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part 1Remember as you read the article to reflect on these questions: (1) What is the main finding in the article? (2) How did the researchers determine their findings (i.e., what technique or experiment did they do…if any)? (3) What is a question you have about this article? and (4) How can you apply this research to improve your life or how does it benefit society?part2some opening thoughts that you have regarding the article
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Environ Sci Pollut Res (2015) 22:119–134
DOI 10.1007/s11356-014-3277-x
WORLDWIDE INTEGRATED ASSESSMENT OF THE IMPACT OF SYSTEMIC PESTICIDES ON BIODIVERSITY AND ECOSYSTEMS
Risks of large-scale use of systemic insecticides to ecosystem
functioning and services
Madeleine Chagnon & David Kreutzweiser & Edward A.D. Mitchell &
Christy A. Morrissey & Dominique A. Noome & Jeroen P. Van der Sluijs
Received: 29 April 2014 / Accepted: 1 July 2014 / Published online: 19 July 2014
# The Author(s) 2014. This article is published with open access at Springerlink.com
Abstract Large-scale use of the persistent and potent
neonicotinoid and fipronil insecticides has raised concerns
about risks to ecosystem functions provided by a wide range
of species and environments affected by these insecticides. The
concept of ecosystem services is widely used in decision making in the context of valuing the service potentials, benefits, and
use values that well-functioning ecosystems provide to humans
and the biosphere and, as an endpoint (value to be protected), in
ecological risk assessment of chemicals. Neonicotinoid insecticides are frequently detected in soil and water and are also
found in air, as dust particles during sowing of crops and
aerosols during spraying. These environmental media provide
essential resources to support biodiversity, but are known to be
threatened by long-term or repeated contamination by
neonicotinoids and fipronil. We review the state of knowledge
regarding the potential impacts of these insecticides on
ecosystem functioning and services provided by terrestrial
and aquatic ecosystems including soil and freshwater functions,
fisheries, biological pest control, and pollination services.
Empirical studies examining the specific impacts of
neonicotinoids and fipronil to ecosystem services have focused
largely on the negative impacts to beneficial insect species
(honeybees) and the impact on pollination service of food
crops. However, here we document broader evidence of the
effects on ecosystem functions regulating soil and water quality,
pest control, pollination, ecosystem resilience, and community
diversity. In particular, microbes, invertebrates, and fish play
critical roles as decomposers, pollinators, consumers, and predators, which collectively maintain healthy communities and
ecosystem integrity. Several examples in this review demonstrate evidence of the negative impacts of systemic insecticides
on decomposition, nutrient cycling, soil respiration, and
Responsible editor: Philippe Garrigues
M. Chagnon (*)
Département des sciences biologiques, Université du Québec à
Montréal, Case Postale 8888, Succursale Centre-Ville, Montréal,
Québec H3C 3P8, Canada
e-mail: [email protected]
D. A. Noome
Task Force on Systemic Pesticides, 46, Pertuis-du-Sault,
2000 Neuchâtel, Switzerland
D. Kreutzweiser
Canadian Forest Service, Natural Resources Canada, 1219 Queen St.
East, Sault Ste. Marie, Ontario P6A 2E5, Canada
D. A. Noome
Kasungu National Park, c/o Lifupa Conservation Lodge,
Private Bag 151, Lilongwe, Malawi
E. A. Mitchell
Laboratory of Soil Biology, University of Neuchâtel,
Rue Emile Argand 11, 2000 Neuchâtel, Switzerland
E. A. Mitchell
Jardin Botanique de Neuchâtel, Chemin du Perthuis-du-Sault 58,
2000 Neuchâtel, Switzerland
C. A. Morrissey
Department of Biology and School of Environment and
Sustainability, University of Saskatchewan, 112 Science Place,
Saskatoon, Saskatchewan S7N 5E2, Canada
J. P. Van der Sluijs
Environmental Sciences, Utrecht University, Heidelberglaan 2,
3584 CS Utrecht, The Netherlands
J. P. Van der Sluijs
Centre for the Study of the Sciences and the Humanities, University
of Bergen, Postboks 7805, N-5020 Bergen, Norway
120
invertebrate populations valued by humans. Invertebrates, particularly earthworms that are important for soil processes, wild
and domestic insect pollinators which are important for plant
and crop production, and several freshwater taxa which are
involved in aquatic nutrient cycling, were all found to be highly
susceptible to lethal and sublethal effects of neonicotinoids and/
or fipronil at environmentally relevant concentrations. By contrast, most microbes and fish do not appear to be as sensitive
under normal exposure scenarios, though the effects on fish
may be important in certain realms such as combined fish-rice
farming systems and through food chain effects. We highlight
the economic and cultural concerns around agriculture and
aquaculture production and the role these insecticides may have
in threatening food security. Overall, we recommend improved
sustainable agricultural practices that restrict systemic insecticide use to maintain and support several ecosystem services
that humans fundamentally depend on.
