50 Years of Ecotoxicology since Silent Spring – A Review

Abstract

In her book Silent Spring, Rachel Carson describes the cata strophic effects of the indiscriminate use of pesticides in the 1940s and 1950s. These substances, most of them insecticides, have since been designated as persistent organic pollutants and are regulated nationally and internationally. They have sub sequently been replaced by less persistent yet highly toxic compounds. The experience gained in those decades triggered environ mental regulation and risk assessment schemes. The ecotoxicological tests required for risk assessment greatly advanced the development of new concepts and tools in this field. Today, we are no longer faced with disastrous poisonings such as those described in Silent Spring. Nevertheless, the same compounds are still present in the environment adding to the increasing number of chemicals organisms must cope with. Many ecotoxicological questions remain to be solved and new ones have emerged regarding, eg., the effects of nanomaterials, the phenomenon of bee colony collapse disorder, and the consequences of climate change.

Full text

das Umweltmagazin
DAS NEUE HEFT
JETZT AM KIOSK!
KLIMAWANDEL
zeo2 erscheint viermal im Jahr.
Ein Jahresabo kostet 22 Euro, eine einzelne Ausgabe am Kiosk 5,50 Euro.
www.zeozwei.taz.de | zeo2abo@taz.de | T (0 30) 2 59 02-200
ECOLOGICAL PERSPECTIVES FOR SCIENCE AND SOCIETY 21/3(2012): 161– 248
FOCUS: 50 YEARS OF »SILENT SPRING«|ENERGIETRÄGER HOLZ |UMWELTETHIK
Mit freundlicher Unterstützung von
ÖKOLOGISCHE PERSPEKTIVEN FÜR
WISSENSCHAFT UND GESELLSCHAFT
ECOLOGICAL PERSPECTIVES FOR
SCIENCE AND SOCIETY
3|2012
FOCUS: 50 YEARS OF »SILENT SPRING«
ENERGIETRÄGER HOLZ
UMWELTETHIK
GAIA is available online at www.ingentaconnect.com/content/oekom/gaia
www.oekom.de |B54649 |ISSN 0940-5550 |GAIAEA 21/3, 161–248 (2012)
GAIA3_2012_Umschlag_88S 20.09.12 15:49 Seite 1

217
he entry “ecotoxicology” inWikipedia states: “The publication
in 1962 of Rachel Carson’s seminal volume, Silent Spring, cat -
a lysed the separation of environmental toxicology1– and, sub-
sequently, ecotoxicology2– from classical toxicology. The revo-
lutionary element in Carson’s work was her extrapolation from
single-organism effects to effects at the whole ecosystem and
the ‘balance of nature’” (Wiki pedia 2011).
Carson describes the catastrophic effects of the insec ticide
dichlordiphenyltrichlorethane (DDT) and other pesticides often
used in agricultural control programs in the 1940s and 1950s.
They belong to a group of persistent organic pollutants (POPs)
that is now wide ly known as the “dirty dozen”:
aldrin, chlor dane, DDT, dieldrin, endrin, heptachlor,
mirex, toxaphene (in secticides),
poly chlorinated dibenzo-p-dioxins and polychlori nated
dibenzofurans (PCDDs/PCDFs) (combustion by-products
from, e. g., waste incin e ration or the metallurgic industry),
hexachlorobenzene (insecti cide, industrial chemical and
combustion by-product), as well as
polychlorinated biphenyls (PCBs) (industrial chemicals
and combustion by-products).
Since the 1960s, environmental laws have taken effect in many
na tions, an entire new research discipline has emerged, and tools
to detect and predict the hazards and risks of environmental con -
taminants have been developed. But how far have we come in our
efforts to prevent the toxic impacts of pesticides, especially insec -
ticides, and other man-made chemicals in the environment? Can
we detect and prevent the consequences of increasing numbers
and quantities of chemicals in our environment? 50 years after
Silent Spring, it is time to take a look at the state of ecotoxicology.>
Contact: Dr.Inge Werner |Center for Applied Ecotoxicology|Eawag |
BUF15–19|Überlandstr. 133 |8600 Dübendorf |Switzerland |
Tel.: +41 44 8235121 |E-Mail: inge.werner@oekotoxzentrum.ch
Dr.Bettina Hitzfeld |Federal Office for the Environment |
Air Pollution Control and Chemicals Division |Bern |Switzerland |
E-Mail: bettina.hitzfeld@bafu.admin.ch
50 Years of Ecotoxicology since Silent Spring –
A Review
GAIA 21/3(2012): 217– 224
Abstract
In her book Silent Spring, Rachel Carson describes the cata strophic
effects of the indiscriminate use of pesticides in the 1940s and
1950s. These substances, most of them insecticides, have since
been designated as persistent organic pollutants and are regulated
nationally and internationally.They have sub sequently been replaced
by less persistent yet highly toxic compounds. The experience
gained in those decades triggered environ mental regulation and
risk assessment schemes. The ecotoxicological tests required for
risk assessment greatly advanced the development of new con-
cepts and tools in this field. Today,we are no longer faced with
disastrous poisonings such as those described in Silent Spring.
Nevertheless, the same compounds are still present in the environ-
ment adding to the increasing number of chemicals organisms
must cope with. Many ecotoxicological questions remain to be
solved and new ones have emerged regarding, eg., the effects of
nanomaterials, the phenomenon of bee colony collapse disorder,
and the consequences of climate change.
Keywords
environmental regulation, pesticides, persistent organic
pollutants (POPs), risk assessment
GAIA 21/3(2012): 217– 224 |www.oekom.de/gaia
T
©2012 I.Werner, B.Hitzfeld; licensee oekom verlag. This is an Open Access article
distributed under the terms of the Creative Commons Attri bution License
(http://creativecommons.org/licenses/by/3.0), which permits unrestricted use,
distribution, and reproduc tion in any medium,provided the original work is properly cited.
Silent Spring has been instrumental in starting off the field of ecotoxicology.
Reviewing the development of environmen tal regulations as well as pesticide risk assessment,
we show that although much progress has been made in
evaluat ing the risk of chemicals in the environ ment,
many challen ges, like assessing mixture toxicity or
sub-lethal impairment, still remain. Moreover, new
pressing issues, like nanomaterials, have emerged.
