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Side Effect of Synthetic Pesticides on Spiders

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Spiders that occur in agroecosystems are often heavily affected by pesticide applications. Insecticides and acaricides, when applied at the recommended concentration and dose, usually cause acute toxicity, while herbicides and fungicides are relatively harmless. Direct toxicity has been studied in a number of spider species with respect to a number of different formulations, though not as many as in other natural enemies. With the advent of selective pesticides, recent studies focus on their sublethal effects. These have so far been studied in 21 species of spiders using 26 formulations (acaricides, insecticides, fungicides, herbicides). Sublethal doses affect a number of life-history traits: movement, dispersal, predation rate, web building, mating, oviposition, fecundity, ontogenetic development, defence, and physiological processes such as enzymatic activities and water loss. Examples of each of these effects are presented. The most frequent evidence of sublethal effects has been gathered for prey consumption. There is also some, though limited, evidence for hormesis or improved performance. Future toxicology research should be concentrated more on sublethal effects and the development of a uniform protocol for sublethal toxicity assessment.
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Chapter 31
Side Effect of Synthetic Pesticides on Spiders
Stano Peka
´r
31.1 Introduction
Spiders are natural enemies occurring in many agroecosystems. Indeed, they are
often the most abundant and diversified natural enemies, which contribute to the
reduction of several pests. However, certain pest management practices, such as the
application of pesticides, can disrupt their role in pest control. There are a number
of different synthetic insecticide and acaricide classes with varying effects on the
nontarget arthropods. Most synthetic insecticides such as organophosphates,
cyclodienes, pyrethroids, carbamates, and organochlorines are neurotoxic and
have a highly negative effect. A few are insect growth regulators, antifeedants, or
microbial pesticides, which are usually less detrimental, at least in terms of acute
toxicity. Unexpectedly, even herbicides and fungicides or their additives can have
serious detrimental effects.
Research on the ecotoxicology of spiders has received rather limited attention in
comparison with other natural enemies, for example, parasitoids (Theiling and
Croft 1988). Early papers investigated the side effects of pesticides in the field by
focusing on the abundance of the spider population and species richness of the
community. Later toxicological studies mainly evaluated the direct toxicity, specif-
ically mortality at different pesticide concentrations and/or doses, with a main
emphasis on the concentration/dose recommended for pest control. Formulations
that caused low mortality were considered harmless and recommended for use.
However, such acute toxicity tests did not consider side effects on other life-history
traits, such as foraging, defence, mating, or migration, which may severely impair
spider pest control abilities. Recent research, therefore, focuses more on the
mechanisms behind the intoxication of surviving individuals and, in particular, on
so-called sublethal effects.
S. Peka
´r(*)
Department of Botany and Zoology, Masaryk University, Brno, Czech Republic
e-mail: pekar@sci.muni.cz
W. Nentwig (ed.), Spider Ecophysiology,
DOI 10.1007/978-3-642-33989-9_31, #Springer-Verlag Berlin Heidelberg 2013
415
The type of effect is a function of the concentration and/or dose (Fig. 31.1). At
relatively high concentrations/doses, contact with a formulation causes high mor-
tality. This is known as a direct effect. At concentrations/doses lower than LC
50
(i.e., lethal concentration) or LD
50
(i.e., lethal dose)—that is, concentration/dose at
which more than 50 % of individuals survive—sublethal effects are observed.
These are evaluated as behavioural or physiological changes in an individual that
survived exposure to a pesticide. Yet even lower concentrations/doses may have a
stimulating effect on behavioural and physiological functions. Such effects are
called hormesis. Very low concentrations or doses have negligible or no effect.
For example, contact with herbicide did not affect the walking activity of two
lycosid species, Pardosa milvina and Hogna helluo (Evans et al. 2010), or court-
ship, mating, prey capture, or escape from predators in another lycosid Pardosa
palustris (Michalkova
´and Peka
´r2009). The application of carbamate did not alter
web structure in an araneid Larinioides sclopetarius (Lengwiler and Benz 1994).
Oviposition and fecundity did not decrease in the lycosid Pirata piratoides after
insect growth regulator application (Deng et al. 2008). Rate of development was not
extended in the lycosid Pardosa amentata after contact with pyrethroid and organ-
ophosphate (Toft and Jensen 1998). Diacylhydrazine did not affect the functional
response in the philodromid Philodromus cespitum (R
ˇeza
´c
ˇet al. 2010).