Environ Sci Pollut Res (2015) 22:119–134
(e.g., climate control, detoxification, water purification, pollination, seed dispersal, pest and disease regulation, herbivory, and weed control), supporting services (e.g., soil formation, nutrient cycling, pollination, soil quality, food
web support, waste treatment, and remediation), and cultural services (e.g., recreation, esthetic, or spiritual value).
The wide application of neonicotinoid systemic pesticides,
their persistence in soil and water, and potential for uptake by
crops and wild plants expose a wide range of species, which
are important in providing valuable ecosystem services. This
paper addresses the risks to ecosystem functioning and services from the growing use of systemic neonicotinoid and
fipronil insecticides used in agricultural and urban settings.
Here, we focus on ecosystem services provided by terrestrial
soil ecosystem functions, freshwater ecosystem functions,
fisheries, biological pest control, and pollination, in addition
to reviewing the overall threats of these systemic insecticides
to food security.
Keywords Ecosystem services . Soil ecosystem .
Neonicotinoids . Pollinators . Freshwater . Rice paddies
Terrestrial soil ecosystem functions
Introduction
Soil ecosystem services and biodiversity
Other papers in this special issue have shown that neonicotinoid
insecticides and fipronil are presently used on a very large scale
(e.g., Simon-Delso et al. 2014, this issue) and are highly persistent, and repeated application can lead to buildup of environmental concentrations in soils. They have high runoff and leaching
potential to surface and groundwaters and have been detected
frequently in the global environment (Bonmatin et al. 2014, this
issue). Evidence is mounting that they have direct and indirect
impacts at field realistic environmental concentrations on a wide
range of nontarget species, mainly invertebrates (Pisa et al. 2014,
this issue) but also on vertebrates (Gibbons et al. 2014, this
issue). Although studies directly assessing impacts to ecosystem
functions and services are limited, here we review the present
state of knowledge on the potential risks posed by neonicotinoids
and fipronil.
The concept of ecosystem services is widely used in decision
making in the context of valuing the service potentials, benefits,
and use values that well-functioning ecosystems provide to
humans and the biosphere (Spangenberg et al. 2014a, b).
Ecosystem services were initially defined as “benefits people
obtain from ecosystems” as popularized by the United Nations
Environment Program (UNEP 2003) and the Millennium
Ecosystem Assessment (MEA 2003, 2005). They are seen as
critical to the functioning of the Earth’s life support system,
which consists of habitats, ecological systems, and processes that
provide services that contribute to human welfare (Costanza
et al. 1997). Under the MEA framework (among others),
ecosystem services have been categorized into provisioning services (e.g., food, wood, fiber, clean water), regulating services
Terrestrial ecosystems are known to provide a complex range of
essential ecosystem services involving both physical and biological processes regulated by soils. Soils support physical processes
related to water quality and availability such as soil structure and
composition (e.g., porosity) to facilitate movement of water to
plants, to groundwater aquifers, and to surface water supplies.
Water quality is improved by filtration through clean soils that
can remove contaminants and fine sediments. As water flows
through soils, it interacts with various soil matrices absorbing and
transporting dissolved and particulate materials including nutrients and other life-supporting elements to plants and microorganisms. Soils further provide stream flow regulation and flood
control by absorbing and releasing excess water.
