Sensitivity of tropical cladocerans to chlorpyrifos and other insecticides as compared to their temperate counterparts

Chemosphere 220 (2019) 937e942

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Sensitivity of tropical cladocerans to chlorpyrifos and other insecticides as compared to their temperate counterparts Larissa Broggio Raymundo a, Odete Rocha a, Raquel Aparecida Moreira b, *, Mariana Miguel b, Michiel Adriaan Daam c ~o Carlos, Rodovia Washington Luis, km 235, 13565-905, Sa ~o Carlos, SP, Brazil Department of Ecology and Evolutionary Biology, Federal University of Sa ~o Carlos Engineering School, University of Sa ~o Paulo, Av. Trabalhador Sa ~o Carlense, 400, 13.560-970 Sa ~o Carlos, Brazil NEEA/CRHEA/SHS, Sa c CENSE, Department of Environmental Sciences and Engineering, Faculty of Sciences and Technology, New University of Lisbon, Quinta da Torre, 2829-516 Caparica, Portugal a

b

h i g h l i g h t s
Toxicity tests were performed with five tropical freshwater species exposed to chlorpyrifos.
Tropical cladocerans have no greater sensitivity to chlorpyrifos than their temperate counterparts.
Cladoceran toxicity data for chlorpyrifos and other insecticides from temperate regions are also protective for tropical ones.
Ceriodaphnia silvestrii is a good test organism for tropical environments.

a r t i c l e i n f o

a b s t r a c t

Article history: Received 5 November 2018 Received in revised form 31 December 2018 Accepted 2 January 2019 Available online 4 January 2019

The use of temperate toxicity data in tropical risk assessments has often been disputed. Previous sensitivity comparisons between temperate and tropical species, however, have not shown a consistent sensitivity difference between climatically-distinct species. Such comparisons were often limited by a small tropical toxicity dataset. In addition, differences in the taxonomic compositions of the temperate and tropical species assemblages used to construct species sensitivity distributions curves also hampered direct comparisons (e.g. type and ration of crustaceans and insects). The aim of the present study was to compare the sensitivity of temperate and tropical cladocerans to insecticides. Acute laboratory toxicity tests were conducted with five Neotropical cladocerans exposed to a concentration series of the insecticide chlorpyrifos. Subsequently, their EC50 values were compared with those reported in the literature for non-tropical cladocerans. An additional literature toxicity data search for insecticides other than chlorpyrifos was also conducted for both temperate and tropical cladocerans to enable a comparison for a wider range of insecticides and taxa. The order of sensitivity of the native cladocerans to chlorpyrifos was birgei (0.211 mg L1) ¼ Daphnia laevis Ceriodaphnia silvestrii (0.039 mg L1) > Diaphanosoma (0.216 mg L1) > Moina micrura (0.463 mg L1) ¼ Macrothrix flabelligera (0.619 mg L1). A regulatory acceptable concentration based on temperate cladoceran toxicity data of both chlorpyrifos and other insecticides also appeared to be sufficiently protective for tropical cladoceran species. Implications for the use of temperate toxicity data in tropical risk assessments and indications for tropical cladoceran test species selection are discussed. © 2019 Elsevier Ltd. All rights reserved.

Handling Editor: Willie Peijnenburg Keywords: Tropical ecotoxicology Risk assessment Pesticide Microcrustacean Species sensitivity distributions

1. Introduction

~o Carlos, * Corresponding author. NEEA/CRHEA/USP, Escola de Engenharia de Sa Universidade de S~ ao Paulo, Endereço postal: Av. Trabalhador S~ ao-carlense, 400 e ~o Carlos, SP, Brazil. Pq. Arnold Schimidt, Sa E-mail address: [email protected] (R.A. Moreira). https://doi.org/10.1016/j.chemosphere.2019.01.005 0045-6535/© 2019 Elsevier Ltd. All rights reserved.