31.2 Direct Effect
Mortality resulting from contact with a pesticide, administered topically, orally, or
via residues, differs among pesticides, formulations, spider species, developmental
stage, and sex and is also influenced by current abiotic and biotic conditions. In
general, highest mortality was caused by standard doses of insecticides and
Concentration / Dose
No effect
Hormesis
Sublethal effect Direct effect
1.0
0.5
0
Probability of mortality
LC/LD 50
Fig. 31.1 Logit response
curve of mortality showing
the variety of effects in
relation to the concentration
or dose (LC or LD
50
)
416 S. Peka
´r
acaricides and lowest mortality by fungicides and herbicides (Theiling and Croft
1988). The causes of mortality differ among pesticide classes. Little is known of
their effect in spiders. Neurotoxic formulations, such as type I pyrethroids, have a
quick knockdown effect. The symptoms of type II pyrethroids include ataxia,
convulsions, contractions, and paralysis. Mortality is caused secondarily through
disturbing the water balance. Besides the effect on neurotransmitters,
organophosphates tend to accumulate in cell membranes and modify their perme-
ability. It has been shown in the sparassid Polybetes pythagoricus that contact with
organophosphate altered the lipid dynamics and caused diminished capacity for
oxygen binding (Cunningham et al. 2002). Pyrethroids can further cause dysfunc-
tion in myocardial cells and alter heart rate (Desneux et al. 2007).
31.3 Sublethal Effects
Sublethal effects have been studied in 21 species of spiders using 26 formulations
(Table 31.1). The frequency of encountering sublethal concentrations/doses for
spiders in the field is assumed to be higher than that of lethal doses. Due to the
enhanced stability of synthetic pyrethroids in the environment, spiders may contact
sublethal doses for several days after spraying (Baatrup and Bayley 1993). Sublethal
doses also occur when the pesticide is diluted in water (such as dew) or because of the
filter effect of plants or spray drift, which give rise to surfaces with sparse contami-
nation. Such situations are frequent in many types of crops. A further situation arises
because of webs. Three-dimensional webs of theridiid and dictynid spiders can
reduce contact of the resident spider with pesticide droplets (Peka
´r1999).
Different classes of pesticides can cause different sublethal effects. These effects of
intoxication interact with numerous life-history traits and can be measured by
investigating changes in physiology and behaviour. Behavioural responses often reflect
changes at the physiological level. Activities such as movement, prey capture, repro-
duction, development, and defence are highly sophisticated, governed by complex
neural interactions, and particularly disrupted by neurotoxic formulations. However, in
contrast to direct effects, recovery from sublethal effects is possible over several days.
For example, P. amentata recovered in 3–4 days (Baatrup and Bayley 1993).
31.3.1 Enzymatic Activity
Pesticides can have a dramatic effect on many physiological processes. Organopho-
sphorous and carbamate compounds inhibit cholinesterases, enzymes in the central
nervous system, as has been shown for the lycosid Anoteropsis hilaris following
organophosphates application (Van Erp et al. 2002) and the linyphiid Hylyphantes
graminicola following both organophosphate and pyrethroid applications (Peng
et al. 2010). In the latter species, reduced activity of cholinesterases pertained even
to offspring.
31 Side Effect of Synthetic Pesticides on Spiders 417
Table 31.1 List of spider species and synthetic formulations that have been used to evaluate sublethal effects
Family/species Insecticide (acaricide) Fungicide Herbicide Reference
Araneidae –
Alpaida veniliae Glyphosate Benamu
´et al. (2010)
Araneus
diadematus
Cypermethrin, paraffin oil Prochloraz,
triadimenol
Samu and Vollrath (1992)
Larinioides
sclopetarius
Deltamethrin, diazinon, dicofol, pirimicarb Lengwiler and Benz (1994)
Neoscona
pratensis
Endosulfan, spinosad Benamu
´et al. (2007)
Linyphiidae –
Erigone atra Fenvalerate Dinter et al. (1998)
Frontinella
communis
Malathion Tietjen and Cady (2007)
Hylyphantes
graminicola
Dimethoate, fenvalerate, methamidophos Deng et al. (2006,2007) and Peng et al. (2010)
Oedothorax
apicatus
Deltamethrin, fenvalerate Everts et al. (1991), Jagers op Akkerhuis et al.