Many of the soil ecosystem services are biologically mediated, including regulation and cycling of water and nutrients, the
facilitation of nutrient transfer and translocation, the renewal of
nutrients through organic and waste matter breakdown, elemental transformations, soil formation processes, and the retention
and delivery of nutrients to plants (Swift et al. 2004; Dominati
et al. 2010; Robinson et al. 2013). Plants, in turn, provide food,
wood, and fiber to support human infrastructure and natural
habitats, while improving soil retention and erosion control.
Over the long term, they also provide raw materials for consumption such as peat for fuel and horticultural substrates and
ornamental plants and flowers for decoration. Further services
include the biological control of pests and diseases through
provision of soil conditions and habitats for beneficial species
and natural enemies of pests, the sequestration and storage of
carbon through plant growth and biomass retention, and the
Environ Sci Pollut Res (2015) 22:119–134
detoxification of contaminants through sorption, immobilization,
and degradation processes.
Many of the biologically mediated soil ecosystem services
listed above require the inputs and activities of interacting diverse
and functional biological communities (Swift et al. 2004;
Lavelle et al. 2006; Barrios 2007). Biodiversity conservation
itself can be considered as an important ecosystem service (Dale
and Polasky 2007; Eigenbrod et al. 2010), following on the
earlier concept that biodiversity serves as a form of insurance
against the loss of certain species and their ecological function
through species redundancy (Naeem and Li 1997; Yachi and
Loreau 1999). Biodiversity has been shown to be positively
related to ecological functions that support ecological services
(Benayas et al. 2009). The stability of soil ecosystems has been
linked to biodiversity and especially the relative abundances of
keystone species or functional groups that underpin the soil food
web structure or that facilitate specialized soil processes (de
Ruiter et al. 1995; Brussaard et al. 2007; Nielsen et al. 2011).
Natural soils are a reservoir of diverse and complex biological
communities. Organisms range from body sizes in millimeters
(macrofauna, macroflora) to cell or body sizes in micrometers
(mesofauna, microfauna, microflora). Key taxa include
macroarthropods (e.g., ground beetles, ants, termites), earthworms, mites, collembolans, protozoans, nematodes, bacteria,
and fungi. The activity of these biota and interactions among
them condition ecosystem processes on which many ecosystem
services depend (Barrios 2007). For example, earthworms have a
large impact on organic matter dynamics, nutrient cycling, and
soil properties. Earthworms break down plant litter into nutrientrich organic matter for other consumers and contribute to the
mixing of organic matter in soils. They produce casts, mucilages,
and other nutrient-rich excretions that contribute to soil fertility
and biogeochemical cycling (Beare et al. 1995). Their burrowing
activity increases soil porosity and aeration, facilitates water and
nutrient transfer, and reduces soil compaction (Edwards and
Bohlen 1996). While earthworms play a key role in soil organic
matter dynamics, the decomposition and mineralization of organic matter is a complex process that is facilitated by the
activities and interactions among diverse biotic communities
including other invertebrates, protists, bacteria, and fungi (Swift
et al. 2004). These biota-mediated soil processes occur at a scale
of centimeters to decimeters by individuals and populations, and
the accumulation of these processes over space and time creates a
continuous process from which soil properties and services arise
to local and regional landscape scales (Lavelle et al. 2006).
A further example of ecosystem services is the biologically
mediated nitrogen cycling in soils. Nitrogen (N) is essential for
plant growth, and plants convey many of the services derived
from soils. Macro- and meso-invertebrates initiate decomposition of soil organic matter by fragmentation, ingestion, and
excretion to release organic N which is subsequently mineralized by highly specialized microbial groups to plant-available
forms of inorganic N. Available N pools in soils are also greatly
121
enhanced by nitrogen-fixing microorganisms that convert atmosphere N to plant-available N through root nodule symbioses in plants, especially legumes. Inorganic N can also be taken
up by soil microbes, assimilated into biomass, and incorporated
into the soil organic N pool (immobilization), which is available
for further cycling (Brady and Weil 1996; Brussaard et al.
1997; Barrios 2007). The excess of N is a major cause of soil
and water eutrophication with consequences on biodiversity
(Vitousek et al. 1997), and therefore, loss of N through denitrification is a another valuable ecosystem service provided by
wetlands and floodplain forest soils (Shrestha et al. 2012).