Inge Werner, Bettina Hitzfeld
50 Years of Ecotoxicology since
Silent Spring – A Review
FOCUS: 50 YEARS OF »SILENT SPRING«
1 “Environmental toxicology” is the study of harmful effects of chemicals on
living organisms (Newman and Un ger 2003).
2 “Ecotoxicology” is the study of harmful effects of chemicals on ecosystems
(Walker et al. 2001).
217_224_Werner 21.09.12 09:50 Seite 217

www.oekom.de/gaia |GAIA 21/3(2012): 217–224
218 Inge Werner, Bettina HitzfeldFORSCHUNG |RESEARCH
Pest Control: A Brief History of Insecticides –
from DDT to Pyrethroids
There are vast gaps in our knowledge of how dieldrin is
stored or distributed in the body or excreted,
for the chemists’ ingenuity in devising insecticides has
long ago outrun biological knowledge of the way
these poisons affect the living organism.
Rachel Carson (1979, p. 39)3
When Carson wrote her book, the production of synthetic pesti -
cides in the United States (US) had soared from 56362 tons of ac -
tive pesticide ingredients in 1947 to 289240 tons in 1960 – more
than a fivefold increase. By 1993, an estimated 500000 tons were
used in the US annually, and 2000 000 tons worldwide (Winston
1999).In the EuropeanUnion (EU15), 327642 tons were sold in
2001 (Eurostat 2001); almost 2300 tons were sold in Switzerland
in 2008 (FOEN2011).Most toxic among this large group of chem-
icals are the synthetic organic insecticides, which share the com-
mon property of damaging the nervous system of animals.
Most synthetic insecticides belong to a few distinct chemical
groups, each with characteristic properties and toxic mechanisms.
In the 1950s and 1960s, the vast majority fell into two large cate -
gories: the chlorinated hydrocarbons (or organochlorines) and or -
ganic phosphorous compounds (or organophosphates, OPs).
The most prominent organochlorine, DDT, and a number of
related compounds bioaccumulate, due to their stability and fat
solubility in the organisms’ fatty tissues. In addition, they may
bio magnify, which causes progressively higher concentrations
in animals higher up the food chain. Besides, they interfere with
the reproductive systems of birds and other vertebrates. One of
the bet ter known environmental impacts of DDT (or rather its
metabolite, dichlorodiphenyldichloroethylene, DDE) is to reduce
the thickness of egg shells in predatory birds, which caused se-
vere reductions in bird populations (e.g., Hickey and Anderson
1968). The ban on agricultural use of DDT and related chemicals
in 1972 (e. g., Germany, Switzerland, and US) has allowed some
species, such as the brown pelican, to recover in recent years (US
DOI 2009). Worldwide these chemicals have been regulated via
the Stockholm Convention on Persistent Organic Pollutants since 2004
(Stockholm Convention 2004). Under this convention the use of
DDT is allowed solely under specific conditions (inter alia com-
pliance with World Health Organization [WHO]recommenda-
tions) for the control of mosquitoes (Anopheles sp.)car ry ing the
malaria parasite. Lindane and endosulfan have been banned since
2009 and 2011, respectively; however, they can still be applied for
control of head lice (lindane) or for specif ic crop-pest combina-
tions for which a party to the Stockholm Con vention has applied
for an exemption (endosulfan).
OP insecticides, the second group, include compounds like
malathion, diazinon, and chlorpyrifos, which were initially devel -
oped and used as deadly nerve gases during World War II. Since
then, these chemicals have been widely applied as insecticides in
agricultural and urban pest as well as disease control. The OPs
are less persistent but more toxic than organochlorines. Because
of their potential for causing toxicity in humans, especially chil-
dren, some of the most commonly used OPs were ultimately
banned in several countries: Parathion was banned in the US in
2000 and in the EU in 2001. In 2001 the US Environmental Pro -
tec tion Agency (US EPA)placed new restrictions on the use of the
OPs phosmet and azinphos-methyl to increase protection of ag -
ri cultural workers, and residential use of diazinon and chlorpyr -
ifos was phased out in 2003 to 2004. Nevertheless, both are still
registered for use in most countries. To this day, OPs and their
less toxic “cousins”, the carbamates, are among the most wide-
ly applied groups of insecticides in the world (Eurostat 2001,
CDPR 2010).
The ban on certain uses of OP insecticides as well as the emer-
gence of resistant insects has since led to their gradual replace-
ment with other classes of insecticides, among them neonicoti-
noids and pyrethroids. Both are derivatives of natural compounds,
nicotine and pyrethrin, which have long been used as natural in -
secticides. Modern synthetic insecticides are far less persistent
than organochlorines and less toxic to mammals than OPs, but
non-target invertebrates and fish can be susceptible at extremely
low concentrations. This poses new challenges for detection and
regulation. For example, pyrethroids cancause acute toxic effects
to aquatic invertebrates below five nanograms per liter (Werner
and Moran 2008), concentrations that are difficult to measure.
Their input into aquatic ecosystems has long been assumed to be
negligible (due to their chemical properties) until recent studies
demonstrated that toxic amounts were present in water and sed-
iment of surface waters (Weston et al. 2005, Amweg et al. 2006); as
a consequence the California Department of Pesticide Regula tion
reevaluated their registration status in California (CDPR 2006).
In spite of this, pyrethroids continue to be widely used in the US
and elsewhere4for urban as well as agricultural application. In
2010 a total of 294.3 tons (active ingredient) of the two most com-
mon pyrethroids, permethrin and bifenthrin, were applied com-
mercially in California alone (CDPR 2010). For the majority of
countries, such use data is not publicly available.
Current Approaches for Protecting the
Environment
Regulation and Risk Assessment
Manufacturers’ tests on the common laboratory animals – (…)
include no wild species, no birds as a rule, no fishes, and are
conducted under controlled and artificial conditions.
Their application to wildlife in the field is anything but precise.
Rachel Carson (1979, p. 119)
3Silent Spring was first published by Houghton Mifflin, Boston, in1962.