(1995;1997) and Dinter et al. (1998)
Tenuiphantes
tenuis
Cypermethrin Shaw et al. (2005)
Lycosidae –
Anoteropsis
hilaris
Chlorpyrifos, diazinon Van Erp et al. (2002)
Pardosa
amentata
Cypermethrin, dimethoate, l-cyhalothrin Baatrup and Bayley (1993), Toft and Jensen
(1998), Nielsen et al. (1999) and Shaw et al.
(2006)
Pardosa milvina Glyphosate Evans et al. (2010) and Wrinn et al. (2012)
Pardosa palustris Chlorpyrifos + cypermethrin, deltamethrin Clomazone,
glyphosate
Peka
´r and Benes
ˇ(2008) and Michalkova
´and
Peka
´r(2009)
Pardosa
pseudoannulata
Imidacloprid, methamidophos Widiarta et al. (2001) and Wang et al. (2006a,
b)
Pardosa
prativaga
Dimethoate Pedersen et al. (2002)
418 S. Peka
´r
Pirata piratoides Buprofezin Deng et al. (2008)
Rabidosa rabida Malathion Tietjen (2006) and Tietjen and Cady (2007)
Schizocosa
ocreata
Malathion Tietjen and Cady (2007)
Philodromidae –
Philodromus
cespitum
Acetamiprid, azadirachtin,
chlorpyrifos + cypermethrin, deltamethrin,
diflubenzuron, methoxyfenozide, spinosad
Clomazone Peka
´r and Benes
ˇ(2008) and R
ˇeza
´c
ˇet al. (2010)
Salticidae –
Salticus scenicus Malathion Tietjen and Cady (2007)
Sparassidae –
Polybetes
pythagoricus
Fenitrothion Cunningham et al. (2002)
31 Side Effect of Synthetic Pesticides on Spiders 419
Acetylcholinesterase is an enzyme decomposing the neurotransmitter acetylcho-
line. Inhibition of acetylcholinesterase would lead to hyperactivity and general
perturbation in all systems. This can result in death. Spiders can resist neurotoxic
effects by producing detoxification enzymes, such as glutathione S-transferase and
glutathione peroxidase. The absence or low activities of detoxification enzymes
increase their susceptibility. In Pardosa amentata Nielsen et al. (1999) found that
detoxification enzymes are present in the bodies of spiders throughout the year. The
activity of glutathione S-transferase was affected only slightly by pyrethroid appli-
cation, while the activity of glutathione peroxidase was strongly induced. Similarly,
in another study, glutathione S-transferase was not induced by an organopho-
sphorous formulation applied on Anoteropsis hilaris (Van Erp et al. 2002). Gluta-
thione peroxidase, unlike glutathione S-transferase, is thus considered an important
system used to combat unpredictable exposure to toxins. Alternatively, resistance to
intoxication can be achieved by the overproduction of acetylcholinesterase, which
was found to be affected by the nutritional state of spiders. Pedersen et al. (2002)
found a strong synergistic effect of nutrition on the regenerative ability of acetyl-
cholinesterase after organophosphate application in the lycosid Pardosa prativaga.
Not only enzymes in the nervous system were found to be affected by pesticides.
Wang et al. (2006a) reported the inhibition of protease activity in the gut of spiders
following application of a high dose of an organophosphate on the lycosid Pardosa
pseudoannulata.
31.3.2 Water Loss
It is known that contact with neurotoxic formulations (organophosphorous, carba-
mate, cyclodiene, and pyrethroid) causes accelerated water loss (Everts et al. 1991),
which can lead to mortality, as has been observed in the linyphiid Oedothorax
apicatus (Jagers op Akkerhuis et al. 1997). Using this species as a model, the
following scenario has been predicted. Contact with pyrethroid will cause abnormal
signalling intensity of the humidity in the cuticle. Such false signalling will cause
the spiders to stop searching for a more favourable humid environment, which is
also achieved via locomotion disruption. After penetration of pyrethroid into the
haemolymph, diuretic hormone is produced, which will cause active water excre-
tion (Jagers op Akkerhuis et al. 1997). Indeed, pyrethroids have been shown to
increase diuresis by anal excretion (Everts et al. 1991). If passive water loss and
water excretion increases with time, it can lead to mortality, particularly in a dry
environment (Jagers op Akkerhius et al. 1995). In O. apicatus, high susceptibility
was found at high temperatures and low humidity. High humidity, on the other
hand, reduced intoxication.