Whereas many countries located in temperate regions are moving towards reduced pesticide use, developing countries in tropical areas have seen an increase in pesticide use over the past decades (Sanchez-Bayo and Hyne, 2011; Lewis et al., 2016). Brazil, for example, has been the world's largest pesticide consumer since

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2008, accounting for about 20% of the total worldwide pesticide use (Albuquerque et al., 2016). This increasing pesticide use in tropical countries has not been accompanied with a similar trend in studies into pesticide toxicity and risk under local tropical conditions (Lewis et al., 2016; Rocha et al., 2018). Thus, risk assessments in tropical countries, if existing, have largely been based on studies conducted under temperate conditions and with taxa typical for temperate regions (Carriquiriborde et al., 2014; Daam and Van den Brink, 2010; Gunnarsson and Castillo, 2018; Lewis et al., 2016; Pathiratney and Kroon, 2016). Several studies have been conducted over the past decades to compare the sensitivity of temperate and tropical taxa using species sensitivity distributions (e.g. Dyer et al., 1997; Kwok et al., 2007; Maltby et al., 2005; Rico et al., 2011). Several of such studies, however, were hampered due to differences in the taxonomic composition of the temperate and tropical species assemblages used to construct the Species Sensitivity Distributions (SSDs) (Jin et al., 2014). Kwok et al. (2007), for example, noted that differences in species composition between tropical and temperate SSDs were most evident for pesticides because tropical datasets contained much higher proportions of fish data whereas temperate datasets contained large proportions of fish, crustacean, and insect data. A difference in the taxonomic composition of the toxicity data is known to have a pronounced effect on the resulting SSD, and hence on sensitivity comparisons based on these SSDs. Maltby et al. (2005), for example, noted a significant difference between recommended and non-recommended arthropod species in their SSDs constructed for the insecticides carbaryl and chlorpyrifos. This, however, appeared to be due to the greater percentage of crustaceans (as compared to insects) in the recommended arthropod curves, since values of the Hazardous Concentration for 5% of the species (HC5) from SSDs only constructed with crustaceans were no longer distinct between recommended and non-recommended species (Maltby et al., 2005). Previous sensitivity comparisons between temperate and tropical arthropods did not distinguish between crustaceans and insects in their SSDs (Hose and Van den Brink, 2004; Maltby et al., 2005; Rico et al., 2011). Subsequently, the conclusion reached by these studies that there are no consistent differences in sensitivity between temperate and tropical arthropods could theoretically be due to bias introduced by a different and lesser taxonomic diversity in the tropical dataset (Jin et al., 2014). To reduce such bias, sensitivity comparisons should therefore preferably be conducted at lower taxonomic levels. Given the above, the aim of the present study was to compare the sensitivity of temperate and tropical cladocerans to the insecticide chlorpyrifos. To this end, laboratory bioassays were conducted evaluating the acute toxicity of chlorpyrifos to five native cladoceran species of wide occurrence in water bodies of the Neotropical region: Ceriodaphnia silvestrii, Daphnia laevis, Diaphanosoma birgei, Macrothrix flabelligera and Moina micrura. Chlorpyrifos was chosen as the test substance since it is allowed for use to combat pests on a wide variety of crops in both Brazil (MAPA, 2016) and elsewhere (e.g. EC, 2018) and has been detected in Brazilian surface waters (Albuquerque et al., 2016 and references therein). In addition, cladocerans are known to be among the most sensitive species to chlorpyrifos and other insecticides (Daam et al., 2008a, b; Giddings et al., 2014; Van Wijngaarden et al., 2005; Zhao and Chen, 2015). Furthermore, published toxicity data for temperate cladocerans are available enabling a sensitivity comparison between temperate and tropical cladocerans to this insecticide. An additional toxicity data search was conducted for tropical and temperate cladocerans to allow comparing their sensitivity to a wider range of insecticides and cladoceran taxa.

2. Materials and methods 2.1. Cultivation and maintenance of cladocerans in the laboratory Individuals from the selected test species were obtained from ~o Paulo, Brazil, as follows: Cerdifferent localities in the state of Sa iodaphnia silvestrii was collected at the Broa Reservoir (Itirapina, SP; 2211‘33.100 S by 47 53‘16.800 W); Moina micrura and Macrothrix flabelligera were sampled in experimental tanks of the aquaculture ~o Carlos (Sa ~o Carlos, SP; station of the Federal University of Sa 2158‘59.300 S by 47 52‘42.400 W); Daphnia laevis from aquaculture tanks at the National Center for Research and Conservation of Continental Fishes (CEPTA) (Pirassununga, SP; 2156‘04.400 S by 47 22‘22.000 W) and Diaphanosoma birgei was collected at the ~o Carlos, SP; 2159‘09.000 S by 47 52‘50.600 Monjolinho Reservoir (Sa W). After collection, organisms were acclimatized and maintained according to the procedures described in the protocols of the Brazilian Association of Technical Standards ABNT NBR 12713 (2016) and ABNT NBR 13373 (2017). The stock cultures were kept in a room with controlled temperature of 25 ± 1  C and a photoperiod of 12:12 h light/dark cycle. Reconstituted water (pH 7.0e7.8; hardness 40e48 mg CaCO3 L1; electrical conductivity ± 160 mS/cm) prepared according to ABNT standards was used as culture medium. The food consisted of an algal suspension of the microchlorophycean Raphidocelis subcapitata (105 cells L1), supplemented with a mixture of fermented yeast (0.5% v/v) and commercial fish feed (0.5% v/v; Tetramin). This suspension was provided (1 mL L1 culture medium) at each medium renewal, which was made three times per week.

