Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment

I Werner, Swiss Centre for Applied Ecotoxicology Eawag-EPFL, Dübendorf, Switzerland

TM Young, University of California, Davis, CA, United States
© 2018 Elsevier Inc. All rights reserved.

Background

Pyrethroids are synthetic, stabilized derivatives of pyrethrins, insecticidal substances obtained from the flowers of a species of
chrysanthemum (Chrysanthemum cinerariaefolium) (Fig. 1). They are potent neurotoxicants. There are two groups of pyrethroids with
distinctive poisoning symptoms, distinguished by an alpha-cyano group in their structure. While those without an alpha-cyano
group (type I pyrethroids, e.g., permethrin, cismethrin, bifenthrin) exert their neurotoxicity primarily through interference with
sodium channel function in the nervous system, type II pyrethroids (with alpha-cyano group, e.g., deltamethrin, esfenvalerate,
cypermethrin) can affect additional ion-channel targets such as chloride and calcium channels. Apart from their primary mechanism
of action, pyrethroids also modulate the release of acetylcholinesterase in the brain’s hippocampus region and can inhibit ATPases.
In addition, these compounds can disrupt hormone-related functions, with transformation products being more potent endocrine
disruptors than parent compounds. In mammals, pyrethroids decrease progesterone and estradiol production, eliciting estrogenic
effects in females and antiandrogenic effects in males. In fish, exposure to pyrethroids has been shown to increase plasma estrogen
and the estrogen-dependent egg yolk precursor proteins vitellogenin and choriogenin (Crago and Schlenk, 2015, and references
therein). Furthermore, pyrethroids inhibit cell cycle processes, cause cell stress, and have immunosuppressive effects. Metabolism
occurs primarily by microsomal cytochrome P450 enzymes (Werner and Moran, 2008; Palmquist et al., 2012, and references
therein) (Fig. 1).

Current Use

Marketed since the 1970s, use of synthetic pyrethroids increased rapidly following bans or use limitations on cholinesterase-
inhibiting organophosphorus insecticides, such as chlorpyrifos and diazinon, in the USA (2000–01) and EU (2009). Today,
pyrethroids, in particular bifenthrin, cypermethrin, esfenvalerate, l-cyhalothrin, cyfluthrin, and permethrin, are among the most
widely applied insecticides worldwide in agriculture, forestry, horticulture, public health (i.e., hospitals, vector control), and
residential pest control (e.g., landscape maintenance, structural pest control) (Spurlock and Lee, 2008; Palmquist et al., 2012).
They are also used as veterinary medicine (e.g., pet shampoos) in animal husbandry and aquaculture (Langford et al., 2014).
In addition, WHO recommends treating bed nets with pyrethroids in malaria prone areas, due to their relatively low mammalian
toxicity (WHO, 2013).

Properties and Environmental Fate

The primary physical–chemical property that controls the environmental behavior of synthetic pyrethroids is their hydrophobicity,
as reflected in their high octanol–water partition coefficients (KOW). With log(KOW) values ranging from 4 to 7.54 (Table 1), these
compounds tend to complex with dissolved organic matter, partition into suspended solids, accumulate in sediments in surface
water, and partition into lipids in aquatic organisms. It is important to note, though, that accurate measurement of octanol–water
partition coefficients for hydrophobic compounds is experimentally challenging, resulting in rather large discrepancies between
published values of log(KOW) for these compounds as noted in Table 1 for deltamethrin and esfenvalerate, both of which have
discrepancies between reported values exceeding 1.6 log units (i.e., differing by more than a factor of 40). It follows that the KOW can
be a relatively poor predictor of environmental fate and bioavailability of these chemicals (Knauer et al., in press). Atmospheric
transport of pyrethroids is generally minimal because their low vapor pressures (<1.8
107 mmHg) and Henry’s Law constants
(<7.2
103 atm m3/mol) limit transfers to the vapor phase (Laskowski, 2002). Although pyrethroids may bioconcentrate (e.g.,
bioconcentration factors for fish of 359–6060; Laskowski, 2002), depuration is also rapid and bioaccumulation through the food
web is not likely to be a significant route of exposure.
Pyrethroids can be degraded by chemical processes, primarily hydrolysis and photolysis, and via biodegradation. As is true for
many esters, hydrolysis rates increase sharply with increasing pH, with half-lives on the order of days to weeks at pH 9, weeks to
months at pH 7, and limited reactivity for most compounds at pH 5 (Laskowski, 2002). Hydrolysis of the ester bond initially
produces an aldehyde (e.g., 3-phenoxybenzaldehyde) and a carboxylic acid with a structure dependent on the particular pyrethroid.
A key difference between naturally occurring pyrethrins and the synthetic pyrethroids is the much greater resistance of the synthetic
analogs to photolysis. Most of the compounds in Table 1 have aqueous photolytic half-lives ranging from weeks to months, while
some have half-lives longer than 1 year (e.g., 408 d for bifenthrin and 603 d for fenpropathrin; Laskowski, 2002). All pyrethroids are
subject to biodegradation in soils and sediments, but the rates depend significantly on the pyrethroid structure as well as on the

Encyclopedia of the Anthropocene https://doi.org/10.1016/B978-0-12-809665-9.09992-4 119

120 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment

Fig. 1 Structures of the natural pyrethrin and the two types of synthetic pyrethroids.

