind metal ions, thus reducing its toxicity to test organisms (Lorenzo et al. 2002). A review of the available literature on marine invertebrates (Tables 4, 5) places S. armata among the most sensitive species suitable for standard toxicity testing.
Daphnia magna is the most frequent model organism in freshwater ecotoxicology world wide. Toxicity values for this species are also summarized in Table 5. In all cases our data are within the values previously found in literature, supporting an adequate reproducibility of the method. In general, interlaboratory variability in short-term toxicity
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S. Pe´rez, R. Beiras
202
Table 3 NOEC and LOEC values of Cu, Cd, Zn and SDS for Siriella armata (at 48 h and 96 h) and Daphnia magna (48 h) Time (h)
Siriella armata Daphnia magna
Cu
Cd
Zn
NOEC
LOEC
NOEC
LOEC
48
20
40
80
160
96
10
20
20
40
48
20
40
162
322
1000
SDS
NOEC
LOEC
NOEC
LOEC
675
1000
5000
10000
200
300
500
1000
1400
9000
15000
Values are in lg/L
Table 4 LC50 values (lg/L) of Cu, Cd, Zn and SDS to other marine and estuarine invertebrates Species
Toxicant Zn
Life stage
Endpointa
Time
References
Fertilized eggs
NL
48
Ferna´ndez and Beiras (2001), Mariani et al. (2006), Bellas et al. (2005)
Cu
Cd
SDS
66.76
9240
A. granosa
230
940
7760
Adults
M
96
Ong & Din (2001)
D. faba
200
990
3610
Adults
M
96
Ong & Din (2001)
M. galloprovincialis
10
1925
160–320
2353
Fertilized eggs
Emb
48
Beiras and Albentosa (2004), Beiras and Bellas (2008)
45.7
838.5
5145
Fertilized eggs
Emb
20
Bellas et al. (2001), Bellas et al. (2005)
Fertilized eggs
NL
24
Gopalakrishnan et al. (2007)
Echinoids P. lividus
3200–4100
Molluscs
Ascidians C. intestinalis Polychaetes H. elegans
122
391
Crustaceans C. granulata
219.2
47.8
172.1
C. sapidus H. gammarus
46
34
M. squinado
50
158
P. duodarum
393.2b
312.1b
P. pugio P. serratus
3304
M
96
Ferrer et al. (2006)
Larvae
M
48
Larvae
M
48
Whiting et al. (1996) Marin˜o-Balsa (2002)
687
Larvae
M
48a /72
Post larvae
M
96
Cripe (1994)
34000
Larvae Larvae
M M
48 72
Whiting et al. (1996) Marin˜o-Balsa (2002)
7420
Larvae
M
96
Mariani et al. (2006)
503.8b
1686
T. fulvus a
Larvae 9800
Marin˜o-Balsa (2002), Bellas et al. (2005)
NL normal larva, Emb embryogenesis, M mortality
b
Metal-only concentrations recalculated from metal chloride values given by Cripe (1994)
c
48 h for SDS
test results of one or even two orders of magnitude is quite common, especially in bioassays with heavy metals. Some of these differences can be explained by environmental variability (differences in exposure conditions among tests) or by biological variability among populations; differences in genotypes can reflect significant differences in response (Baird et al. 1989, 1991). The interference of dissolved organic mater and other factors affecting metal speciation has already been discussed.
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In some cases an overestimation of sensitivity due to poor handling conditions of the test organisms can also interfere with the test results. Among the factors contributing to this overstimation, poor biological condition of the adult brood stock, thermal stress and starvation are remarkable. His et al. (2000) stressed the need for understanding the normal development of a species and master the techniques for optimal laboratory rearing as a previous requirement for valid ecotoxicological studies and
The mysid Siriella armata as a model organism in marine ecotoxicology
203
Table 5 Literature acute toxicity values of several mysidacea and Daphnia magna to Cu, Cd, Zn and SDS. Values are in lg/L, with 95% confidence intervals in parentheses Toxic
Organism
Species
Agea
Time (h)
LC50 (lg/L)
Ta (8C)
S (%)
References
Cu
Mysidacea
M. bahia
J
96
15.5 (12.6–19.6)
20–28
oct-17
Nimmo et al. (1978)
P. flexuosus
J
96
21 (n.d.)