2.2. Acute toxicity tests An analytical standard of chlorpyrifos (CAS number 2921-88-2), purchased from Sigma-Aldrich (purity 99.8%), was used as test compound. Based on preliminary tests conducted in accordance with ABNT (2016), the following five chlorpyrifos test concentrations were selected for the five cladoceran species: 0.01, 0.02, 0.04, 0.08 and 0.16 mg L1 for C. silvestrii; 0.04, 0.08, 0.16, 0.32 and 0.64 mg L1 for D. laevis and D. birgei, and 0.16, 0.32, 0.64, 1.28 and 2.56 mg L1 for M. micrura and M. flabelligera. To this end, a stock solution of 10 mg chlorpyrifos L1 was prepared containing 10% acetone as solvent. Subsequently, besides the chlorpyrifos test concentrations, both a control and solvent control treatment were also tested. All treatments comprised of four replicates, each consisting of a nontoxic polypropylene plastic cup containing 10 mL test solution and five individuals of the respective test organism. The tests were conducted under the same conditions as described for the culture, except that no illumination or food was provided as indicated by ABNT (2016). Forty-eight hours after the start of the test, organisms were evaluated under a stereomicroscope for immobilization, which was determined as the incapacity of organisms to swim after 15s gentle agitating the test vessel. The number of immobile organisms was used to calculate the median effective concentration (EC50), which was calculated as described in the next section. Three definitive tests were performed for each species. At the start and the end of each test, pH (Micronal B374), conductivity and temperature (ORION 145 plus) and dissolved oxygen (YSI 55-25FT) were measured with their corresponding probes, whereas water hardness was measured by EDTA complexometric titration.

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2.3. EC50 calculation

3. Results and discussion

The 48h-EC50 values and their corresponding 95% confidence intervals were calculated with non-linear regression by adjusting a logistic equation to the data using the Statistica 7.0 software (Statsoft, 2004). This curve is described by the following equation: Yi ¼ max/1 þ (Ci/CI50i) bi; Where Yi is the answer of a given parameter; Max is its maximum response; Ci is the chemical concentration i; CI50i is the inhibition concentration of the chemical I and bi is the slope for the chemical I curve.

3.1. Tropical and non-tropical cladoceran sensitivity to chlorpyrifos

2.4. Data mining and species sensitivity distribution curve (SSD) The mean 48h-EC50 values obtained in the three definitive tests for each native species were compared with corresponding values for other cladocerans using the species sensitivity distribution (SSD) approach. Toxicity data for the latter were obtained from the United States Environmental Protection Agency (US-EPA) ECOTOX database (https://cfpub.epa.gov/ecotox/index.html). Geometric means were calculated in cases where more than one 48h-EC50 for immobility was reported for a given species. Log-normal distribution curves of the toxicity values for the native and non-native taxa were constructed separately using the ETX software, version 2.0 (Van Vlaardingen et al., 2004). This software also calculates the HC5 (hazardous concentration for 5% of the species in the species assemblage) and HC50 (hazardous concentration for 50% of the species in the species assemblage) values together with their 95% confidence limits according to Aldenberg and Jaworska (2000). Since the software assumes a log-normal data distribution, lognormality was evaluated with the AndersoneDarling test that is included in the ETX software package, which was accepted at the 5% significance level. Besides the sensitivity comparison of the tested tropical cladocerans with temperate cladocerans, an effort was made to make such a comparison for a wider range of insecticides and cladoceran species. To this end, we downloaded all toxicity data available in the US-EPA ECOTOX for the tropical cladocerans tested in the present study, in addition to tropical cladoceran species recommended for testing in previous studies: Ceriodaphnia cornuta, C. silvestrii, Moina micrura, M. macrocopa, Moinadaphnia macleayi, Diaphanosoma brachyurum, Daphnia lumholtzi, and Pseudosida ramosa (Daam and Van den Brink, 2010; Daam et al., 2011; Mansano et al., 2016). Only toxicity data for compounds indicated as insecticides in the Alan Wood compendium of pesticide common names (http://www. alanwood.net/pesticides/) were considered. For these compounds, cladoceran toxicity data (laboratory 2-4d EC50 for mortality and immobilization; after Brock and Van Wijngaarden, 2012) were compiled from the US-EPA ECOTOX database. As above, geometric means were calculated when more than one toxicity value was available for the same species and compound. To enable grouping toxicity values for different insecticides and cladoceran species in the tropical and non-tropical species assemblages, the toxicity values had to be “normalized”. This was done by applying the relative tolerance (Trel) methodology introduced by Wogram and Liess (2001), i.e. by dividing the toxicity value of a given species with that of the standard test cladoceran Daphnia magna. In this way, a Trel ¼ 1 indicates a sensitivity equal to that of D. magna, whereas a Trel < 1 and Trel > 1 indicate a greater and lesser sensitivity of the cladoceran species as compared to that of D. magna, respectively (Wogram and Liess, 2001).