Table 1 Physical and chemical properties of various pyrethroids

Hydrolysis
Log Solubility Vapor Pressure Henry’s Law Constant Soil Aerobic Soil Anaerobic Half-life
Chemical Kowa,b Kocb (mg/L)a (mm Hg at 25 C)a (atm-m3/mol at 25 C)a Half-life (days)b Half-life (days)b (days)b

Bifenthrin 6, 6.4 237000 0.1 1.8
104 <1.0
103 96.3 425 >30

Cyfluthrin 5.94, 124000 0.002 2.03
109 9.5
107 11.5 33.6 1.84–183
5.97
Lambda- 6.9, 326000 0.003 1.5
109 1.8
107 42.6 8.66– > 30
Cyhalothrin 7.0
Cypermethrin 6.6, 310000 0.004 3.07
109 4.2
107 27.6 55 1.9–619
6.54
Deltamethrin 6.2, <0.002 1.5
108 1.2
104
4.53
Esfenvalerate 4.0, 251700 0.0002 1.5
109 4.1
107 38.6 90.4 >30
5.62
Fenpropathrin 6.0, 0.014 5.5
106 1.8
104
6.0
Phenothrin 7.54 2.0 1.4
107 1.4
106
Permethrin 6.5, 227000 2.2
108 1.9
106 39.5 197 >30–242
6.1
a
Data are cited from USDHHS, 2003.
b
Data are cited from Laskowski, 2002.

environmental conditions. Under aerobic conditions, half-lives measured in soil microcosms were as low as 3 d for permethrin,
while in other cases, such as for bifenthrin, they were longer than 200 d (Meyer et al., 2013). Half-lives were generally somewhat
longer under anaerobic conditions, ranging from a minimum of 21 d (cyfluthrin) to over 200 d (bifenthrin).

Sources of Pyrethroids

The key routes by which pyrethroids enter aquatic systems include drift from aerial or ground-based spraying, agricultural and urban
runoff during rain events, intentional release of agricultural return flows (tailwaters), and municipal wastewater inputs. Obtaining
accurate information regarding pesticide application amounts and timing can be difficult and there are a limited number of
international or national databases to draw upon. The California Department of Pesticide Regulation maintains a long term and
detailed database (http://calpip.cdpr.ca.gov/main.cfm) that allows pesticide usage to be tracked by active ingredient, type of
application (e.g., agricultural or nonagricultural and associated subdivisions), date, etc. The pyrethroids listed in Tables 1 and 2
were those with the largest total mass of active ingredient applied in California in 2014, the most recent year with complete and
 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment 121

Table 2 Environmental detections in water, detection limits, and selected water quality criteria for widely used synthetic pyrethroid insecticides

Active Measured water concentrations California Median of method detection Water quality criteria, Water quality criteria,
ingredient surface water monitoring (ng/L)a limits, California/EU (ng/L) chronic (Country) (ng/L) acute (country) (ng/L)

Permethrin ND/ND/2.2/22 5.0 2CA 10CA

(N ¼ 1177) 1UK 10UK
0.47EUB
Bifenthrin ND/9.1/21/59 2.0 0.6CA 4CA
(N ¼ 846) 0.095EUB
Cyfluthrin ND/ND/2.2/12 5.0 0.2CA 0.8CA
(N ¼ 948) 0.2NL
Cypermethrin ND/ND/ND/3.3 5.0 0.3CA 1CA
(N ¼ 899) 0.08EU 0.6EU
l-Cyhalothrin ND/ND/ND/4.4 2.0 0.5CA 1CA
(N ¼ 903) 0.02NL 0.47NL
0.2EUB
Fenpropathrin ND/ND/ND/ND 3.0 – –
(N ¼ 755)
Esfenvalerate ND/ND/ND/8.4 5.0 0.3CA 2CA
(N ¼ 760; MMDL ¼ 5.0) 0.1NL 0.85NL
Deltamethrin ND/ND/ND/5.5 5.0 0.003NL 0.3NL
(N ¼ 573) 0.7EUB
Phenothrin ND/ND/ND/ND 5.1 – –
(N ¼ 89)
CA
California, USA; EUB European Union Biocide Regulation; UK United Kingdom; NL The Netherlands; EU European Union.
Monitoring results expressed as median/75th percentile/85th percentile/95th percentile. N ¼ number of samples analyzed.
a