20
33
Garnacho et al. (2000)
S. armata
J
96
46.9 (32.2–68.2)
20
35
Present study
N. integer
J
96
68 (57–83)
20
25
Verslycke et al. (2003)
M. bahia
J
96
72.31b (63.3–82.7)
25
25
Cripe (1994)
M. bahia
A
96
181 (146–250)
21
30 ± 2
Lussier et al. (1985)
D. magna
n.d.
n.d.
9.8
n.d.
n.d.
Biesinger and Christiansen (1972) (cited by Baird et al. 1991)
D. magna
N
48
56,2 (53.0–59.3)
20
0
Present study
D. magna
N
48
10.5–70.7c
20
0
Baird et al (1991)
D. magna
N
820
20
0
Meng et al (2008)
M. bahia
J
12.0b (10.6–13.6)
25
25
Cripe (1994)
Daphnia
Cd
Mysidacea
Daphnia
Zn
Mysidacea
Daphnia
SDS
Mysidacea
96
S. armata
J
96
39.5 (21.5–72)
18
38
Birmelin et al. (1995)
S. armata
J
96
99.3 (86.2–114.4)
20
35
Present study
M. bahia S. armata
A A
96 96
110 (102–118) 112 (86–144)
21 18
30 38
Gentile et al. (1982) Birmelin et al. (1995)
N. integer
J
96
318 (262–416)
20
25
Verslycke et al. (2003)
D. magna
N
48
58.16
20
0
Attar and Maly (1982)
D. magna
n.d.
n.d.
65
n.d.
n.d.
Biesinger and Christiansen (1972) (cited by Baird et al. 1991)
D. magna
N
48
3.6–115.9c
20
0
Baird et al. (1991)
D. magna
n.d.
n.d.
188
n.d.
n.d.
Khangarot and Ray (1958) (cited by Baird et al. 1991)
D. magna
N
48
310
20
0
Meng et al (2008)
D. magna
N
48
320 (262–392)
20 ± 1
0
Bodar et al. (1990)
D. magna
N
48
571.5 (491.7–664.1)
20
0
Present study
D. magna
N
48
615
20 ± 1
0
Muyssen and Janssen (2004)
M. bahia
J
96
145.4b (121.4–173.7)
25
25
Cripe (1994)
S. armata
J
96
466.7 (462.1–471.4)
20
35
Present study
M. bahia
A
96
499 (350–600)
21
30 ± 2
Lussier et al. (1985)
N. integer
J
96
1037 (841–1291)
20
25
Verslycke et al. (2003)
P. flexuosus
A
96
3000 (n.d.)
15
27
McLusky and Hagerman (1987)
D. magna
n.d.
48
100
n.d.
n.d.
Biesinger and Christiansen (1972) (cited by Baird et al. 1991)
D. magna
n.d.
n.d.
560
n.d.
n.d.
D. magna
N
48
798.94
20
0
Khangarot and Ray (1958) (cited by Baird et al. 1991) Attar and Maly (1982)
D. magna
N
48
1343.9 (1314.9–1373.4)
20
0
Present study
D. magna
N
48
755.5–1831c
20
0
Baird et al. (1991)
M. intii
J
168
4690 (4270–5140)
20
34
Langdon et al. (1996)
M. bahia
n.d.
n.d.
6600
n.d.
n.d.