Physical-chemical parameters remained constant during the tests: pH ¼ 7.2e7.9; hardness ¼ 40e46 mg CaCO3 L1; water temperature 24e26  C; dissolved oxygen 6e7 mg L1 and electrical conductivity ¼ 197e259 mS cm1. Immobility levels denoted in the control and solvent control of all tests were always below of 10% for both. Subsequently, test conditions were stable and the solvent (acetone) did not influence species health. The 48h-EC50 values of chlorpyrifos calculated in the present study for the five cladocerans are presented in Table 1. From this Table, it can be deducted that the order of sensitivity was C. silvestrii > D. birgei ¼ D. laevis > M. micrura ¼ M. flabelligera. C. silvestrii was approximately five times more sensitive than the next most sensitive tropical species tested (D. birgei; Table 1). The sensitivity of C. silvestrii to chlorpyrifos was comparable to that of the most sensitive non-tropical cladoceran included in the SSD analysis (gmEC50 Daphnia ambigua ¼ 0.036 mg L1; Fig. 1). In addition, it was over ten times more sensitive than the standard temperate test species D. magna (gmEC50 ¼ 0.49 mg L1; Fig. 1). However, an assessment factor of 100 is commonly applied to the acute EC50 of D. magna in the calculation of a regulatory acceptable concentration (RAC; e.g. EFSA, 2013). A RAC for chlorpyrifos based on D. magna would hence also be sufficiently protective for the tropical cladocerans tested in the present study. The SSD curves and the HC5 and HC50 values derived from these curves for tropical and non-tropical species also did not indicate differences in their

Table 1 Median effect concentrations (EC50) for immobility and their 95% confidence intervals (in mg/L) obtained for chlorpyrifos in the 48h toxicity tests with the five tropical cladoceran species. Species

EC50

Ceriodaphnia silvestrii Diaphanosoma birgei Daphnia laevis Moina micrura Macrothrix flabelligera

0.039 0.211 0.216 0.463 0.619

(0.002e0.010) (0.081e0.400) (0.050e0.564) (0.145e0.810) (0.200e1.273)

Fig. 1. Species sensitivity distribution (SSD) curves comparing the sensitivity to chlorpyrifos of the tropical cladocerans tested in the present study (circles) and temperate cladocerans (triangles). Toxicity data for temperate cladocerans were obtained from the US-EPA ECOTOX database as explained in the text. gmEC50 ¼ geometric mean of median effect concentrations.

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Species

HC5

HC50

Temperate Tropical

0.033 (0.0078e0.069) 0.032 (0.0024e0.091)

0.18 (0.092e0.34) 0.22 (0.079e0.61)

sensitivity to chlorpyrifos (Fig. 1; Table 2). Thus, a RAC based on the HC5 value from an SSD constructed with toxicity data for chlorpyrifos of a temperate cladoceran species assemblage would also be protective for tropical cladoceran species. Maltby et al. (2005) did not encounter differences in sensitivity of arthropods exposed to chlorpyrifos in model ecosystem studies or laboratory bioassays. In addition, Daam and Van den Brink (2010) denoted an overall (i.e., considering all parameters evaluated) no observed effect concentration (NOEC) of 0.1 mg chlorpyrifos L1 in model ecosystems studies, irrespective of whether the study was conducted under temperate, Mediterranean or tropical conditions. In line with this, the NOEC for the zooplankton communities in these studies are also comparable, despite that the most sensitive cladoceran species in tropical studies are different (Table 3).