searchable data. The compounds are listed in order of amount applied. All other synthetic pyrethroid insecticides registered in
California had total application amounts below 550 kg in 2014. This data only includes applications by registered pesticide
applicators; usage by homeowners is not included and could significantly increase the total amounts applied for some active
ingredients.
The data emphasizes the diverse nature of pyrethroid usage patterns and routes by which the compounds can enter the aquatic
environment. Although the agriculture sector is a major user of insecticides, and uses the vast majority of certain active ingredients
(esfenvalerate, fenpropathrin, cyhalothrin, cypermethrin), nonagricultural use dominates for other active ingredients (phenothrin,
deltamethrin, cyfluthrin). The latter products are used extensively in residential settings to protect structures and gardens.
Because of the importance of rain-driven runoff of pyrethroids, significant research over the past decade has been devoted to
developing accurate databases and predictive models that describe the fraction of applied pesticide mass that washes off from a
variety of sources. For example, Jorgenson et al. (2012) measured the washoff of formulated pyrethroid insecticides in small scale
rainfall simulation experiments over a range of surface types (concrete, soil, and turf ) and conditions (rainfall intensity, time since
application, number of rain events since initial application). They found that between 0.01% and 27% of the applied pyrethroid
washed off during 1 h simulations, with median washoff factors of 0.034%, 0.53%, and 1.9% for turf, soil, and concrete surfaces
respectively. These numbers are consistent with results from other studies, which found washoff factors of 0.12%–27.2%. The
expanding database of insecticide washoff factors under diverse conditions have facilitated construction of detailed models that
predict washoff coefficients as a function of time between application and rainfall, rainfall intensity and duration, and surface type
(Luo et al., 2014). Models such as these have been used to reconstruct historical patterns of pesticide concentrations in surface
waters to augment the limited historical data on environmental concentrations (e.g., Jorgenson et al., 2013).
Wastewater treatment plants (WWTPs) were not initially thought to be a likely source of pyrethroids to the aquatic environment
because high log(KOW) values suggested that the compounds would be efficiently removed by solids removal processes such as
secondary clarifiers. However, recent studies in California showed that effluent of municipal WWTPs can be an important source.
Of 62 effluent grab samples from 31 WWTPs in California, 90% contained detectable concentrations of pyrethroids with maximum
concentrations of 3.9 (bifenthrin), 4 (cyfluthrin), 1.6 (l-cyhalothrin), 13 (cypermethrin), 1.2 (deltamethrin), 0.6 (esfenvalerate),
0.8 (fenpropathrin), and 170 ng/L (permethrin) (Markle et al., 2014). Roughly 5% of pyrethroids were not removed from the
aqueous phase during wastewater treatment. Concentrations in treated effluent showed a decreasing trend with increasing level of
treatment (primary to tertiary treatment). A high percentage of the pyrethroid mass removed is associated with suspended solids in
the wastewater effluent. Toxicity tests in some wastewater effluents indicate that nearly 40% of the sorbed compound is biologically
active, while in a surface water sample approximately 100% of sorbed compound appeared to be bioavailable (Parry et al., 2015).
The bioavailability of sorbed pyrethroids was strongly negatively correlated with particle size.
122 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment

