Long-term stream invertebrate community alterations induced by the insecticide thiacloprid: Effect concentrations and recovery dynamics
Introduction
One of the crucial aims of ecotoxicology is to assess and define the concentration levels at which contaminants cause effects on communities and ecosystems, and to investigate and predict recovery of these systems following toxicant stress (e.g. Campbell et al., 1999, Giddings et al., 2002). Among the contaminants in current use, modern non-persistent insecticides as well as other pesticides are relevant stressors for many aquatic and terrestrial organisms (Liess et al., 2005), and a great number and variety of studies have been conducted to derive and predict the effect concentrations for these toxicants and to understand the processes of recovery from the effects of these contaminants.
Concentration levels for ecological effects of pesticides and many other toxicants are typically derived from laboratory single-species tests. Results of such tests are used for predicting potential effects of toxicants on ecosystems either by applying safety factors (e.g. EEC, 1991) or using species-sensitivity distribution (SSD) methods (e.g. Posthuma et al., 2002). In addition to these predictive methods based on laboratory single-species tests, a wide array of more complex experimental systems is used for validation of the laboratory tests in semi-natural conditions. These model ecosystems, referred to as micro- and mesocosms, are used for risk assessment of pesticides and are known as higher-tier risk assessment testing systems (Campbell et al., 1999).
For pesticides, a recent review focused on comparison of the result from laboratory and mesocosm test systems revealed that effects of these toxicants on biological communities in mesocosms have rarely been observed at concentrations > 10 times lower than the acute Median Effective Concentrations (EC50) obtained for the species known to be sensitive in laboratory conditions (Daphnia magna), and in most cases have been observed at much higher concentrations (Van Wijngaarden et al., 2005). On the other hand, several microcosm studies focused on chronic post-exposure effects of insecticides have shown that these toxicants can have a long-term influence on most sensitive endpoints even at concentrations up to 1000 times lower than the laboratory-generated acute EC50s (for D. magna or sensitive insect species) (Lozano et al., 1992, Liess and Schulz, 1996, Liess, 2002, Beketov and Liess, 2005). In addition, existing field monitoring studies indicate that pesticides may have adverse effects on freshwater invertebrates at concentrations more than 100 times below the laboratory-generated acute EC50s derived for D. magna (Liess and von der Ohe, 2005, Schäfer et al., 2007).
Recovery of ecological systems after chemical stress caused by pesticides and other environmental toxicants currently receives increasing attention from scientists and regulators (Giddings et al., 2002, Barnthouse, 2004, Caquet et al., 2007). Investigations of the recovery processes usually employ micro- and mesocosms. For pesticides, community recovery in mesocosms is frequently observed within a relatively short period after contamination. Thus, for non-persistent insecticides the majority of previously published studies have shown that recovery is already completed within two months after contamination (reviewed by Van Wijngaarden et al., 2005). However, a few long-term mesocosm experiments have revealed that even a single short-term exposure to pesticides may result in long-term and permanent elimination of long-living species if external recolonisation is hampered (Van den Brink et al., 1996, Caquet et al., 2007). Hence, the rapid recovery observed in many mesocosm systems that are predominantly inhabited by short-living organisms (e.g. plankton and short-living benthic insects) and open for external recolonisation (e.g. aerial entry of insects from neighbouring controls) may easily underestimate the recovery duration for communities that include long-living species and are relatively isolated from unimpaired ecosystems (Caquet et al., 2007, Hanson et al., 2007).
Thus for pesticides uncertainty remains regarding both effect concentrations and recovery patterns. In the authors' opinion one main reason for this uncertainty is the paucity of long-term mesocosm experiments employing ecologically realistic communities with a large proportion of long-living taxa and extensive field monitoring studies. Long-term experimental studies are particularly important for understanding effects on long-living species, as experimental observation periods covering significant part of species lifespans are needed to understand duration of effects and recovery patterns (e.g. for univoltine taxa desirable observation period is from > 0.5 year to ≤ 1 year).