Trel

Table 2 Mean values of the hazardous concentration for 5% (HC5) and 50% (HC50) and their 95% confidence intervals (in mg/L) obtained from the SSD analysis. SSD curves were based on acute 48h-EC50 values for chlorpyrifos and constructed separately for the temperate and tropical cladoceran species assemblies.

Fig. 2. Relative tolerance (Trel) values for temperate and selected tropical cladocerans based on toxicity data available in the US-EPA ECOTOX database. Trel values were calculated by dividing the median effect concentration (EC50) of a given species with that of Daphnia magna (after Wogram and Liess, 2001; For details, please see text).

assessment factor of 100 that, as discussed above, is commonly applied to the acute EC50 value of D. magna to set a RAC is sufficiently protective for both non-tropical and tropical cladocerans. 3.3. Implications for the use of temperate toxicity data in tropical risk assessments

3.2. Sensitivity of tropical and non-tropical cladocerans to other insecticides To enable a comparison of tropical and non-tropical cladocerans for a wider range of insecticides and cladoceran taxa, their relative tolerance (Trel) as compared to D. magna was calculated as described in the Materials and Methods section. Trel values could be calculated for 14 insecticides and covered six tropical (17 Trel values) and 14 non-tropical (40 Trel values) cladoceran species. This result confirms the relatively low availability of toxicity data for tropical species as compared to non-tropical species, which has been discussed by many authors (e.g. Carriquiriborde et al., 2014; Lewis et al., 2016; Moreira et al., 2017; Rocha et al., 2018). Fig. 2 shows the calculated Trel values of insecticides other than chlorpyrifos for the tropical and non-tropical cladocerans separately. As can be deducted from this Figure, D. magna is clearly the most sensitive cladoceran in the overall dataset. Subsequently, the

Previous studies have not demonstrated a consistent difference in sensitivity between tropical and temperate aquatic species or (model) ecosystems (Daam and Van den Brink, 2010 and references therein; Dyer et al., 1997; Maltby et al., 2005; Rico et al., 2011; Wang et al., 2014). The present study also did not demonstrate a greater sensitivity of tropical cladocerans to chlorpyrifos or other insecticides as compared to their temperate counterparts (Figs. 1 and 2; Tables 2 and 3). From a Regulatory perspective, these findings thus support the use of toxicity data from temperate regions for the risk assessment of low-persistent insecticides like chlorpyrifos for aquatic communities in tropical regions. Several other authors also concluded that no additional assessment factor is warranted when using temperate toxicity data in other climate zones (Daam et al., 2008a, b; Hagen and Douglas, 2014; Khatikarn et al., 2016). Other studies, however, concluded that an additional assessment factor of two (Rijk, 2010; Wang et al., 2014), four (Wang and Leung, 2015),

Table 3 No observed effect concentrations (NOEC) and lowest observed effect concentrations (LOEC) for zooplankton communities in selected model ecosystem experiments evaluating short-term exposure to chlorpyrifos (single applications except Daam et al. (2008b), who evaluated two applications with a two-week interval) under temperate, Mediterranean and tropical conditions. The most sensitive zooplankton taxa and their respective NOECs in brackets denoted in each of these experiments is also indicated. All data in mg/L. Location Temperate The Netherlands The Netherlands

Mediterranean Spain Portugal Tropical Thailand Thailand a

Experimental design

NOEC

LOEC

Most sensitive cladoceran

Reference

Lentic, outdoor, experimental ditches Lentic, indoor, microcosms Mesotrophic; cool (16e18  C) Mesotrophic; warm (24e28  C) Eutrophic; warm (25e28  C)

0.1

0.9

Daphnia gr. galeata (0.1)

Van den Brink et al. (1996)

0.1 0.1 0.1

1 1 1

Daphnia gr. galeata (0.1) Daphnia gr. galeata (0.1) Daphnia gr. galeata (0.1)

Van Wijngaarden et al. (2005) Van Wijngaarden et al. (2005) Van Wijngaarden et al. (2005)