420 S. Peka
´r
31.3.3 Movement
Locomotion is a fundamental behavioural property of spiders. It reflects interaction
with the environment; therefore, walking activity is the easiest behaviour in which
to detect sublethal effects, particularly in cursorial species. At relatively higher
doses or concentrations, movement is usually reduced, while at relatively lower
doses or concentrations, it is induced. The application of pyrethroids on P. amentata
caused ataxia and paralysis of the fourth legs for 3 days, probably due to relaxation
of the flexor muscles (Shaw et al. 2006). It increased quiescence for 12 h, and
recovery was observed after 24 h (Baatrup and Bayley 1993). In two linyphiids,
Tenuiphantes tenuis and Oedothorax apicatus, pyrethroids reduced levels of move-
ment, which lasted for several days (Shaw et al. 2005; Everts et al. 1991). This is
because high velocities require greater neural control and energy, which the spider
is likely deprived of. Contact with surfaces treated with organophosphate shifted the
circadian rhythm in the lycosid Rabidosa rabida and the salticid Salticus scenicus
(Tietjen and Cady 2007). The spiders were active earlier than normal. The authors
suggest that organophosphate affected the interaction between the light receptors
and the circadian clock. The lycosid Pardosa palustris not only moved less on
organophosphate- and pyrethroid-treated surfaces than on control (Fig. 31.2) but
exhibited an uncoordinated walking pattern (Peka
´r and Benes
ˇ2008).
If movement is induced, it is probably an indication of avoidance and subsequent
dispersal. Avoidance is induced by repulsion. In pyrethroids, the active ingredient is
often highly repellent, whereas in other pesticides repulsion is caused by the
additives (Desneux et al. 2007). Whether pesticides induce dispersal has not yet
been studied. However, results from two studies suggest that it might. The lycosid
Pardosa milvina increased its speed of movement on a herbicide-treated surface and
thus minimised exposure and risk (Evans et al. 2010). Contact with a surface treated
with an organophosphate elevated activity in the lycosids Schizocosa ocreata and
R. rabida, in the linyphiid Frontinella communis, and in the S. scenicus presumably
because the spiders tried to avoid it (Tietjen and Cady 2007). Alternatively,
ab
Fig. 31.2 Path tracks by Pardosa spiders when exposed to control surface (a) and pyrethroid
residues (b) for a period of 2 h
31 Side Effect of Synthetic Pesticides on Spiders 421
in lycosid and salticid species, increased activity could be caused by impaired visual
processing due to the abnormal function of neurotransmitters in the protocerebral
ganglion.
31.3.4 Predation
Reduced locomotor activity must have a negative effect on prey search and
frequency of capture, particularly in cursorial species. In web-building species,
such inhibition leads also to alteration of the web size and/or web design. Further-
more, some pesticides may reduce olfactory capacity and disrupt the detection of
kairomones from prey and, if a pesticide has an antifeedant property, even decrease
consumption (Desneux et al. 2007).
Reduced prey capture frequency lasting for several days was reported for several
species: Pardosa pseudoannulata after neonicotinoid application (Widiarta et al.
2001); the araneid Neoscona pratensis following spinosyn application (Benamu
´
et al. 2007); and Pardosa amentata and two linyphiids, Erigone atra and Oedothorax
apicatus, following the application of pyrethroids (Dinter et al. 1998; Shaw et al.
2006). The araneid Alpaida veniliae rejected prey intoxicated with herbicide for
4 days probably because of aversion (Benamu
´et al. 2010). Surprisingly, even insect
growth regulators caused reduced prey consumption in P. piratoides, but the mech-
anism is not known (Deng et al. 2008).
A more sophisticated approach to investigating sublethal effects on predation is to
study the functional response, that is, the relationship between prey capture and prey
density, as it allows two components of predation to be estimated: searching efficiency and
handling time. Only in a few studies, the functional response has been investigated.
Typically, spiders show type 2 response. In Philodromus cespitum exposure to
benzoylurea, spinosyn, and neonicotinoid reduced type 2 functional response (Fig. 31.3)
due to an increase in handling time (R
ˇeza
´c
ˇet al. 2010). In females of Hylyphantes
graminicola,preycapturewasreducedfor24hfollowing topical application of an
organophosphate, after which it changed from type 2 to type 1 response (Deng et al. 2007).