Environmental Occurrence

Although pyrethroids are heavily used worldwide, there is presently limited information on environmental concentrations in
surface waters at the global level (Stehle and Schulz, 2015). Major limitations for obtaining such data are (i) the lack of monitoring
programs in many areas of the world, (ii) the lack of sensitivity of routine chemical-analytical methods for these chemicals, in
particular for analyses of the water phase, and (iii) the challenge of monitoring for chemicals that primarily occur in short-term
pulses. Because pyrethroids are toxic at extremely low water concentrations, monitoring data that are based on insufficiently low
detection limits (>1 ng/L) are of little use. To obtain the required detection limits, the primary strategies have been to rely on
pyrethroid specific detection methods (e.g., negative chemical ionization mass spectrometry, Parry and Young, 2013) and/or to
improve the signal strength by concentrating the compounds using adsorptive methods such as passive sampling (Moschet et al.,
2014, 2015).
Perhaps the most systematic effort to monitor for pyrethroid insecticides in surface waters and sediments and to make the data
broadly available has been made in California. The searchable database of the Department of Pesticide Regulation includes
monitoring data collected by multiple government agencies going as far back as 1995 for some compounds (http://www.cdpr.ca.
gov/docs/emon/surfwtr/surfcont.htm). Over time, two trends are apparent in the data. First, analytical methods have continuously
improved, resulting in far lower detection limits. Second, the attention paid to pyrethroids has led to mitigation measures and better
pesticide stewardship, leading to an overall decrease in the detection of high concentrations. Table 2 summarizes some key results
from the database for the most heavily used pyrethroids in California during the period 2011–15. For each compound, the table
includes some selected concentration descriptors (median value, 75th percentile, 85th percentile, 95th percentile), the number of
samples analyzed and the median method detection limit during the period. With the exception of phenothrin, there are more than
500 samples represented over the 5-year period for each compound in sediment and water. It is important to note that, although the
database includes data obtained across California and is the most comprehensive data the authors are aware of, neither site selection
nor timing is random; it is therefore not appropriate to view the summary statistics as indicating the fraction of waterways statewide
that might be impaired by pyrethroid insecticides. Bifenthrin was the most frequently detected pyrethroid in both surface water and
sediment samples, found at detectable levels in 44% of 846 surface water samples and 63% of 647 sediment samples. This high
detection frequency is likely related to its generally greater resistance to both biotic and abiotic degradation processes, but is also due
to the fact that it has the lowest median detection level of the compounds listed in Table 2 in both water (2 ng/L) and sediment
(0.50 mg/kg). Bifenthrin also has the highest 50th, 75th, 85th, and 95th percentile concentrations in both water and sediments.
Although all of the compounds in Table 2 were detectable in at least 5% of the sediment samples, two (fenpropathrin and
phenothrin) were detectable in fewer than 1.2% of the surface water samples. General trends apparent in Tables 1 and 2 are that
compounds with higher total usage, a higher fraction of nonagricultural usage, and longer degradation half-lives are found most
frequently and at the highest concentrations.
There are fewer data on environmental occurrence of pyrethroids outside of California, however, it is apparent that these
compounds can be found in aquatic systems worldwide. One or more pyrethroids were detected in almost half (45%) of 98 stream
bed sediment samples collected in 2007 from seven metropolitan areas in the United States (Kuivila et al., 2012). Maximum
concentrations were 11.2 mg/kg bifenthrin (most frequently detected), 9.3 mg/kg permethrin, 3.0 mg/kg cyhalothrin, 38.3 mg/kg
resmethrin, and 8.9 mg/kg cypermethrin. Cypermethrin was the most frequently detected pyrethroid in the Ebro River delta, Spain,
with concentrations in water and sediments ranging from 0.73 to 57.2 ng/L and 8.27 to 71.9 mg/kg, respectively (Feo et al., 2010).
Sediments of canals in Ho Chi Minh City, Vietnam, contained 3693 mg/kg (dry weight) permethrin and 478 mg/kg bifenthrin (Le
Thanh et al., personal communication). A study in China detected esfenvalerate, cypermethrin, and permethrin in approximately
80%, and deltamethrin, l-cyhalothrin, and cyfluthrin in 45%–60% of 44 surface sediment samples collected from four lakes,
respectively (Wang et al., 2016). Elevated water and sediment concentrations of cypermethrin and l-cyhalothrin were also reported
from Argentina, Brazil, and Paraguay (Hunt et al., 2016; Jergentz et al., 2005).
Environmental concentrations of pyrethroids, both in water and in sediments, frequently exceed regulatory water quality criteria
and therefore constitute a risk to aquatic organisms (Table 2). A comprehensive analysis of monitoring data of ca. 500 chemicals in
inland surface waters of the European Union (2006–15) showed that pyrethroids, in particular deltamethrin, bifenthrin, and
esfenvalerate, were among the compounds with the highest risk quotients (Lettieri et al., 2016). Similarly, among 302 pesticides
monitored in surface waters of Greece in 2010–12, six pyrethroids were identified as priority substances with long term risk to the
environment, four of them with risk quotients of >1000. Existing analytical methods were considered inadequate, as analytical
reporting limits were above concentrations toxic to aquatic life (Tsaboula et al., 2016). Maximum concentrations measured in Greek
water samples were 316 ng/L l-cyhalothrin, 107 ng/L a-cypermethrin, 156 ng/L cypermethrin, 28 ng/L deltamethrin, 122 ng/L
bifenthrin, and 157 ng/L permethrin. Following an extensive analysis of published data on insecticide concentrations worldwide,
Stehle and Schulz (2015) reported that among 11,300 concentrations detected in surface water samples, 52.4% exceeded their
respective water quality thresholds. The number of exceedances was significantly higher for pyrethroids (65.8%) than for organ-
ophosphate (43.7%) or organochlorine (24.4%) insecticides, even in countries with stringent environmental regulations.
In jurisdictions where water quality criteria are less stringent (but quantifiable) they may not be protective of nontarget species
(Guy et al., 2011).
 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment 123

Environmental Effects
Toxicity to Individuals
Acute toxicity (expressed as the species-specific median lethal concentration (LC50)) of pyrethroids to aquatic species occurs at
water concentrations well below 1 mg/L. Crustaceans and insects are the most sensitive taxa with LC50s in the low ng/L range
(Werner and Moran, 2008). Importantly, daphnids, while the most widely used species in aquatic toxicity testing, are not among the
sensitive taxa (Rico and Van den Brink, 2015; Deanovic et al., 2013).
Sublethal effects are more difficult to detect and quantify than survival, however, they can be of great ecological importance.
Behavioral endpoints are among the most sensitive and ecologically relevant parameters affected by neurotoxic compounds such as
pyrethroids. Abnormal behavior includes, for example, changes in food preference or predator avoidance, activity level, feeding
success, swimming performance, learning, response to predators, reproductive behavior, and social interaction such as aggression.
Such changes can directly translate into increased vulnerability to predation, decreased food intake and growth, and reduced
reproductive success, respectively (Rasmussen et al., 2013). Studies have shown that even brief (24 h) exposure to pyrethroids at
environmental concentrations can cause abnormal swimming behavior, compromise swimming ability and impair reproductive
behavior in fish and aquatic invertebrates; for example, a 5-day exposure to <4 ng/L cypermethrin impaired the response of male
Atlantic salmon to prostaglandin-type pheromones produced in the urine of reproductively receptive female fish (Werner and
Moran, 2008).
Other types of delayed or chronic toxicity can have similarly important consequences for individuals and populations, and are
generally not detected in routine laboratory toxicity tests. Exposure to low concentrations of pyrethroids may require the
expenditure of additional energy for detoxification, metabolism, and restoration of behavioral and physiological homeostasis,
ultimately reducing growth, fecundity, and population size. For example, environmentally realistic concentrations reduced liver
glycogen and growth in exposed fish and aquatic invertebrates at concentrations far below LC50s (reviewed by Werner and Moran,
2008; Palmquist et al., 2012). Altered blood cell counts and increased vulnerability to disease—both observed in fish as a result of
exposure to sublethal concentrations of pyrethroids—may translate to deleterious effects on populations in the field. A shift in
timing of insect emergence or unsuccessful molting due to single short (1–48 h) pulses of 5–10 ng/L esfenvalerate (Palmquist et al.,
2012) may affect not only insect populations but also predators, such as amphibians, fish, bats, and birds, that depend on them as
important food sources (e.g., Hallmann et al., 2014).