Impacts of neonicotinoid insecticides on soil ecosystem
services
Given that many of the ecosystem services of soils are biologically mediated, and pesticides can cause depletion or
disruption of nontarget biotic communities in soils, it follows
that pesticides can pose risks to soil ecosystem processes and
services. Effects of pesticides in soils can range from direct
acute and chronic toxicity in organisms to many sublethal or
indirect effects on behavior, functional roles, predator-prey
relationships, and food web dynamics. Any or all of these
can occur at the organism, population, or community levels
and, therefore, may impact soil biodiversity or ecosystem
stability (Edwards 2002). Since soil biodiversity is related to
ecological functions that support ecological services (Benayas
et al. 2009), pesticide-induced disruptions to biodiversity and
ecological function could impair ecosystem services derived
from soils (Goulson 2013). Impacts on soil biodiversity and
their implications for ecosystem function have been demonstrated for other pesticides affecting microbial (Johnsen et al.
2001) and invertebrate (Jansch et al. 2006) communities, and
the same risks are likely to arise from neonicotinoid insecticides in soils. Neonicotinoids can persist in soils for several
years (Goulson 2013; Bonmatin et al. 2014, this issue) and
can cause significant adverse effects on key soil organisms at
environmentally realistic concentrations (Pisa et al. 2014, this
issue) and, therefore, have the potential to pose a risk to soil
ecosystem services.
While the link between adverse effects on organisms and
ecological function or services in soils is theoretically sound,
empirical evidence of effects on soil ecosystem services from
neonicotinoid insecticides is sparse, partly because its largescale use started only a decade ago. In our review of the
literature, we found only a few studies that reported the effects
of neonicotinoids on soil organism function with implications
for ecosystem services. Peck (2009a, b) assessed the impacts
of the neonicotinoid, imidacloprid, applied to turfgrass for
scarab beetle control and found direct and indirect long-term
effects on some arthropods and suggested negative implications (although not empirically tested) for soil nutrient cycling
and natural regulation of pests. In laboratory microcosms,
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Kreutzweiser et al. (2008a, 2009) tested the effects of
imidacloprid in the leaves from systemically treated trees on
the breakdown of autumn-shed leaves by litter dwelling earthworms over a 35-day exposure period. At realistic field concentrations, the leaf-borne residues of imidacloprid were not
directly toxic to earthworms, but did cause feeding inhibition
that resulted in a significant reduction in leaf litter breakdown.
They further demonstrated that this effect was due to sublethal
toxic effects, not avoidance behavior (Kreutzweiser et al.
2009). When imidacloprid was added directly to terrestrial
microcosms to simulate a soil injection method for treating trees,
a similar effect was detected with significantly reduced breakdown of leaf litter by earthworms at ambient litter concentrations
of 7 mg/kg and higher (Kreutzweiser et al. 2008b). Taken
together, these studies demonstrated that when imidacloprid is
applied as a systemic insecticide for the control of wood-boring
insects in trees, residual imidacloprid in autumn-shed leaves
poses risk of reduced leaf litter breakdown through a feeding
inhibition effect on earthworms, and this has negative implications for organic matter dynamics in soils. A similar effect would
presumably occur in the breakdown of other imidaclopridbearing plant litter in other soils, including agricultural but, to
our knowledge, this has not been tested directly. Other effects of
neonicotinoids on earthworm behavior that may further influence ecological processes in soils (e.g., burrowing behavior) are
reviewed in Pisa et al. (2014, this issue).
Soil microbial communities have also been affected by
imidacloprid, which can affect leaf litter decomposition.
Although imidacloprid did not inhibit microbial decomposition
of autumn-shed leaves of ash trees (Fraxinus spp.)
(Kreutzweiser et al. 2008b), microbial decomposition of leaves
from maple (Acer saccharum) trees was significantly inhibited
at concentrations expected from systemic treatments to control
wood-boring insects (Kreutzweiser et al. 2008a). The authors
offer suggestions for observed differences in effects among tree
species. Regardless of differences between studies, the data
indicate that imidacloprid residues in leaf material have the
potential to interfere with microbial decomposition of leaf litter,
with implications for organic matter breakdown and nutrient
cycling.