For the relevance of Silent Spring in a historical perspective see Mauch
(2012, in this issue).
4 In the EU, cypermethrin and bifenthrin are registered while the use of
permeth rin is no longer allowed.
217_224_Werner 21.09.12 09:50 Seite 218

FOCUS: 50 YEARS OF »SILENT SPRING«
GAIA 21/3(2012): 217– 224 |www.oekom.de/gaia
219RESEARCH
>
Effect-Based Environmental Criteria
In rivers, a really incredible variety of pollutants combine to
produce deposits that the sanitary engineers can only despairingly
refer to as “gunk”.
Rachel Carson (1979, p. 51)
Effect (or hazard) based environmental quality standards (EQS)
or criteria have been used since the 1970s, after theUS Water Qual -
ity Act of 1965 required the development of numeric criteria for
the protection of human health (Water Quality Act 1965). With
the enactment of the Clean Water Act in 1977, the philosophy of
water pollution control in the US shifted (Clean Water Act 1977).
It became a national policy that “the discharge of toxic pollutants
in toxic amounts be prohibited”. Thus EQS became valuable tools
to assess the risk of individual chemicals in the aquatic environ-
ment. In theEU, theWater Framework Directive (WFD)drives the
derivation of EQS (WFD 2000).TheWFD aims to ensure the good
chemical status of both surface water and groundwater bodies
across Europe. The WFD describes the strategy for the establish-
ment of harmonized quality standards and emission controls for
priority substances posing a significant risk to, or via, the aquat-
ic environment.
Such EQS are an important tool for achieving the protection
goals. However, their usefulness in assessing the combined ef-
fects of chemicals and other stressors (physical, bio logical) and
of chemical mixtures is limited. In addition, the abili ty to derive
EQS for all pesticides of interest – which would be costly but not
impossible – is often hampered by the lack of effect data, and in
some cases, such as for pyrethroids, analytical detection limits
may not be as low as concentrations where toxic effects can oc-
cur. The difficulties to regulate such compounds are significant
as present environmental laws rely heavily on analytical data.
Biological Tools
We are accustomed to look for the gross and immediate effect
and to ignore all else. (…) The lack of sufficiently delicate methods
to detect injury before symptoms appear is one of the great
unsolved problems in medicine.
Rachel Carson (1979, p. 170)
Plant protection products (PPPs) are the chemicals that have been
regulated the longest. In the EU, PPPs may only be sold and used
after they have been shown to not have harmful or unacceptable
effects on humans or the environment, and to be sufficiently ef-
fective. From 1991 until 2011, this was regulated under Directive
91/414/EEC(D91/414/EEC 1991).The review process under this
directive identified 1000 active ingredients on the European mar-
ket. Of these, only 26 percent have subsequently been approved
for use, 67 percent were removed from the market due to with-
drawal by industry or incomplete dossiers, seven percent (about
70 substances) failed the review and were removed from the mar-
ket as no safe use could be shown (European Commission 1993).
To perform this assessment, the directive prescribes ecotoxico-
logical tests in its “uniform principles for the evaluation and au-
thorisation of PPPs”.Here effects of the active ingredient and the
product are tested on non-target species using standardized test
protocols, and then compared with a predicted exposure concen -
tration (figure 1).
So-called toxicity/exposure ratios (TER) for both short- and
long-term exposure are determined that should not exceed cer-
tain trigger values. For example, the ratio between toxicity and ex -
posure for fish and Daphnia magna (figure2, p.220) under acute
exposure conditions should not be below 100(i.e., the predicted
concentration of the PPPs in the environment must not exceed
0.1 microgram perliter, if the measured acute toxic effect concen -
tration in fish is ten micrograms per liter or lower).
In the case of birds and mammals, exposure occurs often via
food, granules, seeds or water as well as preening, thus these ex -
posure routes are considered in risk assessment. Secondary poi-
soning, bioaccumulation, biomagnification, and endocrine effects
are al so taken in to account. In the application of the directive,
guidance on risk assessment procedures for birds and mammals
as well as for aquatic and terrestrial species was developed. This
has had a great impact on the development of ecotoxicological
tests and concepts.
New regulation on PPPs has come into force in the EU in2011
that introduced hazard based cut-off criteria: PPPs must not have
CMR (carcinogenic, mutagenic or reprotoxic), POP (persistent or -
ganic pollutant), PBT (persistent, bioaccumulative, toxic) or vPvB
(very persistent, very bioaccumulative) characteristics or cause
en docrine disruption (Regulation [EC]No 110 7/2009).5The devel -
opment of these criteria and their application as a “no-go” in the
registration process of PPPs are crucial steps towards the protec-
tion of the global environment and human health,however, it is
quite apparent that the concerns raised by Rachel Carson are still
relevant today.
The components of environmental risk assessment. Both biolog-
ical effect thresholds and exposure concentration and routes are considered
when deriving toxicity/exposure ratios.
FIGURE 1:
5 In contrast, industrial chemicals with PBT properties are not completely
banned in the EU but have to be registered according to Registration, Evalu -
ation, Autho risation and Restriction of Chemicals (REACH)(Scheringer 2012,
in this issue). PPP regulation is stricter than REACH as PPPs are brought
direct ly into the envi ronment under normal use conditions. This is effec tive
under Regula tion (EC)No 110 7/2009 when new active substances are to be
registered.
217_224_Werner 21.09.12 09:50 Seite 219

www.oekom.de/gaia |GAIA 21/3(2012): 217–224
Inge Werner, Bettina HitzfeldFORSCHUNG |RESEARCH220
Long before the onset of environmental regulation, biological tools
based on indicator species were used to detect environmental haz-
ards, such as the “canary in the coal mine” used to warn miners
of dangerous levels of carbon monoxide and methane. Standard-
ized biological methods to measure water quality developed quick-
ly after the US EPA initiated a national policy in 1984 to control
toxic substances based on a water quality approach. The issuance
of permits for effluent discharges into surface waters was subse -
quently tied to whole effluent testing using standardized toxicity
tests.6Such tests enable the direct measurement of toxicity inde -
pendent of the number of causative chemicals or mixture effects.