The effect on web design has been studied mainly in orb-weaving species
probably because changes to the web architecture are easier to detect and quantify
than in species constructing three-dimensional webs. Topical application of
pyrethroids dramatically reduced web frequency and size in the araneid Araneus
diadematus (Samu and Vollrath 1992). In another araneid, Larinioides sclopetarius,
application of organophosphate and organochlorine only slightly altered web archi-
tecture, but the application of pyrethroid delayed web construction and reduced its
size by more than 70 % (Lengwiler and Benz 1994). Oral application of herbicide
altered web production in terms of number of radii and spiral threads (Fig. 31.4)in
Alpaida veniliae (Benamu
´et al. 2010). Sublethal doses of spinosyn and a pyrethroid
reduced the frequency of web building in Neoscona pratensis (Benamu
´et al. 2007).
Reductions in the size of webs were also observed in the sheet-web-building
linyphiid Tenuiphantes tenuis following pyrethroid application (Shaw et al. 2005).
422 S. Peka
´r
31.3.5 Reproduction
Reproduction involves a series of processes coordinated by the nervous and hor-
monal systems, namely, mate finding, chemical or sound communication, court-
ship, mating, egg sac production, spermatogenesis/oogenesis, and brood care. All
these processes are prone to being affected particularly by neurotoxic substances,
yet evidence is scarce. Contact with surfaces treated with an organophosphate
lowered the rate of mating in Rabidocosa rabida (Tietjen 2006). In a few other
cases the inhibitory effect seems to result from reduced prey consumption prior to
Fig. 31.4 Comparison of webs produced by Alpaida veniliae in the laboratory (a) constructed
under control conditions and (b) constructed under glyphosate treatment applied orally via prey
(photos: Benamu
´)
0
2
4
6
8
10
12
0 5 10 15 20
Prey density
No. of prey killed
control
acetamiprid
spinos ad
Fig. 31.3 Functional response curves of type 2 in Philodromus spiders and Drosophila flies
offered as prey following application of two insecticides (neonicotinoid and spinosyn) and the
control. Points are means; whiskers are standard errors of the mean
31 Side Effect of Synthetic Pesticides on Spiders 423
oviposition. A pyrethroid and/or organophosphates caused a reduction in egg sac
production in three linyphiids, Erigone atra,Oedothorax apicatus (Dinter et al.
1998), and Hylyphantes graminicola (Deng et al. 2006; Peng et al. 2010). Females
of Pirata piratoides produced fewer eggs and had lower fertility following insect
growth regulator application (Deng et al. 2008). Application of herbicide decreased
fecundity and fertility in Alpaida veniliae (Benamu
´et al. 2010). This was probably
the result of starvation, as the spiders refused to consume contaminated prey.
31.3.6 Development
Abnormal egg sacs and dehydrated eggs were observed in Neoscona pratensis after
spinosyn and pyrethroid applications (Benamu
´et al. 2007). Herbicide applied
through prey in Alpaida veniliae increased the number of abnormal eggs and
prolonged instar duration (Benamu
´et al. 2010). In Hylyphantes graminicola,
offspring from mothers exposed to pyrethroid took longer to develop and had
lower mass (Peng et al. 2010). Organophosphate application resulted in smaller
body size in H. graminicola (Deng et al. 2006). Whether this was a direct effect of
the formulation or an indirect effect of reduced feeding remains to be investigated.
31.3.7 Defence
Secondary defence strategies, such as escape, are based on movement abilities. In
cursorial species, reduced speed of movement would increase susceptibility to
predation. In web-building species, for example, linyphiids, spraying causes them
to leave their webs. As a result, they become more exposed to predators. Everts
et al. (1991) proved that reduced speed of movement in Oedothorax apicatus
females following contact with pyrethroid caused higher predation by carabids.
Pesticides can also interrupt signalling from kairomones produced by predators.
Spiders thus would not be able to avoid areas signalling the presence of predators.
Wrinn et al. (2012) tested whether Pardosa milvina can recognise cues from its
intraguild predators when the surface is treated with glyphosate and found that the
response to kairomones from one predator was not dramatically altered by the
herbicide but elevated to cues from another predator.
31.4 Hormesis
As outlined above, low doses or concentrations of pesticides can cause improved
performance. This could help spiders to suppress pests if the magnitude of improve-
ment was marked. Evidence for hormesis in spiders is still scarce and insufficient
chiefly because most toxicological studies have centred on higher concentrations/
424 S. Peka
´r
doses. A low dose of organophosphates stimulated predation in Hylyphantes
graminicola (Deng et al. 2007), which killed more prey (but did not consume
them), and in two lycosids, Pardosa pseudoannulata and Pardosa amentata
(Toft and Jensen 1998; Wang et al. 2006b). Detailed analysis of the functional
response revealed that it was due to an improvement in the searching efficiency
of the predator. Physiological processes are stimulated by low doses too.