Effects on Populations
While indirect effects can decimate populations via, for example, food deprivation, pyrethroids may also directly decrease
reproductive success of aquatic species. These compounds can bind to steroid receptors, with metabolites and transformation
products shown to be more potent than the parent compound. There is evidence that disruption of the endocrine system by
pyrethroids reduces reproductive success of aquatic organisms. In fish, cypermethrin reduced sperm motility (Singh and Singh,
2008) and fertilization success (Werner and Moran, 2008). Exposure to bifenthrin (500 ng/L) altered endocrine signaling, decreased
choriogenin concentrations, and reduced the number of fertilized eggs per female in inland silverside (Brander et al., 2016).
A decrease in fecundity was seen in adult medaka following dietary uptake of esfenvalerate, and larval survival of offspring was
reduced (Werner and Moran, 2008). Consumption of diet containing esfenvalerate by final instar mayfly nymphs reduced the
number and length of eggs in emerged females (Palmquist et al., 2012). In other aquatic invertebrates (daphnids, mysid shrimp),
pyrethroids at concentrations of <10 ng/L reduced fecundity and delayed the age at first reproduction. Population growth rate of
Daphnia magna was inhibited after 24-h exposure to 600 ng/L fenvalerate (Werner and Moran, 2008). While such cause-effect
relationships are extremely difficult to demonstrate in field populations, there is evidence that pyrethroids played an important role
in the decline of several fish species in the Sacramento Bay-Delta (California) (Fong et al., 2016).

Effects on Communities
Field and mesocosm studies measure the effect of chemical exposure on aquatic communities. Unlike single-species toxicity tests,
they incorporate more complex exposure scenarios, interactions between species (e.g., predation pressure, interspecific competition
for resources) as well as—in the case of field studies—exposure to complex mixtures of chemicals and/or multiple stressors. They
also reflect the consequences of sublethal and delayed effects on abundance and community structure.
One-time applications of pyrethroids to mesocosms at doses commonly used for crop protection were shown to cause
significant decreases in abundance and diversity of aquatic invertebrates over several weeks to months (Werner and Moran,
2008; Palmquist et al., 2012). In their review of 75 freshwater field studies with pyrethroids, Hill et al. (1994) concluded that
acute biological effects to aquatic crustaceans and insects occur at application rates equivalent to a single “drift-entry” (1%–5% of
the maximum use-rate) to a surface water body. Recovery is possible, however, it is governed by species-specific attributes, such as
generation time, reproductive rate, and other life history traits as well as re-colonization potential (Werner and Moran, 2008).
124 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment

It follows that species with one or few reproductive cycles per year and no resting stages are most at risk. Physiological adaptation to
insecticides is, however, common in target insects, and known to occur in the amphipod, Hyalella azteca (Weston et al., 2013),
however, it is unknown if this also applies to other taxa.
Pyrethroids tend to quickly dissipate from the water column and bind to organic matter or particles within hours to days (see
above). While environmental fate models such as the FOCUS models assume that such particle-bound chemicals are no longer
bioavailable or toxic, field and field-relevant laboratory studies clearly show that sediment-associated pyrethroids are toxic at
environmentally relevant concentrations (Parry et al., 2015; Ding et al., 2011). Carpenter et al. (2016) showed that bed sediment
concentrations of bifenthrin in urban streams of Oregon (USA) were highly correlated with benthic invertebrate assemblages. The
abundance of sensitive invertebrates, % EPT-taxa (ephemeroptera, plecoptera, trichoptera) and select mayfly taxa was reduced, and
noninsects and tolerant invertebrates dominated streams with high sediment concentrations of bifenthrin.