Others have assessed the effects of imidacloprid on microbial
activity in agricultural soils after treated seed applications. Singh
and Singh (2005a) measured microbial enzyme activity as an
indicator of population level effects and found that imidacloprid
in soils after seed treatment had stimulatory effects on microbial
enzyme activity for up to 60 days. In the same set of experiments,
they also measured available N in soils and reported increased
available N (Singh and Singh 2005b). In a further study at the
same site, Singh and Singh (2006) found increased nitrate-N but
decreased ammonium, nitrite-N, and nitrate reductase enzyme
activity in soils in which imidacloprid-coated seeds had been
planted. Tu (1995) added imidacloprid to sandy soils and reported decreased fungal abundance and short-term decreases in
Environ Sci Pollut Res (2015) 22:119–134
phosphatase activity but no measurable effects on nitrification
or denitrification rates. Ingram et al. (2005) reported no inhibition of microbial urease activity by imidacloprid in turfgrass soil
or sod. Similarly, Jaffer-Mohiddin et al. (2010) found no
inhibition, and some stimulation, of amylase and cellulase
activity in soils under laboratory conditions. Ahemad and Khan
(2012) measured decreased activity and plant growth promoting
traits of a N-fixing bacterium, Rhizobium sp., isolated from pea
nodules of plants exposed to imidacloprid in soils, but only at
three times the recommended application rate (no significant
effects at the recommended rate). Overall, these studies demonstrate that neonicotinoids can induce measurable changes in soil
microbial activity but the effects are often stimulatory, short-term,
and of little or no measurable consequence to soil nutrient
cycling. The reported microbial responses have been attributed
to inductive adaptation as microbes assimilate or mineralize
components of the imidacloprid molecule (Singh and Singh
2005a), essentially a biodegradation process (Anhalt et al.
2007; Liu et al. 2011; Zhou et al. 2013; Wang et al. 2013).
By contrast, at least two other studies have reported adverse
or negative effects of neonicotinoids on soil microbial
communities and their function. Yao et al. (2006) reported
significantly inhibited soil respiration at field realistic concentrations of acetamiprid. Cycon et al. (2013) found measurable
changes in soil community structure and diversity, and that
these were generally found in conjunction with reduced soil
metabolic activity at or near realistic field rates of
imidacloprid. It is possible that community level changes
associated with the neonicotinoid exposure may facilitate the
adaptive responses in functional parameters listed above.
Conclusions on soils as ecosystem services
Given that many soil ecosystem services are dependent on soil
organisms, that neonicotinoid insecticides often occur and can
persist in soils, and that their residues pose a risk of harm to
several key soil invertebrates, neonicotinoids have the potential
to cause adverse effects on ecosystem services of soils. From a
theoretical perspective and based on findings from studies of
better-studied pesticides, the potential for neonicotinoid impacts on soil ecosystem services appears to be high but there
are few empirical studies that have tested these effects. From
the few studies available, it appears that invertebrate-mediated
soil processes are at greater risk of adverse effects from
neonicotinoid residues than are microbial-mediated processes.
One issue that remains elusive is the degree to which soil
biological communities can absorb pesticide impacts before
ecosystem function, and ultimately, the delivery of services is
measurably impaired at a local or regional scale. Studies are
conflicting with regard to the degree of functional redundancy
and resilience inherent in soil and other biological communities
that are rich in diversity. Swift et al. (2004) review the impacts
of agricultural practices, including the use of pesticides, on the
Environ Sci Pollut Res (2015) 22:119–134
relationship between biodiversity and ecosystem function and
show that some changes in biological communities can be
harmful to ecosystem function while others are functionally
neutral. They suggest that microbial communities have a high
degree of functional redundancy and resilience to impacts on
their functional role in soil organic matter processing. On the
other hand, reductions in highly specialized taxa with unique or
critical roles in an important ecosystem function such as decomposition and nutrient cycling can measurably impact the
delivery of ecosystem services (Barrios 2007). Earthworms
could be categorized as such, and since adverse effects on
earthworms have been reported at realistic concentrations of
neonicotinoids in soils and leaf litter, this provides reasonable
evidence that some soil ecosystem services can be impaired by
the use of neonicotinoid insecticides. Further empirical studies
coupled with ecological modeling to test the likelihood and
extent of these effects are warranted.