Organophosphates induced, though only slightly, the hatching rate in
H. graminicola (Deng et al. 2006). When P. pseudoannulata was treated with a
low dose of an organophosphate, the protease activity increased (Wang et al.
2006a). Strangely enough, growth rate was higher and body size was larger in
Pirata piratoides after application of an insect growth regulator at LD50 than after
application at LD10 (Deng et al. 2008). The occurrence and magnitude of hormesis
in spiders thus requires additional investigation.
31.5 Conclusions
Sublethal concentrations/doses affect a variety of traits. Although evidence of
sublethal effects has been gathered for several spider species and formulations, it
is still insufficient with respect to all possible effects, species, formulations, and
concentrations/doses. Many effects—for example, on dispersal, defence, or
fecundity—are only presumed and remain to be investigated.
Due to the current development of plant protection measures towards the use of
selective chemical substances with limited direct effect on natural enemies, the
toxicology of spiders should be centred on sublethal effects. New protocols and
guidelines for risk assessment are needed to achieve fast and reliable quantification
of the effects. This should be paralleled by the detailed study of a selected agrobiont
species and estimation of the relative importance of particular life-history traits
prone to sublethal doses. For example, predation and reproduction represent two
different life-history components. Predation is a daily activity, while reproduction
usually takes place only once in a spider’s life. Thus, failure to capture prey has an
immediate effect on biological control, whereas failure to reproduce would affect
the control potential of the next generation.
What is the influence of sublethal effects at the population level? It is difficult to
estimate because the consequences of effects at physiological levels are often
unknown (Desneux et al. 2007). However, it is expected that even minor disruptions
caused by sublethal doses can render spiders ineffective for biological control and,
on a longer-term basis, can have an impact on the intrinsic rate of population
increase.
31 Side Effect of Synthetic Pesticides on Spiders 425
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31 Side Effect of Synthetic Pesticides on Spiders 427
... Studies on the impact of pesticide treatments on the agrobiont spider fauna have mostly been focused on their lethal/sublethal eff ect , Mullié & Everts 1991, Dinter & Poehling 1995, Pekár 2002, 2012, Fernandes et al. 2016 or infl uence on the spiders' locomotion (Baatrup & Bayley 1993, Pekár & Haddad 2005, Pekár & Beneš 2008, predatory activity (Deng et al. 2007, Pekár 2013, Korenko et al. 2016, web building (Benamú et al. 2010) and reproduction (Dinter et al. 1998, Tietjen 2006, Deng et al. 2008. Some research has been focused on the relationship between the use of insecticides and overall spider abundance (Bogya & Markó 1999, Thorbek & Bilde 2004, Diehl et al. 2013. ...
... It has been found that a low dose of insecticides can stimulate predation in Hylyphantes graminicola (Sundevall, 1830) (Linyphiidae) (Deng et al. 2007), Pardosa pseudoannulata (Böesenberg & Strand) and P. amentata (Clerck, 1757) (Lycosidae) (Toft & Jensen 1998, Wang et al. 2006, which killed more prey organisms but did not consume them. Buprofezin also induced a higher growth rate and larger body size in Pirata piratoides (Schenkel) (Lycosidae) (Deng et al. 2008) due to improvement in the efficiency of searching for prey (Pekár 2013). Low doses of pesticides can have a beneficial effect and improve performance, despite being toxic at higher levels, a phenomenon known as hormesis (Pekár 2013). ...
... Buprofezin also induced a higher growth rate and larger body size in Pirata piratoides (Schenkel) (Lycosidae) (Deng et al. 2008) due to improvement in the efficiency of searching for prey (Pekár 2013). Low doses of pesticides can have a beneficial effect and improve performance, despite being toxic at higher levels, a phenomenon known as hormesis (Pekár 2013). We only can assume that the larger size of female individuals of O. apicatus on the conventional OSR field can be explained by this. ...
... Elevated temperature affects the spiders' response to pyrethroids in two opposing ways, hastening absorbance, which increases toxicity, but also increasing metabolism of the pesticide, which shortens recovery time for sublethal doses [26]. Pyrethroids also interfere with water transport in arthropods, leading to dehydration [26,27], which can affect all aspects of physiology. ...