Roberts et al. (cited by ECOTOX database)
S. armata
J
96
8478.6 (7220.5–9929.4)
20
35
Present study
M. bahı´a
J
48
17000 (12000–25000)
25
20
Whiting et al. (1996)
123
S. Pe´rez, R. Beiras
204 Table 5 continued Toxic
a
Organism
Species
Agea
Time (h)
LC50 (lg/L)
Ta (8C)
S (%)
References
Daphnia
D. magna
N
48
13500
20
0
Lewis and Horning (Lewis and Horning 1991)
D. magna
N
48
14500–16200
20
0
Villegas-Navarro et al. (1999)
D. magna
N
48
19129 (19023–19235)
20 ± 1
0
Guilhermino et al. (2000)
D. magna
N
48
27342.6 (22487.7– 33201.0)
20
0
Present study
D. magna
N
48
31000
20
0
Janssen and Persoone (1993)
A adults, J juveniles, N neonates
b
Metal-only concentrations recalculated from metal chloride values given by Cripe (1994)
c
Range of values between different genotypes
n.d. No data
interpretation of their results. We have conducted a series of preliminary experiments in order to make sure that feeding rate and other incubation parameters maximized control survival (data not shown). With the test conditions proposed in this study we frequently found a 100% control survival, and could set an acceptability criterion of C90% to ensure reliable results. The adoption of control acceptability criteria have been repeatedly advocated as a need in toxicity testing in order to guarantee optimum quality of the biological material and therefore robust and reliable results, particulary when test organisms come from wild populations and experience a sharp change in environmental conditions when transferred into the laboratory (OSPAR Commission 2006). In conclusion, Siriella armata is a good species to be used in acute bioassays, because of its wide distribution, abundance and ease of handling, short life cycle, and in addition because of its sensitivity, enhanced by using neonates. The use of neonates in a static, non-renewal system allowed us to reduce the dimension of the incubation chambers down to microplates, enabling micro-scale toxicity testing. In addition, the easy maintenance of S. armata in laboratory and the rapid life cycle of this species provide promising grounds for their use also in chronic toxicity tests. Acknowledgments We wish to thank Dr. J. Bellas, I. Dura´n, D. Rial and the staff of Department of Ecology and Animal Biology (University of Vigo, Galicia, Spain). We are also grateful to E. Poza, R. Go´mez, D. Costas and M.J. Valcarce for the capture and maintenance of mysids in the laboratory, and all the staff of Estacio´n de Ciencias Marin˜as de Toralla (ECIMAT, Vigo, Galicia) for their support during the course of this work. S. Pe´rez was granted with a fellowship from the University of Vigo. This study was also partially funded by the research proyect PGIDIT05RMA31201PR from Xunta de Galicia.
123
References Adema DDD (1978) Daphnia magna as a test animal in acute and chronic toxicity test. Hydrobiologia 59(2):125–134 Amiard JC, Amiard-Triquet C, Berthet B, Metayer C (1987) Comparative study of the patterns of bioaccumulation of essential (Cu, Zn) and non-essential (Cd, Pb) trace metals in various estuarine and coastal organisms. J Exp Mar Biol Ecol 106:73–89 Attar NJ, Maly EJ (1982) Acute toxicity of cadmium, zinc and cadmium-zinc mixtures to Daphnia magna. Arch Environ Contam Toxicol 1:291–296 Baird DJ, Barber I, Bradley M, Calow P, Soares AMVM (1989) The Daphnia bioassay: a critique. Hydrobiologia 188(189):403–406 Baird DJ, Barber I, Bradley M, Soares AMVM, Calow P (1991) A comparative study of genotype sensitivity to acute toxic stress using clones of Daphnia magna. Ecotoxicol Environ Saf 2:257–265 Beiras R, Albentosa M (2004) Inhibition of embryo development of the commercial bivalves Ruditapes decussatus and Mytilus galloprovincialis by trace metals; implications for the implementation of seawater quality criteria. Aquaculture 230:205–213 Beiras R, Bellas J (2008) Inhibition of embryo development of the Mytilus galloprovincialis marine mussel by organic pollutants; assessment of risk for its extensive culture in the Galician Rias. Aquaculture 227:208–212 Beiras R, His E (1995) Effects of dissolved mercury on embryogenesis, survival and growth of Mytilus galloprovincialis mussel larvae. Mar Ecol Prog Ser 126:185–189 Bellas J, Beiras R, Marin˜o-Balsa