In addition, aquatic community indices such as the saprobic (Kolk-
witz and Marsson 1909) or SPEAR (SPEcies At Risk) indices (Liess
et al. 2008)integrate the effects of all chemical, physical, and bio -
logical stressors acting in a system.Bioassays can measure mecha -
nism-specific(in vitro)or integrative(in vivo)toxic effects and pro-
vide the data needed for the derivation of EQS. The measurement
of toxic effects due to low-level, pseudo-persistent contamination
or intermittent exposure to pollutants, however, poses new chal-
lenges in monitoring, especially where predictive indicator tools
are required. Technological advances in biochemistry and molec -
u lar biology increasingly enable us to refine these tools, but many
gaps in our ability to diagnose the health of organisms or ecosys-
tems remain (see also Challenges below) due to temporal and fi-
nancial restrictions that are necessarily present when using bio -
assays in regulatory and scientific investigations: 1. Standardized
test systems rely on measuring responses in model species that
may not be representative of more vulnerable species. 2.Likewise,
toxicity endpoints (parameters quantified in toxicity tests) that can
easily be measured in laboratory settings may ignore many of the
intricate, more sensitive functions or species interactions that are
essential for the ecological fitness of an organism and populations.
Molecular techniques looking at changes in gene expression or
proteins (e.g., toxicogenomics and proteomics) hold much prom -
ise, and will likely become an essential aspect of any biomarker
portfolio developed for resident species in the near future, espe -
cially because of their versatility in studying different species and
endpoints. The potential power of these methods is already be-
ing demonstrated in management (Ankley et al. 2006), and inter -
national standardization efforts are underway. There is, however,
a great need for studies linking molecular responses to higher-
level effects such as growth, reproduction, and survival, so that
results can be interpreted in an ecological context (Fedorenkowa
et al. 2010). The promising concepts of “adverse outcome path-
ways (AOP)” (Kramer et al. 2011) and systems biology (Garcia-
Rey ero and Perkins 2011) aim at establishing these linkages, how-
ever, integration of such concepts into hazard or risk assessment
will require the standardization of methods (Van Aggelen et al.
2010). From this it may seem that community indices would cur-
rently be the most integrative and the most meaningful parame -
ters to monitor the consequences of toxic chemicals in the envi -
ronment, but such indices often do not allow an identification of
the causative agents. Many field studies, therefore, result in the
conclusion that multiple stressors are causing a negative impact
at the population level. Despite 50 years of research and many
more tools at our disposal, our ability to measure and detect or
even predict the impact of toxic chemicals in our environment
is still insufficient.
Challenges in Assessing the Environmental
Impacts of Chemicals
Just like when Carson rang the alarm bells, insecticides and oth-
er pesticides continue to pose a significant threat to surface wa-
ter quality. Although their application has become less careless
and the compounds less persistent, they have become an essen-
tial part of our modern world and still enter our natural environ -
ment in considerable amounts.
The Toxic Effects of Chemical Mixtures
Another almost unexplored area is the question of interactions
between chemicals, (…) All of these questions urgently require
the precise answers that only extensive research can provide,
yet funds for such purposes are pitifully small.
Rachel Carson (1979, p. 141)
The waterflea,Daphnia magna,is one of the most sensitive indica-
tor organism for the toxic effects of insecticides in the aquatic environment.
FIGURE 2:
6http://water.epa.gov/scitech/methods/cwa/wet/index.cfm
©Christian Rellstab/Eawag
217_224_Werner 21.09.12 09:50 Seite 220

FOCUS: 50 YEARS OF »SILENT SPRING«
GAIA 21/3(2012): 217– 224 |www.oekom.de/gaia
221RESEARCH
In the 1990s, a US-survey showed that over 50 percent of more
than 4000 stream water samples contained six or more pesticides
(Gilliom et al. 1999). Such chemical mixtures must be considered
to be the most common exposure scenario in the envi ron ment.
To date, however, regulatory requirements on risk as sessments
of chemicals are largely based on individual substances. It was on -
ly within the last decade that broad interest in the need for assess -
ing the risks of combined exposure to multiple substances start-
ed to mount. Available approaches for assessing the toxicity of
chemical mixtures include mathematical models (Backhaus and
Faust 2012) and biological tools (figure 3, see also Biological Tools
above). Only well-defined mixtures can be assessed using the two
classical mathematical models: concentration addition (mixture
ingredients have the same mechanism of action) and indepen -
dent action (mixture ingredients have different mechanisms of ac -
tion). Biological tools allow quantification of the combined effects
of chemical mixtures even if ingredients are unknown; however,
the choice of test species and endpoints is crucial for obtaining
meaningful data.Where in vitro methods exist to quantify specif -
ic toxic effects, e.g., inhibition of the enzyme acetylcholine ester -
ase in nerve cells (by OPs and carbamates) or of photosynthesis
in algal cells (primarily by herbicides), effects can be expressed as
toxicity equivalents normalized to a reference substance, which
allows comparison across mixtures containing different concen-
trations and chemicals (Escher et al. 2008).
Multiple regulatory agencies (e.g., the European Food Safety
Agency [EFSA], US EPA, and UK Intergovernmental Group on
Health Risks from Chemicals) have recently issued or updated
guidance documents for addressing mixture toxicity assessment.
In 2009 the EU Council asked the EUCommission to advise on
the adequacy of current legislation for addressing the toxicology
of mix tures and to propose appropriate guidance (Korten kamp et
al. 2009). A WHO International Programme on Chemical Safety
(IPCS) framework for risk assessment of combined exposures to
multiple chemicals was presented at a workshop of WHO, Orga -
ni zation for Economic Cooperation and Development(OECD),and
International Life Sciences Institute – Health and Environmen-
tal Sciences Institute (ILSI–HESI) in 2010 (Meek et al. 2011). Its
application in the regulatory process will be a great step forward
in evaluating the risks of chemical mixtures in the environment.
Chronic Poisonings
Because these small amounts of pesticides are cumulatively
stored and only slowly excreted, threat of chronic poisoning and
degenerative changes of the liver and other organs is very real.