Chemical Mixtures and Multiple Stressors

In surface waters, the simultaneous occurrence of multiple pesticides and other contaminants is the norm (e.g., Moschet et al., 2014;
Ensminger et al., 2013) thus the combined effects of contaminant mixtures must be considered when evaluating the ecological risks
of pyrethroids (Laetz et al., 2015). While most binary pyrethroid mixtures showed additive responses, synergism was detected in
some cases (Callinan-Hoffmann et al., 2016). Synergistic effects with other types of cooccurring chemicals, especially organophos-
phate and carbamate insecticides, piperonyl-butoxide (PBO, a synergist present in some pyrethroid formulations) and other inert
ingredients of pesticide products, have been reported. For example, the presence of PBO can enhance the toxicity of pyrethroids by
10–150 times (Werner and Moran, 2008).
Organisms in the environment not only experience simultaneous exposure to multiple chemicals but also to additional stressors,
such as disease, temperature stress, oxygen depletion, etc. Simultaneous exposure to toxic chemicals and stressful environmental
conditions can considerably alter the physiological condition and, therefore, susceptibility and ecological fitness of an organism.
For example, water temperature is inversely related to pyrethroid toxicity. Recent studies showed that this effect is mostly due to the
increased sodium current flow through (i.e., increased sensitivity of ) nerve cell membranes at low temperature. In temperate
climates, toxic effects in the field may thus be more severe than expected, as laboratory toxicity tests are generally conducted at
temperatures above 23 C. Unexpected effects may also result from simultaneous exposure to pyrethroids and pathogens. Sublethal
concentrations of esfenvalerate made juvenile Chinook salmon significantly more susceptible to infectious hematopoietic necrosis
virus (Werner and Moran, 2008). Results of such studies demonstrate that pyrethroids may compromise survivorship of aquatic
populations in the field at environmental concentrations.

Summary and Conclusions

The usage of pyrethroid insecticides increased as a response to the phasing out of other insecticide classes. These compounds enter
aquatic environments via drift, runoff from sprayed outdoor areas and effluent of WWTPs. Pyrethroids do not readily volatilize and
exhibit strong adsorption to organic matter, soils and clay, an aspect that largely governs their environmental fate and
bioavailability.
Nontarget aquatic organisms, in particular insects, crustaceans, and fish, are highly sensitive to pyrethroids. At sublethal
concentrations, these compounds disrupt the nervous system leading to deleterious effects on behavior, physical fitness, as well
as impairment of the immune system and reproduction. However, the consequences of delayed toxic effects, effects of multiple
stressors and resulting disturbance of organism behavior and species interactions remain poorly understood. It is therefore not
surprising that toxicity thresholds derived from field studies are lower than those derived from single-species toxicity tests even after
application of safety factors.
Although toxic concentrations of pyrethroids in sediments or surface waters have been reported worldwide, there is limited
information on their temporal and spatial distribution. Samples for analysis are typically taken from large, permanent rivers, while
small streams and ponds where biological productivity is generally higher, tend not to be sampled at all. This underestimates the
true biological impact of runoff. Sensitivity of chemical-analytical methods is often not sufficient to detect benchmark (pg/L) or
effect concentrations (ng/L) in water samples. Monitoring data based on insufficiently low detection limits are of little use, however,
and can convey a false sense of safety with regard to the environmental risk of pyrethroids. This is of special concern where chemical
mixtures or multiple stressors are present, which is the norm in contaminated aquatic environments. For estimating environmental
risk of chemicals in surface water, it is not advisable to rely on analytical data and comparison to quality benchmarks of individual
chemicals alone, as detectability depends on both availability of sensitive analytical methods and reference chemicals.
Widespread use of pyrethroids is expected to continue. In order to protect aquatic environments, exposure models used for
prospective risk assessment during registration of pesticides should be refined to ensure responsible use of these insecticides.
In addition, principles of integrated pest management and best management practices should be applied to prevent pesticide runoff
and drift, and reduce or prevent exposure of nontarget species.
 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment 125

Acknowledgments

The authors are grateful to Dr. Pierre Mineau, Carleton University, Ottawa, Canada, for the invitation to contribute this article to
Encyclopedia of the Anthropocene, and to Dr. Marion Junghans, Swiss Centre for Applied Ecotoxicology, for providing up-to-date
information on water quality criteria.

See also: The Impact of Pesticides on Our Freshwater Resources; Systemic Insecticides and Their Environmental Repercussions.