JC, Ferna´ndez N (2005) Toxicity of organic compounds to marine invertebrate embryos and larvae: a comparison between the sea-urchin embryogenesis bioassay and alternative test species. Ecotoxicology 14:335–351 Bellas J, Thor P (2007) Effects of selected PAHs on the survival and reproduction of the calanoid copepod Acartia tonsa. Ecotoxicology 16:465–474 Bellas J, Va´zquez E, Beiras R (2001) Toxicity of Hg, Cu, Cd, and Cr on early developmental stages of Ciona intestinalis (Chordata, Ascidiacea) with potential application in marine water quality assessment. Water Res 35(12):2905–2912 Birmelin J, Cuzin-Roudy MR, Gnassia-Barelli M, Puiseux-Dao S (1995) The Mysid Siriella armata as a test organism in toxicology: effects of cadmium. Mar Environ Res 39:317–320
The mysid Siriella armata as a model organism in marine ecotoxicology Blust R, Kockelbergh E, Baillieul M (1992) Effect of salinity on the uptake of cadmium by the brine shrimp Artemia franciscana. Mar Ecol Prog Ser 84:245–254 Bodar CWM, van der Sluis I, van Montfort JCP, Voogt PA, Zandee DI (1990) Cadmium resistance in Daphnia magna. Aquat Toxicol 16:33–40 Cripe GM (1994) Comparative acute toxicities of several pesticides and metals to Mysidopsis bahia and postlarval Penaeus duorarum. Environ Toxicol Chem 13(11):1867–1872 Cuzin-Roudy J, Tchernigovtzeff C (1985) Chronology of the female molt cycle in Siriella armata M.Edw. (Crustacea: Mysidacea) based on marsupial development. J Crust Biol 5(1):1–14 Cuzin-Roudy J, Berreur-Bonnenfant J, Fried Montaufier MC (1981) Chronology of post-embryonic development in Siriella armata (M.Edw.) (Crustacea: Mysidacea) reared in the laboratory: growth and sexual differentiation. J Crust Biol 5(1):1–14 Emson S, Crane M (1994) A comparison of the toxicity of Cadmium to the Mysid shrimps Neomysis Integer (Leach) and Mysidopsis bahia (Molenock). Water Res 28(8):1711–1713 Ferna´ndez N, Beiras R (2001) Combined toxicity of dissolved mercury with Copper, Lead and Cadmium on embryogenesis and early larval growth of the Paracentrotus lividus sea-urchin. Ecotoxicology 10:263–271 Ferrer L, Andrade S, Asteasuain R, Marcovecchio J (2006) Acute toxicities of four metals on the early life stages of the crab Chasmagnathus granulata from Bahı´a Blanca estuary, Argentina. Ecotoxicol Environ Saf 65:209–217 Garnacho E, Peck LS, Tyler PAA (2000) Variations between winter and summer in the toxicity of copper to a population of the mysid Praunus flexuosus. Mar Biol 137:631–636 Gentile SM, Gentile JH, Walker J, Heltshe JF (1982) Chronic effects of cadmium on two species of mysid shrimp: Mysidopsis bahia and Mysidopsis bigelowi. Hydrobiologia 93:195–204 Gopalakrishnan S, Thilagam H, Raja PV (2007) Toxicity of heavy metals on Embryogenesis and larvae of the marine sedentary polychaete Hydroides elegans. Arch Environ Contam Toxicol 52:171–178 Guilhermino L, Diamantino T, Silva MC, Soares AMVM (2000) Acute toxicity test with Daphnia magna: an alternative to mammals in the prescreening of chemical toxicity? Ecotoxicol Environ Saf 46:357–362 His E, Beiras R, Seaman MNL (2000) The assessment of marine pollution–bioassays with bivalve embryos and larvae. In: Southward AJ, Tyler PA, Young CM (eds) Adv Mar Biol 37. Academic Press, San Diego, pp 1–178 Janssen CR, Persoone G (1993) Rapid toxicity screening-tests for aquatic biota. 1. Methodology and experiments with Daphnia magna. Environ Toxicol Chem 12(4):711–717 Langdon CJ, Harmon VL, Vance MM, Kreeger KE, Kreeger DA, Champan GA (1996) A 7-d toxicity test for marine pollutants using the Pacific mysid Mysidopsis intii. 1. Culture and protocol development. Environ Toxicol Chem 15(10):1815–1823 Lewis PA, Horning WB II (1991) Differences in acute toxicity test results of three reference toxicants on Daphnia at two temperatures. Environ Toxicol Chem 10:1351–1357 Lorenzo JI, Nieto O, Beiras R (2002) Effect of humic acids on speciation and toxicity of copper to Paracentrotus lividus larvae in seawater. Aquat Toxicol 58:27–41 Lorenzo JI, Aierb E, Mubian VK, Blust R, Beiras R (2003) Indications of regulation on copper accumulation in the blue mussel Mytilus edulis. In: Villalba A, Reguera B, Romalde JL, Beiras R (eds) Moluscan shellfish safety, pp 533–544. Xunta de Galicia-UNESCO. ISBN 84-453-3638-X Clave: CL Lussier SM, Gentile JH, Walker J (1985) Acute and chronic effects of heavy metals and cyanide on Mysidopsis Bahı´a (Crustacea: Mysidacea). Aquat Toxicol 7:25–35