Rachel Carson (1979, p. 36)
There is a wide range of possible contaminant effects that can
compromise the ecological fitness of individual organisms or a
population.Ultimately, the impact a toxic contaminant or contam -
inant mixture may have depends on, most importantly, the rela -
tive sensitivity of the species as well as the intensity and timing
of exposure. Acutely toxic events, most visibly fish kills, that were
relatively common a few decades ago, are now rarely observed.
However, chronic effects in the form of sub-lethal damage to or-
ganisms can be observed at concentrations found in the environ -
ment. These include impairment of the reproductive (Sumpter
2005) or immune system (Arkoosh et al. 2001), and genetic (Shu -
gart 1995), developmental, and behavioral changes (Weis and Weis
1995, Sandahl et al. 2007). They can severely reduce ecological fit-
ness and ultimately survival, since the individual must be able to
successfully compete with others for food, avoid predation, repro -
duce, and cope with pathogens and other environmental stressors.
Such effects are not easily detected and can act for long periods
of time before being recognized.
Endocrine disruption is a very prominent example of such sub-
lethal effects: endocrine disrupting chemicals (EDCs) interfere
with the normal functioning of the endocrine system. Exposure
to ex tremely low concentrations can impede gonadal function,
re duce fertilization success, decrease fecundity, and alter mating
behavior (Sumpter 2005,Martinovic et al. 2007) in aquatic species.
One of the more potent estrogens found in surface waters is 17
al pha-ethinylestradiol (the synthetic estrogen used in birth-con-
trol pills). This compound, like natural estrogens, is not complete -
ly removed by sewage treatment plants (Johnson and Williams
2004), and can cause the collapse of fishpopulations at trace con-
centrations of lower than six nanograms per liter (Kidd et al. 2007).
Other known EDCs include industrial chemicals and waste prod -
ucts, such as PCDDs, PCDFs andPCBs, organochlorine and pyre -
throid pesticides (and their metabolites), surfactants, as nonylphe -
nol polyethoxylates used in pesticide formulations, and phthalates
used in plastic products (Scheringer 2012, Langston 2012, both
in this issue). Despite decades of research, no water or sediment
quality criteria currently exist for protect ing human and aquatic
life against endocrine disruption and its related effects.
Laboratory to Environment Extrapolation
Campus earthworms had been fed inadvertently to crayfish in a
research project and all the crayfish had promptly died.
Rachel Carson (1979, p. 62)>
Current approaches to measure or predict the combined effects of
chemical mixtures. Mathematical models require both exposure and effect data
to predict toxicity, while biological methods measure toxicity directly.
FIGURE 3:
217_224_Werner 21.09.12 09:50 Seite 221

222 Inge Werner, Bettina HitzfeldFORSCHUNG |RESEARCH
In the past, serious environmental threats caused by pollutants
have primarily been brought to light as a result of observing se-
vere biological effects in the field. Examples include DDE and egg -
shell thinning in birds (Hickey and Anderson 1968), sex changes
in freshwater fish associated with EDCs (Vos et al. 2000), and tu-
mors in marine fish associated with polycyclic aromatic hydro-
carbons (Baumann and Harshbarger 1995). In order to prevent
such ecological damage before it occurs, there is an urgent need
for techniques that detect the less obvious sub-lethal impairment
that might ultimately result in population level effects (Depledge
and Galloway 2005).
Effectively linking the effects of pollutants in laboratory bioas-
says through the various hierarchical levels of biological organi -
za tion to ecosystem and potentially human health requires a prag -
matic integrated approach based on existing data that ei ther links
or correlates processes of pollutant uptake, detoxifica tion and pa -
thology with each other and higher level effects (Depledge 2009).
Portfolios of carefully selected biological indicators, including lab-
oratory bioassays, analysis of biomarkers – molecu lar, biochemi -
cal, cellular, and physiological alterations caused by external stres-
sors (Van der Oost et al. 2003, Forbes et al. 2006)– in spe cies of
concern, field studies, and a thorough understanding of organis -
mal function, species interactions as well as the influence of addi -
tional physical and biological stressors (e.g., disease, food deple -
tion) are required to evaluate toxicity and assess the risk to eco -
systems. New information on toxic mechanisms and biological
approaches (e. g., AOPs) hold much promise in this regard, but
the level of uncertainty in predictions will remain high in the
foreseeable future. Application of the “precautionary principle”
(EEA 2001) will therefore be needed for some time.
Burning Topics
Nanomaterials
What are the effects? Rachel Carson (1979, p. 208)
Nanomaterials have special properties due to their nanoscale di-
mensions. They are defined as materials with a particle size less
than 100 nanometer in at least one dimension. Thus their toxico -
logical properties might be different than that of “classical” parti -
cles or substances. Manufactured nanomaterials are in use in a
multitude of products, including pesticides (Khot et al. 2012). Their
uses bring benefits but their risks have until now not been fully
understood. New regulations will require information on the eco -
toxicological effects of nanomaterials. The development of ade-
quate test methods is currently one of the big challenges for eco-
toxicologists.
Bee Colony Collapse Disorder
But in May of that year this man lost 800 colonies after
the state had sprayed a large area. (…) Another beekeeper,
whose 400 colonies were incidental targets of the 1957 spray,
reported that 100 per cent of the field force of bees(…) had been
killed in forested areas and up to 50 per cent in farming areas
sprayed less intensively. “It is a very distressful thing,” he wrote,
“to walk into a yard in May and not hear a bee buzz”.
Rachel Carson (1979, p. 146)
The “pollinator crisis” or the “colony collapse disorder” has been
one of the biggest environmental concerns in recent years (UNEP
2010, SETAC 2011). Pollinators play a central and crucial role in
the boosting of reproduction of wild plants and in fruit produc-
tion of many commercial crops. The value of the polli nation ser -
vice rendered by managed pollinating species such as the honey -
bee, Apis mellifera, has been estimated to be in the order of 22.8
to 57billion Eu ros. An unusual reduction in managed honeybee
col ony numbers has been observed since 1998 in many Europe -
an countries, North America, China, and North Africa. The caus-
es for this decrease have not yet been elucidated completely and
are probably multifactorial (the UN report identifies habitat de-
struction, increased pathologies, invasive species, and pollution).