References

Brander SM, Jeffries KM, Cole BJ, DeCourten BM, White JW, Hasenbein S, Fangue NA, and Connon RE (2016) Transcriptomic changes underlie altered egg protein production and
reduced fecundity in an estuarine model fish exposed to bifenthrin. Aquatic Toxicology 174: 247–260.
Callinan-Hoffmann K, Deanovic L, Werner I, Stillway M, Fong S, and Teh S (2016) An analysis of lethal and sublethal interactions among type I and type II pyrethroid pesticide mixtures
using standard Hyalella azteca water column toxicity tests. Environmental Toxicology and Chemistry 35(10): 2542–2549.
Carpenter KD, Kuivila KM, Hladik ML, Haluska T, and Cole MB (2016) Storm-event-transport of urban-use pesticides to streams likely impairs invertebrate assemblages. Environmental
Monitoring and Assessment 188: 345.
Crago J and Schlenk D (2015) The effect of bifenthrin on the dopaminergic pathway in juvenile rainbow trout (Oncorhynchus mykiss). Aquatic Toxicology 162: 66–72.
Deanovic LA, Markiewicz D, Stillway M, Fong S, and Werner I (2013) Comparing the effectiveness of chronic water column tests with Hyalella azteca (Order: Amphipoda) and
Ceriodaphnia dubia (Order: Cladocera) in detecting toxicity of current-use insecticides. Environmental Toxicology and Chemistry 32(3): 707–712.
Ding Y, Weston DP, You J, et al. (2011) Toxicity of sediment-associated pesticides to Chironomus dilutus and Hyalella azteca. Archives of Environmental Contamination and Toxicology
61: 83.
Ensminger MP, Budd R, Kelley KC, et al. (2013) Pesticide occurrence and aquatic benchmark exceedances in urban surface waters and sediments in three urban areas of California,
USA, 2008–2011. Environmental Monitoring and Assessment 185(5): 3697–3710.
Feo ML, Ginebreda A, Eljarrat E, and Barcelo D (2010) Presence of pyrethroid pesticides in water and sediments of Ebro River Delta. Journal of Hydrology 393(3–4): 156–162.
Fong S, Louie S, Werner I, Davis J, and Connon RE (2016) Contaminant effects on California Bay-Delta species and human health. San Francisco Estuary and Watershed Science 14(4)
jmie_sfews_33448. Retrieved from: http://escholarship.org/uc/item/52m780xj.
Guy M, Singh L, and Mineau P (2011) Using field data to assess the effects of pesticides on crustacea in freshwater aquatic ecosystems and verifying the level of protection provided by
water quality guidelines. Integrated Environmental Assessment and Management 7(3): 426–436.
Hallmann CA, Foppen RPB, van Turnhout CAM, de Kroon H, and Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature
511: 341–343.
Hill IR, Shaw JL, and Maund SJ (1994) Review of aquatic field tests with pyrethroid insecticides. In: Hill IR (ed.) Freshwater Field Tests Hazard Assess. Chem. [Proc. Eur. Workshop
Freshwater Field Tests], pp. 249–271. Boca Raton, FL: Lewis Publisher.
Hunt L, Bonetto C, Resh VH, et al. (2016) Insecticide concentrations in stream sediments of soy production regions of South America. Science of the Total Environment 547: 114–124.
Jergentz S, Mugni H, Bonetto C, and Schulz R (2005) Assessment of insecticide contamination in runoff and stream water of small agricultural streams in the main soybean area of
Argentina. Chemosphere 61: 817–826.
Jorgenson BC, Wissel-Tyson C, and Young TM (2012) Factors contributing to the off-target transport of pyrethroid insecticides from urban surfaces. Journal of Agricultural and Food
Chemistry 60(30): 7333–7340.
Jorgenson B, Brown L, Macneale K, Schlenk D, Scholz NL, Spromberg J, Werner I, Weston D, Young T, Zhang M, and Zhao Q (2013) Predicted transport of pyrethroid insecticides from
an urban landscape to surface water. Environmental Toxicology and Chemistry 32(1): 2469–2477.
Knauer, K., Homazava, N., Junghans, M., Werner, I. (in press). The influence of particles on bioavailability and toxicity of pesticides in surface water. Integrated Environmental
Assessment and Management.
Kuivila KM, Hladik ML, Ingersoll CG, Kemble NE, Moran PW, Calhoun DL, Nowell LH, and Gilliom RJ (2012) Occurrence and potential sources of pyrethroid insecticides in stream
sediments from seven U.S. metropolitan areas. Environmental Science and Technology 46: 4297–4303.
Laetz CA, Hecht SA, Incardona JP, Collier TK, and Scholz NL (2015) Ecological risk of mixtures. In: Amiard-Triquet C, Amiard J-C, and Mouneyrac C (eds.) Aquatic ecotoxicology:
Advancing tools for dealing with emerging risks, pp. 441–462. Cambridge, Massachusetts, USA: Academic Press.
Langford KH, Øxnevad S, Schøyen M, and Thomas KV (2014) Do antiparasitic medicines used in aquaculture pose a risk to the norwegian aquatic environment? Environmental Science
and Technology 48: 7774–7780.
Laskowski DA (2002) Physical and chemical properties of pyrethroids. Reviews of Environmental Contamination and Toxicology 174: 49–170.
Lettieri, T., Chirico, N., Carvalho, R.N., Napierska, D., Loos, R., Sanseverino, I., Marinov, D., Ceriani, L. and Umlauf G. (2016). Modelling-based strategy for the Prioritisation Exercise
under the Water Framework Directive. European Commission, Directorate General Joint Research Centre, Institute for Environment and Sustainability. Draft Report.
Luo Y, Jorgenson BC, Thuyet DQ, Young TM, Spurlock F, and Goh KS (2014) Insecticide washoff from concrete surfaces: Characterization and prediction. Environmental Science and
Technology 48(1): 234–243.
Markle JC, van Buuren BH, Moran K, and Barefoot AC (2014) Pyrethroid pesticides in municipal wastewater: A baseline survey of publicly owned treatment works facilities in California
in 2013. In: Jones RL, Shamim M, and Jackson SH (eds.). Describing the behavior and effects of pesticides in urban and agricultural settings 1168, pp. 177–194.
Meyer BN, Lam C, Moore S, and Jones RL (2013) Laboratory degradation rates of 11 pyrethroids under aerobic and anaerobic conditions. Journal of Agricultural and Food Chemistry
61(20): 4702–4708.
Moschet C, Vermeirssen ELM, Seiz R, Pfefferli H, and Hollender J (2014) Picogram per liter detections of pyrethroids and organophosphates in surface waters using passive sampling.
Water Research 66: 411–422.
Moschet C, Vermeirssen ELM, Singer H, Stamm C, and Hollender J (2015) Evaluation of in-situ calibration of Chemcatcher passive samplers for 322 micropollutants in agricultural and
urban affected rivers. Water Research 71: 306–317.
Palmquist K, Salatas J, and Fairbrother A (2012) Pyrethroid insecticides: Use, environmental fate, and ecotoxicology. In: Perveen F (ed.) Insecticides—Advances in integrated pest
management. Rijeka, Croatia: InTech. ISBN: 978-953-307-780-2 708 pages. https://www.intechopen.com/books.
Parry E and Young TM (2013) Distribution of pyrethroid insecticides in secondary wastewater effluent. Environmental Toxicology and Chemistry 32(12): 2686–2694.
Parry E, Lesmeister S, Teh S, and Young TM (2015) Characteristics of suspended solids affect bifenthrin toxicity to the calanoid copepods Eurytemora affinis and Pseudodiaptomus
forbesi. Environmental Toxicology and Chemistry 34(10): 2302–2309.
Rasmussen JJ, Norum U, Jerris MR, Wiberg-Larsen P, Kristensen EA, and Friberg N (2013) Pesticide impacts on predator–prey interactions across two levels of organisation. Aquatic
Toxicology 140–141: 340–345.
126 Pyrethroid Insecticides—Exposure and Impacts in the Aquatic Environment