205 Mariani L, De Pascale D, Faraponova O, Tornambe` A, Sarni A, Giuliani S, Ruggiero G, Onorati F, Magaetti E (2006) The use of a test battery in marine ecotoxicology: the acute toxicity of sodium dodecyl sulfate. Environ Toxicol 21(4):373–379 Marin˜o-Balsa JC (2002) Uso de las fases larvarias de crusta´ceos deca´podos y misida´ceos en ecotoxicologı´a marina. Tesis Doctoral. Universidad de Vigo. 207 pp Marin˜o-Balsa JC, Poza E, Va´zquez E, Beiras R (2000) Comparative toxicity of dissolved metals to early larval stages of Palaemon serratus, Maja squinado and Homarus gammarus (Crustacea: Decapoda). Arch Environ Contam Toxicol 39(3):345–351 Martin M, Osborn K, Billig P, Glickstein N (1981) Toxicities of ten metals to Crassostrea gigas and Mytilus edulis embryos and Cancer magister larvae. Mar Pollut Bull 12(9):305–308 Mclusky DS, Hagerman L (1987) The toxicity of chromium, nickel and zinc: effects of salinity and temperature, and the osmoregulatory consequences in the mysid Praunus flexuosus. Aquat Toxicol 10:225–238 Meng Q, Li X, Feng Q, Cao Z (2008) The acute and chronic toxicity of five heavy metals on the Daphnia magna. In: Bioinformatics and biomedical engineering, 2008, ICBBE 2008. The 2nd international conference, pp 4555–4558. ISBN:978-1-42441747-6 Muyssen BTA, Janssen CR (2004) Multi-generation cadmium acclimation and tolerance in Daphnia magna Straus. Environ Pollut 130:309–316 Nimmo DR, Rigby RA, Bahner LH, Sheppard JM (1978) The acute and chronic effects of cadmium on the estuarine Mysid, Mysidopsis bahı´a. Bull Environ Contam Toxicol 19(1):80–85 Ong ES, Din ZB (2001) Cadmium, copper, and zinc toxicity to the clam, Donax faba C. and the blood cockle, Andara granosa L. Bull Environ Contam Toxicol 66:86–93 OSPAR Commission (2006) Background document on assessment criteria for the sediment seawater elutriate, pore-water and whole sediment bioassays. SIME 06/4/8-E(L) Rainbow PS (1995) Physiology, physicochemistry and metal uptake—a crustacean perspective. Mar Pollut Bull 31(1–3):55– 59 Sardo AM, Morgado F, Soares AMVM (2005) Mesopodopsis slaberi (Crustacea: Mysidacea): can it be used in toxicity test? Ecotoxicol Environ Saf 60:81–86 Sarma SSS, Nandini S (2006) Review of recent ecotoxicological studies on cladocerans. J Environ Sci Health Part B 41(8):1417– 1430 Smokorowski KE, Lasenby DC, Evans RD (1998) Quantifying the uptake and release of cadmium and copper by the opossum shrimp Mysis relicta preying upon the cladoceran Daphnia magna using stable isotope tracers. Can J Fish Aquat Sci 55:909–916 Tattersall WM, Tattersall OS (1951) The British Mysidacea, vol 136. The Ray Society, Bernard Quaritch Ltd, London UNE-EN ISO 6341:1996 (1996) Calidad del agua. Determinacio´n de la inhibicio´n de la movilidad de Daphnia magna straus. (Cladocera crusta´cea). Ensayo de Toxicidad aguda USEPA (2002a) Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms, 5th edn. EPA 821-R-02-012 USEPA (2002b) Short-term methods for estimating the chronic toxicity of effluents and receiving waters to marine and estuarine organisms, 3rd edn. EPA 821-R0-20-14 Verslycke T, Vangheluwe M, Heijerick D, De Schamphelaere K, van Sprang P, Janssen CR (2003) The toxicity of metal mixtures to the estuarine mysid Neomysis integer (Crustacea: Mysidacea) under changing salinity. Aquat Toxicol 64:307–315 Villegas-Navarro A, Romero Gonza´lez MC, Rosas Lo´pez E (1999) Evaluation of Daphnia magna as an indicator of toxicity and
123
206 treatment efficacy of textile wastewaters. Environ Int 25(5):619– 624 Whiting VK, Cripe GM, Lepo JE (1996) Effects of the anionic surfactant, sodium dodecyl sulfate, on newly-hatched blue crabs, Callinectes sapidus, and other routinely tested estuarine crustaceans. Arch Environ Contam Toxicol 31:293–295
123
S. Pe´rez, R. Beiras Widdows J (1993) Marine and estuarine invertebrate toxicity test. In: Calow P (ed) Handbook of ecotoxicology, vol 1, Chap 9. Blackwell Scientific, Oxford, pp 145–166 ECOTOX database. Available on EPA’s public web page http:// cfpub.epa.gov/ecotox/