Pesticides have been implicated by many studies, among them
herbicides, broad-spectrum as well as systemic insecticides, such
as the neonicotinoids used in seed treatment (EFSA2012, Hen-
ry et al. 2012).
POPs Are Still with Us
To find a diet free from DDT and related chemicals, it seems
one must go to a remote and primitive land, still lacking
the amenities of civilization. Such a land appears to exist,
at least marginally,on the far Arctic shores of Alaska –
although even there one may see the approaching shadow.
When scientists investigated the native diet of the Eskimos
in this region it was found to be free from insecticides. (…)
There was only one exception – two white owls from
Point Hope carried small amounts of DDT,perhaps
acquired in the course of some migratory journey.
Rachel Carson (1979, p. 163)
While Carson described the Arctic as free from contamination of
organochlorine pesticides, she recognized that the contaminants
might eventually enter these remote regions and foresaw one of
the possible pathways via migratory species. Nowadays, we know
that the Arctic (and Antarctic)is not“free from DDT and related
chemicals” and recognize that these regions and the Inuit peo-
ple are especially vulnerable due to the long-range transport and
biomagnification properties of POPs (Scheringer 2012, in this
is sue). 42 years after Carson’s description of their effects on wild -
life, POPs have been prohibited globally for production and use
since 2004 (Stockholm Convention 2004). To date, 177 countries
are parties to the Stockholm Convention, and in 2009 and 2010 ten
POPs were added to the list (see Stockholm Con vention 2004 for
further details). The international community has thus banned a
total of 22 substances with POP properties. However, the identi -
fi cation of additional POPs still in use today and the global moni -
tor ing of banned POPs remain challenges for both the scientific
and regulatory communities.
www.oekom.de/gaia |GAIA 21/3(2012): 217–224
217_224_Werner 21.09.12 09:50 Seite 222

FOCUS: 50 YEARS OF »SILENT SPRING«
GAIA 21/3(2012): 217– 224 |www.oekom.de/gaia
223RESEARCH
>
Climate Change
The amount of food available, conditions of weather and climate,
the presence of competing or predatory species, all are critically
impor tant.
Rachel Carson (1979, p. 215)
The expected impacts of climate change on the toxicological and
ecotoxicological effects of POPs have recently been described in
an expert group report by the United Nations Environment Pro-
gramme (UNEP) and the Arctic Monitoring and Assessment Pro-
gramme (AMAP)(UNEP/AMAP 2011). Climate change can affect
the environmental fate of chemicals in many ways, most notably
through the intensity of storms and changes in abiotic parame -
ters, such as temperature, salinity,pH, and UV radiation. In turn,
these factors can modify uptake, metabolism and toxicity of chem-
icals and alter trophic structures and interactions as well as phys -
i o logical and behavioral adaptation mechanisms. The report con-
cludes that it is uncertain in which animal or human populations
or regions the toxic effects of POPs will increase or decline as a
result of climate change.
Are Pesticides Safer Today?
A few minutes’ research in any supermarket is enough to alarm
the most stouthearted customer – provided, that is, he has even a
rudimen tary knowledge of the chemicals presented for his choice.
The display is homey and cheerful, and, with the pickles and olives
across the aisle and the bath and laundry soaps adjoining,
the rows upon rows of insecticides are displayed.
Rachel Carson (1979, p. 158)
50 years ago, concerns over pesticide effects on human health
and the environment werelargely focused on organochlorine in -
sec ti cides. Compared to today, the number of chemicals under
consid eration was low and their toxic effects in the environment
were obvious.The highly persistent chemicals were measurable
in sediments and tissues making it possible to track their move-
ment to the current day. After their ban in the US, the number
and diversity of pesticide products greatly expanded. Organophos -
phates and others are by design less persistent than the “legacy
pesticides” and many are difficult to measure at concentra tions
toxic to aquatic organisms (Kuivila and Hladik 2008).Indi rect ef -
fects on fish and other predators via food depletion (phyto- and
zooplankton) can be important factors in population dynam ics.
Modern pesticides are highly effective and designed to disrupt the
physiology of specific taxonomic groups; nevertheless, it has been
nearly impossible to manufacture a pesticide that is selective for
the target species yet nontoxic to other species, particu larly close-
ly related taxa. Thus, there is an enduring trade-off between the
societal benefits of applying pesticides (e.g., increased agricultur -
al production, reductions in vector-borne diseases) and minimiz -
ing unintended impacts on aquatic ecosystems and human health.
Despite successes in improving water quality in many nations,
surface waters today are still not providing healthy habitats for
fish. Habitat degradation, including the effects of chemi cals, and
nonindigenous species were named as the main threats to at-risk
fishes (Jelks et al. 2008). 50 years after Silent Spring, a significant
number of issues related to the environmental effects of these
chemicals remain to be solved. We have undoubtedly acquired
more knowledge, but the complexity of ecosystem function still
poses enormouschallenges inour ability to predict,mea sure, and
reduce the environmental risks of chemicals.
References
Amweg, E.L., D. P. Weston, J. You,M.J. Lydy.2006. Pyrethroid insecticides
and sediment toxicity in urban creeks from California and Tennessee.
Environmen tal Science and Technology 40/5: 1700–1706.
Ankley,G. T. et al. 2006.Toxicogenomics in regulatory ecotoxicology.
Environmen tal Science and Technology 40/13: 4055– 4065.
Arkoosh,M.R. et al.2001. Increased susceptibility of juvenile chinook salmon to
vibriosis after exposure to chlorinated and aromatic compounds found in
contaminated urban estuaries. Journal of Aquatic Animal Health 13:257 –268.
Backhaus, T., M. Faust. 2012.Predictive environmental risk assessment of
chemical mixtures: A conceptual framework. Environmental Science and
Technology 46/5: 2564 –2573.
Baumann, P. C., J.C. Harshbarger.1995. Decline in liver neoplasms in wild
brown bullhead catfish after coking plant closes and environmental PAHs
plummet. Environmental Health Perspectives 103/2: 168– 170.