Rico A and van den Brink P (2015) Evaluating aquatic invertebrate vulnerability to insecticides based on intrinsic sensitivity, biological trains and toxic mode of action. Environmental
Toxicology and Chemistry 34(8): 1907–1917.
Singh PB and Singh V (2008) Cypermethrin induced histological changes in gonadotropic cells, liver, gonads, plasma levels of estradiol-17 beta and 11-ketotestosterone, and sperm
motility in Heteropneustes fossilis (Bloch). Chemosphere 72: 422–431.
Spurlock F and Lee M (2008) Synthetic pyrethroid use patterns, properties, and environmental effects. In: Gan J, Spurlock F, Hendley P, and Weston D (eds.) Synthetic pyrethroids:
Occurrence and behavior in aquatic environments, pp. 3–25. Washington, DC: American Chemical Society.
Stehle S and Schulz R (2015) Agricultural insecticides threaten surface waters at the global scale. Proceedings of the National Academy of Sciences 112(18): 5750–5755.
Tsaboula A, Papadakis E-N, Vryzas Z, Kotopoulou A, Kintzikoglou K, and Papadopoulou-Mourkidou E (2016) Environmental and human risk hierarchy of pesticides: A prioritization
method, based on monitoring, hazard assessment and environmental fate. Environment International 91: 78–93.
U.S. Department of Health and Human Services (USDHHS) (2003) Agency for Toxic Substances and Disease Registry, “Toxicological Profile for Pyrethrins and Pyrethroids.”
Wang J-Z, Bai Y-S, Wu Y, Zhang S, Chen T-H, Peng S-C, Xie Y-W, and Zhang X-W (2016) Occurrence, compositional distribution, and toxicity assessment of pyrethroid insecticides in
sediments from the fluvial systems of Chaohu Lake, Eastern China. Environmental Science and Pollution Research 23: 10406–10414.
Werner I and Moran K (2008) Effects of pyrethroid insecticides on aquatic organisms. Synthetic pyrethroids, occurrence and behavior in aquatic environments. In: Gan J, Spurlock F,
Hendley P, and Weston D (eds.) pp. 310–334. Washington, DC: American Chemical Society.
Weston DP, Poynton HC, Wellborn GA, Lydy MJ, Blalock BJ, Sepulveda MS, and Colbourne JK (2013) Multiple origins of pyrethroid insecticide resistance across the species complex of
a nontarget aquatic crustacean, Hyalella azteca. Proceedings of the National Academy of Sciences of the United States of America 110: 16532–16537.

Further Reading
http://www.cdpr.ca.gov/docs/emon/surfwtr/surfcont.htm—California Department of Pesticide Regulation, California Monitoring database.
http://www.cdpr.ca.gov/docs/pur/purmain.htm—California Department of Pesticide Regulation, California Pesticide Use Reporting (PUR) database.
https://ec.europa.eu/jrc—EU Joint Research Centre.
http://www.epa.gov/ecotox/—US EPA ECOTOX database.
World Health Organization. World Malaria Report 2013. Geneva: WHO; 2013 [cited 2015 Aug 8]. http://www.who.int/malaria/publications/world_malaria_report_2013/en/.