... The rapid rebound of mosquito populations over the three days following adulticide application [13,17] matches the three-day period of spider immobility found in this study and others [23,24,27]. Recovery of spiders' web construction and prey capture abilities would correspond to the return to the lower survival rate of adult Ae. aegypti three days after adulticide spray application. ...
... Recovery of spiders' web construction and prey capture abilities would correspond to the return to the lower survival rate of adult Ae. aegypti three days after adulticide spray application. Non-lethal effects on spiders in this study have been seen in other species and with other pesticides [1,4,5,27]. Similarly, population increase of agricultural pests following reduction of spiders through pesticide application has been documented repeatedly [28]. ...
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Spiders are important population regulators of insect pests that spread human disease and damage crops. Nonlethal pesticide exposure is known to affect behavior of arthropods. For spiders such effects include the inability to repair their webs or capture prey. In this study, nonlethal exposure of Mabel’s orchard spider (Leucauge argyrobapta) to the synthetic pyrethroid permethrin, via web application, interfered with web reconstruction and mosquito capture ability for 1–3 days. The timing of this loss-of-predator ecosystem function corresponds to the rapid population rebound of the yellow fever mosquito (Aedes aegypti) following insecticide application to control arbovirus epidemics. We suggest this temporal association is functional and propose that follow-up study be conducted to evaluate its significance.
... As insecticides decline in use due to increased resistance, regulation and detrimental environmental effects, alternative and integrated pest management is increasingly pertinent (Fountain et al., 2007;Loetti & Bellocq, 2017;MacFadyen et al., 2009;Pekár, 2013;Whitehorn et al., 2012). Specialist predators and parasitoids offer effective biocontrol, but given their dependence on a narrow niche of host/prey taxa, pest populations can reach large sizes before these biocontrol agents intervene (Ammann et al., 2020;Jordan et al., 2020;Levie et al., 2005;Sunderland et al., 1997). ...
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Spiders are among the dominant invertebrate predators in agricultural systems and are significant regulators of insect pests. The precise dynamics of biocontrol of pests in the field are, however, poorly understood. This study investigates how density-independent prey choice, taxonomy, life stage, sex, and web characteristics affect spider diet and biocontrol. We collected spiders in four genera of Linyphiidae (i.e., Bathyphantes, Erigone, Tenuiphantes, and Microlinyphia), and individuals from the Lycosidae genus Pardosa, and their proximate prey communities from barley fields in Wales, UK between April and September 2018. We analyzed the gut contents of 300 individual spiders using DNA metabarcoding. From the 300 spiders screened, 89 prey taxa were identified from 45 families, including a wide range of pests and predators. Thrips were the dominant prey, present in over a third of the spiders sampled , but a type IV functional response appears to reduce their predation at peak abundances. Spider diets significantly differed based on web characteristics, but this depended on the genus and sex of the spider and it was not the principal separating factor in the trophic niches of linyphiids and lycosids. Diets significantly differed between spider genera and life stages, reflected in different propensities for intragu-ild predation and pest predation. Adult spiders predated a greater diversity of other predators, and juveniles predated a greater diversity of pests. Overall, Tenuiphantes spp. and Bathyphantes spp. exhibited the greatest individual potential for biocontrol of the greatest diversity of pest genera. The greater trophic niche complementarity of Pardosa spp. and Erigone spp., however, suggests that their complementary predation of different pests might be of greater overall benefit to biocontrol. Sustainable agriculture should aim to optimize conditions throughout the cropping cycle for effective biocontrol, prioritizing provision for a diversity of spiders which predate a complementary diversity of pest species.
... The most abundant species in olive canopies was the linyphiid Frontinellina frutetorum, also observed by Gaymard & Lecigne (2018) in mesophile woods. In fact, this species was numerous in the samples from woods and garrigue next to olive groves, despite previous analyses highlighting a lower number of F. frutetorum in garrigue-dominant landscapes (Picchi et al. 2016), probably due to the risk of desiccation (Pekár 2013). Likewise, Frontinellina frutetorum was dominant among 48 species in Iranian olive groves (Ghavami 2006). ...
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In the Monte Pisano area (Tuscany, central Italy), spiders were collected within two research projects during three years (2010, 2013, 2014). Olive groves and adjacent semi-natural habitats (wood and Mediterranean garrigue) were investigated with three sampling methods (pitfall trapping, beating at branches and hand collection in the canopy). A total of 148 species was identified. The ground spider (Gnaphosidae) Zelotes fulvaster (Simon, 1878) was recorded for the first time in Italy.