Long-term mesocosm experiments are rare. To the authors' knowledge only 5 out of 62 community-level studies on non-persistent insecticides published so far (70 papers) include post-contamination observation periods longer than half a year. These are studies by Brock et al. (1992), Fairchild and Eidt (1993), Van den Brink et al. (1996), Woin (1998), and Hanson et al. (2007) (for the studies reported as paper series, only the first papers are cited). All these investigations were performed with standing-water systems.
Although these long-term studies were not focused on understanding the importance of species' life-cycle traits for post-exposure recovery, two of them have shown that recovery of long-living (univoltine) species after pronounced toxic effect can take long time periods comparable to the species' lifespans (≥ 1 year) (Van den Brink et al., 1996, Woin, 1998). However, the numerical proportion of the long-living species (with generation time ≥ 1 year) in the communities analysed in these two studies was low (about 10 and 24% of the analysed communities respectively; own calculations based on reported information). Besides, long-term effects on the entire community structure were either not found under ecologically realistic conditions (as stated by the authors) because relatively few long-living taxa were affected (Van den Brink et al., 1996) or this aspect was not analysed (Woin, 1998). Importantly, invertebrate communities in natural streams uncontaminated with pesticides usually include much greater proportions of long-living taxa. For example in Europe, the percentage of the taxa having generation time ≥ 1 year in uncontaminated streams in France and Finland varies from 60 to 80% and from 40 to 70% of the overall taxa richness respectively (own calculations with data from Schäfer et al., 2007). However, significance and patterns of the long-term effects caused by single pulse contamination with an insecticide remain to be investigated.
The aim of the present study was to investigate long-term effects of a single pulse contamination with the neonicotinoid insecticide thiacloprid on invertebrate communities of stream mesocosms, which were allowed to establish a community having a relatively high proportion of long-living univoltine taxa (about 50% of the taxa richness at levels of taxonomic identification similar to those used by Schäfer et al. (2007)) for 16 months before contamination. In particular, the objectives were (i) to derive the community Lowest-Observed-Effect Concentration (LOEC) and compare it with laboratory-generated toxicity data, and (ii) to assess the long-term effect-and-recovery dynamics with special focus on short- and long-living taxa. The insecticide was applied as a single pulse to simulate contamination due to spray drift or surface water runoff, which represent a relevant input path for small streams in agricultural areas (Liess et al., 1999, Neumann et al., 2002).
Section snippets
Description of artificial stream system
The mesocosm system used in the present study consisted of 16 artificial streams. Each stream has the following characteristics: length 20 m, width at water surface 0.32 m (± 0.03), average depth 0.25 m (± 0.11), discharge 160 L/min (± 9), slope 2%; approximate total volume 1000 L (range in parentheses). Each stream is designed as a closed circulation system. In this system the water flows as follows: from the upstream to the downstream sections of the stream it is propelled by gravity, then it
Thiacloprid exposure dynamic
In the main experiment thiacloprid concentrations were monitored during the eleven days after exposure (Table 2). As explained above, in order to better examine dynamic of the toxicant in water a complementary experiment was conducted. In this latter experiment thiacloprid was monitored until complete disappearance from the water phase (27 days, Table 3). In both experiments the measured concentrations of thiacloprid were within the range of nominal concentrations after contamination (Table 2,
Comparison of concentrations causing effects in the mesocosm with organism-level toxicity data
As mentioned, for pesticides there is some uncertainty regarding the levels of concentration that cause effects on aquatic non-target organisms in higher-tier test systems. Hence it is interesting to compare the concentrations causing effects in the present mesocosms with available laboratory-generated organism-level toxicity data.