Lentic, outdoor, mesocosms Lentic, indoor, micrococosms

0.1 <0.17

1 0.17

Daphnia gr. galeata (0.1) Daphnia gr. magna (<0.17)

pez-Mancisidor et al. (2008) Lo Pereira et al. (2017)

Lentic, outdoor, microcosms Lentic, outdoor, microcosms

0.1 <1

1 1

Moina micrura (0.1) C. cornuta/M. micrura (<1)a

Daam et al. (2008a) Daam et al. (2008b)

C. cornuta was more sensitive after the first, and M. micrura after the second application.

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Potentially affected aff f ected fraction

2.2 to 6.2 (Hobbs, 2006) or even ten (Kwok et al., 2007) should be applied when extrapolating temperate toxicity data to tropical regions. According to Lau et al. (2014), an assessment factor of ten may not even sufficient for the studied chemicals. Since there appears to be no universal predictable pattern of toxicity difference between climatically-distinct areas, Chapman et al. (2006) concluded that toxicity data from one geographic region will not be universally protective of other regions. Given that temperate and tropical ecosystems differ considerably in their species traits and composition, as well as their physical-chemical conditions and functioning, the extrapolation of toxicity data between climaticallydistinct areas may indeed be disputed (Batley et al., 2014; Daam € et al., 2018; Sa nchez-Bayo and and Van den Brink, 2010; Ramo Hyne, 2011; Shuhaimi-Othman et al., 2013). Only the use of native species provides an ecologically-realistic assessment of their true sensitivity, besides that this implies fewer logistical constraints and avoids the introduction of exotic species (Mansano et al., 2016). For these reasons, Guidelines of US EPA, Australia and New Zealand recommend using only toxicity data from native species to derive water quality criteria (Zheng et al., 2017 and references therein). As discussed above, several tropical cladoceran species have previously been recommended for use as standard test species in tropical toxicity evaluations (e.g. Daam and Van den Brink, 2010; Daam et al., 2011; Mansano et al., 2016). In Fig. 3, the relative sensitivity of these species is visualized in an SSD constructed with the data that were compiled for the tropical species in Fig. 2. This SSD confirms the high sensitivity of C. silvestrii to insecticides as noted in the present and other studies (Casali-Pereira et al., 2015; Mansano et al., 2016, Fig. 3). Its widespread distribution in the Neotropical realm (Fonseca and Rocha, 2004) makes it a very suitable test cladoceran for tropical South-America, and guidelines for laboratory maintenance and toxicity testing have been previously developed for this species (ABNT, 2017). Moinodaphnia macleayi also appears relatively sensitive to insecticides (Fig. 3), and its use has been recommended for tropical Australia, where test protocols have also been developed for this commonly-occurring species in this region (Riethmuller et al., 2003). Subsequently, appointing a single cladoceran species for use as a “default” standard tropical test species is constrained by limited geographical distributions of species. C. cornuta, however, which also demonstrated a relatively high sensitivity to insecticides (Fig. 3), has been discussed to be widely distributed in tropical regions around the

Moina macrocopa Daphnia laevis Diaphanosoma brachyurum Ceriodaphnia cornuta Moinodaphnia macleayi Ceriodaphnia silvestrii

gmTrel Fig. 3. Species sensitivity distribution (SSD) constructed based on the gmTrel values (geometric mean of relative tolerance values) calculated for the selected tropical cladoceran taxa from insecticide toxicity data available in the US-EPA ECOTOX database. Trel values were calculated by dividing the median effect concentration (EC50) of a given species with that of Daphnia magna (after Wogram and Liess, 2001; For details, please see text).