Carson, R. 1979 (orig. 1962).Silent spring. Middlesex, UK: Penguin.
CDPR (California Department of Pesticide Regulation). 2006. Reevaluation.
www.cdpr.ca.gov/docs/registration/reevaluation/chemicals/pyrethroids.
htm (accessed August 18,2012).
CDPR. 2010. Pesticide use reporting database. www.cdpr.ca.gov/docs/pur/
purmain.htm (accessed July 10, 2012).
Clean Water Act.1977.Clean Water Act of 1977. Public Law 95-217, December
27,1977. United States Statutes at Large 91:1566–1611.
D91
/414/EEC.1991. Council Directive 91/414/EEC of 15 July 1991concerning
the placing of plant protection products on the market. Official Journal of
the European Union L 230, 19.8.1991:1–32.
Depledge, M.H. 2009. Novel approaches and technologies in pollution
assess ment and monitoring: A UK perspective.Ocean and Coastal
Manage ment 52: 336– 341.
Depledge, M.H., T.S. Galloway.2005. Healthy animals,healthy ecosystems.
Frontiers in Ecology and Environment 3/5: 251–258.
EEA (European Environment Agency). 2001. Late lessons from early warnings:
The precautionary principle 1896– 2000.Copenhagen: EEA.
EFSA (European Food Safety Authority). 2012. Assessment of the scientific
infor mation from the Italian project “APENET” investigating effects on
honeybees of coated maize seeds with some neonicotinoids and fipronil.
EFSA Journal 10/6: 2792 –2818.
Escher,B., N. Bramaz, J.F. Mueller,P. Quayle, S.Rutishauser, E.L. M.Vermeirssen.
2008. Toxic equivalent concentrations(TEQs)for baseline toxicity and
specif ic modes of action as a tool to improve interpretation of ecotoxicity
testing of environmental samples. Journal of Environmental Monitoring 10:
612– 621.
European Commission.1993.Review programme of existing pesticides: Overview.
http://ec.europa.eu/food/plant/protection/evaluation/rev_prog_exist_
pest_en.htm (accessed October 20, 2011).
Eurostat. 2001.Verkauf von Pflanzenschutzmitteln. appsso.eurostat.ec.europa.eu/
nui/show.do?dataset=food_in_apest1&lang=de(accessed October 20, 2011).
Fedorenkowa, A., J.Arievonk, H. J. Roblenders, N. Joopouborg, A. Breure,
A. Janhendriks. 2010. Ecotoxicogenomics:Bridging the gap between genes
and populations. Environmental Science and Technology 44/11: 4328 – 4333.
FOEN (Federal Office for the Environment). 2011. Environment Switzerland
2011. Bern: FOEN. www.bafu.admin.ch/umwelt/10822/10823/index.html?
lang=en (accessed October 28, 2011).
217_224_Werner 21.09.12 09:50 Seite 223

www.oekom.de/gaia |GAIA 21/3(2012): 217–224
224 Inge Werner, Bettina HitzfeldFORSCHUNG |RESEARCH
Bettina Hitzfeld
Born 1961 in Luxembourg, Luxembourg. PhD 1991.
Since 2002 at the Swiss Federal Office for the Environment,
Bern, and since 2007 head of the Section Biocides and
Plant Protection Products. Areas of expertise: risk
assessment of biocides and plant protection products,
ozone depleting substances, synthetic climate change gases,
multilateral environmental agreements.
Forbes,V.E., A.Palmqvist, L.Bach. 2006.The use and misuse of biomarkers
in ecotoxicology.Environmental Toxicology and Chemistry 25/1: 272– 280.
Garcia-Reyero, N., E.J. Perkins.2011. Systems biology: Leading the revolution
in ecotoxicology.Environmental Toxicology and Chemistry 30/2: 265 –273.
Gilliom, R.J., J. E.Barbash, D.W. Kolpin,S. J. Larson. 1999. Testing water quality
for pesticide pollution. Environmental Science and Technology 33/7: 164–169.
Henry,M. et al.2012.A common pesticide decreases foraging success and
survival in honeybees. Science 336/6079: 348– 350.
Hickey,J.J., D.W. Anderson. 1968. Chlorinated hydrocarbons and eggshell
changes in raptorial and fish-eating birds. Science 162/3850: 271– 273.
Jelks, H.L. et al. 2008. Conservation status of imperiled North American
freshwa ter and diadromous fishes. Fisheries 33/8: 372– 407.
Johnson, R.C., R. J. Williams. 2004.A model to estimate influent and effluent
concentrations of estradiol, estrone, and ethinylestradiol at sewage treat-
ment works. Environmental Science and Technology 38/13: 3649– 3658.
Khot, L.R. et al. 2012.Applications of nanomaterials in agricultural production
and crop protection: A review. Crop Protection 35: 64–70.
Kidd, K.A. et al.2007. Collapse of a fish population after exposure to a synthetic
estrogen. Proceedings of the National Academy of Sciences104/2: 8897–8901.
Kolkwitz, R., M. Marsson.1909.Oekologie der tierischen Saprobien.
Internationa le Revue der gesamten Hydrobiologie 2: 126 –152.
Kortenkamp, A., T. Backhaus, M. Faust. 2009. State of the art report on mixture
toxicity.Final report.http://ec.europa.eu/environment/chemicals/pdf/
report_Mixture%20toxicity.pdf (accessed August 23,2012).
Kramer,V. J. et al. 2011. Adverse outcome pathways and ecological risk
assessment: Bridging to population-level effects. Environmental Toxicology
and Chemistry 30/1: 64–76.
Kuivila, K.M., M. L. Hladik. 2008.Understanding the occurrence and transport
of current-use pesticides in the San Francisco Estuary Watershed.
San Francisco Estuaryand Watershed Science 6/3:article 2. http://repositories.
cdlib.org/jmie/sfews/vol6/iss3/art2 (accessed August 18, 2012).
Langston, N. 2012.Rachel Carson’s legacy:Endocrine disrupting chemicals
and gender concerns. GAIA 21/3: 225 –229.