Thiacloprid is known to be selectively toxic to insects (Beketov and Liess, 2008a, Beketov and Liess, 2008b). The lowest acute (observation time 96 h) LC50 known for
Conclusion
We conclude that in mesocosms the long-term (7 month) LOEC calculated for the entire community by multivariate statistical methods can be found at concentrations in the range of the acute LC50 of sensitive species. However, it cannot be excluded that effect on a minority of species can occur at concentrations far below the laboratory-generated acute LC50.
Concerning the post-exposure recovery, we conclude that within the levels of effect concentrations, recovery of the affected organisms may be
Acknowledgements
The authors wish to thank Elke Büttner for the chemical analyses and Paul van den Brink for valuable suggestions on statistical analyses. The research was supported by the European Union (project INTERACT, Marie Curie IIF contract No.MIF1-CT-2006-021860). R.B. Schäfer received funding through a scholarship of the “Studienstiftung des deutschen Volkes e.V.” (Bonn, Germany).
References (51)
- et al.
Effects of four synthetic musks on the life cycle of the harpacticoid copepod Nitocra spinipes
Aquat Toxicol
(2003) - et al.
Indirect effects of contaminants in aquatic ecosystems
Sci Total Environ
(2003) - et al.
Correlation between overall pesticide effects monitored by shrimp mortality test and change in macrobenthic fauna in a river
Ecotoxicol Environ Saf
(1997) - et al.
Determination of insecticide contamination in agricultural headwater streams
Water Res
(1999) - et al.
The significance of entry routes as point and non-point sources of pesticides in small streams
Water Res
(2002) - et al.
Effects of pesticides on community structure and ecosystem functions in agricultural headwater streams of three biogeographical regions in Europe
Sci Total Environ
(2007) - et al.
Mapping ecological risk of agricultural pesticide runoff
Sci Total Environ
(2007) - et al.
Importance of the population structure at the time of toxicant exposure
Ecotoxicol Environ Saf
(1999) Quantifying population recovery rates for ecological risk assessment
Environ Toxicol Chem
(2004)Relative sensitivity to insecticides deltamethrin and esfenvalerate of several aquatic insects (Ephemeroptera and Odonata) and Daphnia magna
Russ J Ecol
(2004)
Acute contamination with esfenvalerate and food limitation: chronic effect on the mayfly Cloeon dipterum
Environ Toxicol Chem
The influence of predation on the chronic response of Artemia sp. populations to a toxicant
J Appl Ecol
Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropods
Environ Toxicol Chem
Potential of 11 pesticides to initiate downstream drift of stream macroinvertebrates
Arch Environ Contam Toxicol
Variability in the rate of egg development of the stonefly, Nemoura cinerea (Plecoptera)
Freshw Biol
Fate and effects of the insecticide Dursban 4E in indoor Elodea-dominated and macrophyte-free freshwater model ecosystem: I. Fate and primary effects of the active ingredient chlorpyrifos
Arch Environ Contam Toxicol
Guidance document on higher-tier aquatic risk assessment for pesticides (HARAP)
Influence of isolation on the recovery of pond mesocosms from the application of an insecticide. 2. Benthic macroinvertebrate responses
Environ Toxicol Chem
Increased sensitivity of the macroinvertebrate Paramorea walkeri to heavy-metal contamination in the presence of solar UV radiation in Antarctic shoreline waters
Mar Ecol Prog Ser
Council Directive of 15 July 1991 concerning the placing of plant protection products on the market
The biological profile of thiacloprid—a new chloronicotinyl insecticide
Pflanzenschutz-Nachr Bayer
Pertrubation of the aquatic invertebrate community of acidic bog ponds by the insecticide fenitrothion
Arch Environ Contam Toxicol
Life cycles and microdistribution of Nemoura cinerea (Retz.) and Nemurella picteti Klap. (Plecoptera: Nemouridae) from two small lowland streams in Southern Poland
Acta Hydrobiol
Community-Level Aquatic System Studies—Interpretation Criteria (CLASSIC)
Influence of isolation on the recovery of pond mesocosms from the application of an insecticide. 1. Study design and planktonic community responses
Environ Toxicol Chem
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