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world (Barrios et al., 2015; Choueri et al., 2009). Since C. cornuta has also been shown to be sensitive to a wide range of compounds, it has been used and recommended as a test species in different parts of the tropical zone (Barrios et al., 2015; Bui et al., 2016; Do Hong rez-Legaspi et al., 2004; Hong and Li, 2007; Lopes et al., 2011; Pe et al., 2017). In any case, both temperate (C. dubia; Wong et al., 2009; Versteeg et al., 1997) and other tropical representatives of the Ceriodaphnia genus not mentioned above (e.g. C. rigaudi; Mohammed, 2007) appear good sensitive candidates for toxicity testing where available. Conflicts of interest The authors declare that they have no conflict of interest. Acknowledgements We thank the Foundation for Research Support of the State of ~o Paulo (Process number: FAPESP 2017/13288-3). Financial supSa port was also provided to M. Daam by the Portuguese government (FCT) through a postdoc grant for the last author (SFRH/BPD/ 109199/2015) and the research unit UID/AMB/04085/2013 (CENSE). References ~o Brasileira de Normas Te cnicas, 2016. Aquatic Ecotoxicology ABNT - Associaça Acute Toxicity - Test Method with Daphnia Spp (Crustacea, Cladocera) (ABNT NBR 12713), p. 27. cnicas, 2017. Aquatic Ecotoxicology ABNT - Associaç~ ao Brasileira de Normas Te Chronic Toxicity - Test Method with Ceriodaphnia Spp (Crustacea, Cladocera) (ABNT NBR 13373), p. 20. Albuquerque, A.F., Ribeiro, J.S., Kummrow, F., Nogueira, A.J.A., Montagner, C.C., Umbuzeiro, G.A., 2016. Pesticides in Brazilian freshwaters: a critical review. Environ. Sci. Process Impact. 18, 779e787. Aldenberg, T., Jaworska, J.S., 2000. Uncertainty of hazardous concentrations and fraction affected for normal species sensitivity distributions. Ecotoxicol. Environ. Saf. 46, 1e18. Barrios, C.A.Z., Nandini, S., Sarma, S.S.S., 2015. Effect of crude extracts of Dolichospermum planctonicum on the demography of Plationus patulus (Rotifera) and Ceriodaphnia cornuta (Cladocera). Ecotoxicology 24, 85e93. Batley, G.E., Van Dam, R.A., Warne, M.St.J., Chapman, J.C., Fox, D.R., Hickey, C.W., Stauber, J.L., 2014. Technical Rationale for Changes to the Method for Deriving Australian and New Zealand Water Quality Guideline Values for Toxicants. Commonwealth Scientific and Industrial Research Organization (SCIRO) report, Australia, p. 40. Bui, T.K.L., Do-Honga, L.C., Daoc, T.S., Hoang, T.C., 2016. Copper toxicity and the influence of water quality of Dongnai River and Mekong River waters on copper bioavailability and toxicity to three tropical species. Chemosphere 144, 872e878. Brock, T.C.M., Van Wijngaarden, R.P.A., 2012. Acute toxicity tests with Daphnia magna, Americamysis bahia, Chironomus riparius and Gammarus pulex and implications of new EU requirements for the aquatic effect assessment of insecticides. Environ. Sci. Pollut. Res. 19, 3610e3618. Carriquiriborde, P., Mirabella, P., Waichman, A., Solomon, K., Van den Brink, P.J., Maund, S., 2014. Aquatic risk assessment of pesticides in Latin America. Integrated Environ. Assess. Manag. 10, 539e542. Casali-Pereira, M.P., Daam, M.A., Resende, J.C., Vasconcelos, A.M., Espíndola, E.L., Botta, C.M., 2015. Toxicity of Vertimec® 18 EC (active ingredient abamectin) to the neotropical cladoceran Ceriodaphnia silvestrii. Chemosphere 139, 558e564. Chapman, P.M., McDonald, B.G., Kickham, P.E., McKinnon, S., 2006. Global geographic differences in marine metals toxicity. Mar. Pollut. Bull. 52, 1081e1084. ~o, M.G.G., Lombardi, A.T., Vieira, A.A.H., Choueri, R.B., Gusso-Choueri, P.K., Mela 2009. The influence of cyanobacterium exudates on copper uptake and toxicity to a tropical freshwater cladoceran. J. Plankton Res. 31, 1225e1233. Daam, M.A., Crum, S.J.H., Van den Brink, P.J., Nogueira, A.J.A., 2008a. Fate and effects of the insecticide chlorpyrifos in outdoor plankton-dominated microcosms in Thailand. Environ. Toxicol. Chem. 27, 2530e2538. Daam, M.A., Van den Brink, P.J., Nogueira, A.J.A., 2008b. Impact of single and repeated application of the insecticide chlorpyrifos on freshwater plankton communities under tropical conditions. Ecotoxicology 17, 756e771. Daam, M.A., Van den Brink, P.J., 2010. Implications of differences between temperate and tropical freshwater ecosystems for the ecological risk assessment of pesticides. Ecotoxicology 19, 24e37. Daam, M.A., Satapornvanit, K., Van den Brink, P.J., 2011. Applicability of ecotoxicological methodologies dev0eloped in temperate regions for the risk assessment of pesticides in tropical Thailand: from laboratory to (semi-) field. In: Visser, J.E.

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