Liess, M., R.B. Schaefer, C.A. Schriever. 2008. The footprint of pesticide stress
in communities: Species traits reveal community effects of toxicants.
Science of the Total Environment 406/3: 484 – 490.
Martinovic, D., W. T. Hogarth, R. E. Jones, P. W. Sorensen. 2007. Environmental
estrogens suppress hormones, behavior, and reproductive fitness in male
fathead minnows. Environmental Toxicology and Chemistry 26/2: 271–278.
Mauch, C. 2012. Der Mensch als Gast der Borgias. Rachel Carsons Silent Spring
aus historischer Sicht. GAIA 21/3: 230 –231.
Meek, M.E., A. R.Boobis, K. M. Crofton, G. Heinemeyer, M.van Raaij, C.Vickers.
2011. Risk assessment of combined exposure to multiple chemicals: A WHO/
IPCS framework. Regulatory Toxicology and Pharmacology 60: S1– S14.
Newman, M. C., M.A. Unger. 2003. Fundamentals of ecotoxicology.
Boca Raton, FL: CRC Press.
Regulation (EC)No 1107 /2009. 2009. Regulation (EC)No 1107/2009 of the
Euro pean Parliament and of the Council of 21 October 2009 concerning the
placing of plant protection products on the market. Official Journal of the
Euro pean Union L 309: 1– 50.
Sandahl, J.F.,D.H. Baldwin,J.J. Jenkins, N.L. Scholz.2007.A sensory system
at the interface between urban stormwater runoff and salmon survival.
Environmental Science and Technology 41/8: 2998– 3004.
Scheringer,M. 2012. Umweltchemikalien 50 Jahre nach Silent Spring:
ein unge löstes Problem. GAIA 21/3: 210–216.
SETAC(Society of Environmental Toxicology and Chemistry). 2011. Summary
of the SETAC Pellston workshop on pesticide risk assessment for pollinators.
Pensacola, FL: SETAC.
Shugart, L. R.1995.Environmental genotoxicology. In: Fundamentals of aquatic
toxicology. Edited by G.M. Rand. Bristol,PA: Taylor and Francis.405– 419.
Stockholm Convention. 2004.Stockholm Convention on persistent organic
pollutants. www.pops.int (accessed August18,2012).
Sumpter, J.P. 2005. Endocrine disrupters in the aquatic environment:
An overview. Acta Hydrochimica Hydrobiologica 33/1: 9 – 16.
UNEP (United Nations Environment Programme). 2010. UNEP emerging
issues: Global honeybee colony disorder and other threats to insect pollinators.
Nairobi: UNEP.
UNEP, AMAP (Arctic Monitoring and Assessment Programme). 2011. Climate
change and POPs: Predicting the impacts.Report of the UNEP/AMAP expert
group. Geneva: Secretariat of the Stockholm Convention.
US DOI (U.S.Department of the Interior, Fish and Wildlife Service). 2009.
Endan gered and threatened wildlife and plants; removal of the brown
pelican (Pelecanus occidentalis)from the Federal List of Endangered and
Threatened Wildlife. Federal Register 74/220: 59444– 59472.
Van Aggelen,G. et al.2010.Integrating omic technologies into aquatic ecologi -
cal risk assessment and environmental monitoring: Hurdles, achievements,
and future outlook. Environmental Health Perspectives 118/1: 1 – 5.
Van der Oost,R., J.Beyer,N.P. E.Vermeulen.2003. Fish bioaccumulation and
biomarkers in environmental risk assessment: A review. Environmental
Toxicology and Pharmacology 13/2: 57 –149.
Vos, J.G. et al. 2000. Health effects of endocrine-disrupting chemicals on
wildlife, with special reference to the European situation.Critical Reviews
in Toxicology 30/1: 71–133.
Walker, C.H., S. P. Hopkin, R.M. Sibly, D.B. Peakall.2001.Principles of
ecotoxicol ogy. 2nd edition. London: Taylor and Francis.
Water Quality Act.1965.An Act to amend the Federal Water Pollution Control Act
to establish a Federal Water Pollution Control Administration, to provide grants
for research and development, to increase grants for construction of sewage
treatment works, to require establishment of water quality criteria, and for
other purposes. Public Law 89-234, October 2, 1965. United States Statutes
at Large 79: 903.
Weis, J.S., P. Weis.1995.Effects of embryonic exposure to methylmercury
on larval prey-capture ability in the mummichog, Fundulus heteroclitus.
Environ mental Toxicology and Chemistry 14/1: 153 – 156 .
Werner, I., K.Moran. 2008. Effects of pyrethroid insecticides on aquatic
organisms. In: Synthetic pyrethroids: Occurrence and behavior in aquatic
environ ments. Edited by J. Gan et al. American Chemical Society(ACS)
Symposium Series 991. Washington, D.C.: ACS. 310– 335.
Weston, D.P.,R.W. Holmes, J. You, M.J. Lydy.2005. Aquatic toxicity due to
residen tial use of pyrethroid insecticides. Environmental Science and
Technol ogy 39/24: 9778–9784.
WFD (Water Framework Directive). 2000. Directive 2000/60/EC of the European
Parliament and of the Council of 23 October 2000 establishing a framework
for Community action in the field of water policy.Official Journal of the
Europe an Union L 327: 1–73.
Wikipedia. 2011.Ecotoxicology. http:// en.wikipedia.org/wiki/Ecotoxicology
(accessed October 28, 2011).
Winston, M. L. 1999. Nature wars: People vs.pests. 3rd edition. Cambridge, MA:
Harvard University Press.
Submitted November 1, 2011; revised version
accepted July 16, 2012.
Inge Werner
Born 1957 in Bräunlingen, Germany. PhD 1995. 1996 to 2010
research in aquatic toxicology at the University of Califor nia
in Davis, USA. Since 2010 head of the Swiss Centre for
Applied Ecotoxicology located at Eawag, Dübendorf, and
the École Polytechnique Fédérale de Lausanne(EPFL).
Areas of expertise: biomarkers and detection of pollutant effects in aquatic
orga nisms, with emphasis on the sub-lethal effects of insecticides.
217_224_Werner 21.09.12 09:50 Seite 224