Freshwater ecosystem functions
Nutrient cycling and water quality
Pollution by pesticides is widely recognized to be a major
threat to freshwater ecosystems worldwide (Gleick et al.
2001; MEA 2005). Freshwater ecosystems provide an important array of ecosystem services, ranging from clean drinking
water and irrigation water to industrial water, water storage,
water recreation, and an environment for organisms that
support fish and other important foods. Invertebrates make
up a large proportion of the biodiversity in freshwater food
chains and are a critical link for transfer of energy and
nutrients from primary producers to higher trophic levels
both in the aquatic and terrestrial ecosystems. Thus,
alteration of invertebrate abundance, physiology, and life
history by insecticides can have a serious impact on services
provided by freshwater ecosystems. Equally, their role in
decomposition of organic matter and nutrient cycling offers
an essential purification service of water used for human
consumption or to support aquatic life.
Peters et al. (2013) conducted a review of the effect of
toxicants on freshwater ecosystem functions, namely leaf litter
breakdown, primary production, and community respiration.
For the review, 46 studies met their empirical specifications
(for example, effect size and control treatment available). An
important outcome of their review is that in over a third of the
observations, reduction in ecosystem functions was occurring
at concentrations below the lower limits set by regulatory
bodies to protect these ecosystems. These lower limits were
often set using LC50 values for common test species like
Daphnia magna, with risk assessment procedures not including more sensitive species or consideration of species that
have critical roles in maintaining ecosystem function. A key
123
shortcoming of the review of Peters et al. (2013) is
that a large number of the included studies involved
effects of organophosphates, pyrethroids, and carbamates,
but no information is given for the newer insecticide classes
such as neonicotinoids or fipronil.
Relatively few studies have formally tested the effects of
neonicotinoids or fipronil on ecosystem services in freshwater
systems. A recent study by Agatz et al. (2014) did consider
the effect of the neonicotinoid, imidacloprid, on the feeding
activity of Gammarus pulex, a common freshwater amphipod
that plays an important role in leaf litter breakdown.
Prolonged inhibition of feeding after exposure was found at
concentrations of imidacloprid (0.8 to 30 μg/L) that are within
the range of those measured in several aquatic environments.
Reduced leaf feeding and altered predator-prey interactions of
a similar shredder species, Gammarus fossarum, have been
reported at thiacloprid concentrations of 1–4 μg/L (Englert
et al. 2012). Similar findings have been shown for other
shredder species, stonefly (Pternonarcyidae) and crane fly
(Tipulidae) larvae, exposed to imidacloprid in leaves and in
water exhibiting mortality at 130 μg/L and feeding inhibition
at 12 μg/L when applied directly to water but were more
tolerant when exposed through the leaves (Kreutzweiser
et al. 2008a). In a second study, the authors were able to
determine that the effects on feeding inhibition were important
in reducing leaf litter decomposition rates at concentrations of
18 to 30 μg/L (Kreutzweiser et al. 2009).
Prolonged exposure, or exposure to multiple compounds,
might affect this and other shredder populations. Although not
widely measured, inhibition of this functional feeding group
has the potential to negatively affect the conversion of coarse
terrestrial material into fine particulates that can be more
readily consumed by other species. This in turn is expected
to alter the aquatic invertebrate community, decomposition
rates, and nutrient cycling, ultimately influencing water quality and the support of biodiversity which is an important
ecosystem service. It should be noted that G. pulex is more
sensitive to imidacloprid than Daphnia species and that both
are crustacea and not insects. Several insects tend to be much
more sensitive than G. pulex to imidacloprid so the risk to
decomposition processes might be larger than has been
assessed by studies with G. pulex, depending on the affected
species role in the function of ecosystems and the amount of
functional redundancy in the community (Beketov and Liess
2008; Ashauer et al. 2011).
Aquatic food chain effects
Ecosystem services related to decomposition and nutrient
cycling are important for water quality; however, there is an
additional concern for potential indirect effects of insecticides
in reducing important invertebrate prey. This may be critical
for many freshwater species that are valued for food (e.g., fish
124
and crayfish) and for ecological reasons (amphibians and
aquatic birds). While rarely studied, indirect food chain effects
have been reported in freshwater systems. For example,
Hayasaka et al. (2012a) performed an experimental rice paddy
mesocosm study using the systemic insecticides imidacloprid
and fipronil, applied at recommended rates. Zooplankton, benthic, and neuston communities in the imidacloprid-treated field
had significantly lower species abundance than those from control. Hayasaka et al. (2012a, b) further found that two annual
applications of imidacloprid and fipronil were important in reducing benthic arthropod prey which led to reductions in growth
of medaka fish (Oryzias latipes). Sánchez-Bayo and Goka (2005,
2006) also studied the ecological changes in experimental
paddies treated with imidacloprid throughout a cultivation period. A total of 88 species were observed, with 54 of them aquatic.
They reported plankton, neuston, benthic, and terrestrial communities from imidacloprid-treated fields had significantly lower
abundance of organisms compared with control. Our knowledge
about how aquatic communities react to, and recover from,
pesticides, particularly in relation to the water residues, is deficient (Sánchez-Bayo and Goka 2005, 2006).
While not conclusively proven, many of the insectivorous
bird species declines are also coincident with agricultural areas
using these pesticides and speculation about recent population
declines through reductions in emergent invertebrate prey from
insecticide use seems plausible given the correlative evidence
(Benton et al. 2002; Boatman et al. 2004; Mason et al. 2012).
Neonicotinoids are the latest generation of pesticides that have
the ability to enter freshwater bodies and negatively affect
invertebrate populations which in turn can reduce emergent
insects that numerous water-dependent birds and other wildlife
depend on. A recent study by Hallmann et al. (2014) is the first
to demonstrate the potential cascading effect of low
neonicotinoid concentrations in water to insectivorous birds.
Future studies should consider the importance of pesticide
effects at the community level considering the intricate interaction among species in the trophic chain and the indirect effects
on species deemed important for human consumption, recreation, or esthetic value.
Conclusions on freshwater ecosystem functions
Many aquatic species are directly exposed to neonicotinoid
and fipronil insecticides in water, often over prolonged periods. Data from long-term and large-scale field monitoring by
Van Dijk et al. (2013) have demonstrated the negative effects
of imidacloprid on invertebrate life. Such negative impacts
have the potential to adversely alter the base of the aquatic
food web given that this group is a critical link for the transfer
of nutrients and energy from primary producers to consumers.
Reductions in survival, growth, and reproduction of freshwater organisms, particularly aquatic insects and crustaceans, can
alter ecosystem functions related to decomposition and
Environ Sci Pollut Res (2015) 22:119–134
nutrient cycling. These processes are central to providing
ecosystem services such as clean freshwater and the support
of biodiversity. Equally important are the effects on the trophic
structure, which can influence the stability, resilience, and
food web dynamics in aquatic ecosystems, but also terrestrial
ecosystems given that many aquatic insects have adult life
stages out of the water.
Fisheries and aquaculture
Sustainably managed fisheries and aquaculture can offer solutions to a growing demand for aquatic animal protein
sources. In Africa, Asia, and Latin America, freshwater inland
fisheries are providing food to tens of millions of people
(Dugan et al. 2010) while ensuring employment, especially
to women (BNP 2008). Pesticide use could hamper the successful expansion of global fisheries as well as small-scale
inland fisheries, aquaculture, and combined rice-fish farming
systems, if those pesticides are negatively affecting fisheries.
Neonicotinoid use has been increasing in fish farming and
aquaculture environments because of their relatively low acute
toxicity to fish and their effectiveness against sucking parasites and pests. For example, imidacloprid (neonicotinoid) is
replacing older pesticides, such as pyrethroids to control rice
water weevil (Lissorhoptrus oryzophilus Kuscel) infestations
in rice-crayfish (Procambarus