... Arthropod predators (spiders and insect predators) are natural enemies commonly found in many agroecosystems. They are often the most abundant and diversified natural enemies, and contribute to the reduction of several pests (Pekár, 2013). Predators typically consume several prey species during their lives and can be predacious when immature, as adults, or during both phases of their lives (Strand & Obrycki, 1996). ...
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Many problems arise in the cultivation of crops; one of these problems is insect pests that can threaten crop production. Integrated pest management is an alternative technique for managing the balance of the agricultural environment. Habitat manipulation by increasing plant diversity with refugia is considered an alternative way to maintain natural enemy in an agro ecosystem. The use of soybean as a refugium in a crop field is still limited. Research was conducted to investigate the diversity of predatory arthropods in soybean as a refugium in a chilli pepper crop field at the Agro-technology Training Centre (ATC) at the University of Sriwijaya. In this study, four varieties of soybean (Dena 1, Detam 3 PRIDA, Deja 1, and Devon 1) were used as refugia. Three observation methods were carried out using nets, pitfall traps and visual observation for 7 weeks. The results show that arthropod diversity in soybean plants comprised 6 orders with 10 families and 19 species. Odontoponera denticulata (Hymenoptera) was the most predominant arthropod predator, observed in 73% of all soybean varieties. The number of canopy-dwelling arthropod predators was similar in the four soybean varieties.
... Pesticides are highly successful at killing pests, but they also unconsciously reduce the nontarget organisms and natural predators of insect pests including spiders (Amalin et al. 2000, Deng et al. 2006, Cole et al. 2010). Spiders are highly at risk to pesticides that are being used in agricultural fields injudiciously (Pekar 2013). These chemicals affect their longevity, reproduction, defense, development, physiology, mobility, and activities of enzymes (Stark and Banks 2003, Moura et al. 2006, Tahir et al. 2012, Miao et al. 2014, Ndakidemi et al. 2016. ...
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The present study was designed to record the effect of λ-cyhalothrin, Bifenthrin, and Glyphosate on the mortality, avoidance behavior, foraging activity, and activity of Acetylcholine esterase (AChE) and Carboxylesterase (CarE) in Neoscona theisi (Walckenaer, 1841). Highest mortality (70%) in N. theisi was recorded against λ-cyhalothrin. However, Glyphosate was found to be least toxic. Spider spent less time on insecticides/herbicide-treated surfaces. Insecticides/herbicide-treated N. theisi consumed less prey than untreated control spiders. Similarly, when N. theisi were offered insecticide/herbicide-treated prey, they consumed significantly less. Increased AChE and CarE activities were recorded in insecticides/herbicide-treated spiders as compared to control group. Total protein contents were less in insecticides/herbicide-treated spiders than control group. The results revealed that λ-cyhalothrin is more harmful to spiders as compared to Bifenthrin and Glyphosate. It is suggested that the effect of all pesticides used in agro-ecosystem on beneficial insects should be evaluated before using them in the fields.
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Clubroot, caused by Plasmodiophora brassicae, is an internationally important disease of oilseed rape (Brassica napus), causing serious losses in Europe, North America and Australia. Nowadays, the disease is an increasing problem not only to oilseed rape but also to all Brassica species. The detection of 124 new P. brassicae-infested fields during 2013-2017 across several federal states in Germany suggests that clubroot disease maybe more widespread in oilseed rape fields than previously thought. To date, growing resistant cultivars is the most effective and environmentally safe strategy for controlling clubroot (Hirai, 2006; Diederichsen et al., 2009), but sometimes this resistance can be overcome as new pathotypes of the pathogen emerge (Zamani-Noor, 2017). At the present study, calcium cyanamide and burnt lime used with cultivar resistance were evaluated for their potential in integrated management of clubroot disease in oilseed rape cultivation.
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Plasmodiophora brassicae has recently become one of the most damaging pathogens to oilseed rape (OSR) cultivation in Europe. Questionnaires submitted by farmers and extension services revealed short rotation (once in 2-3 years) of the crop in 70% of fields. Frequency of OSR in the rotation significantly correlated with the incidence and prevalence of clubroot disease. Although there was a significant negative correlation between the disease index and soil pH, the occurrence of clubroot was not restricted to fields with highly acidic soils. Characterization of P. brassicae populations on the European Clubroot Differentials (ECD), and classification by the differential hosts of Williams or Somé et al. revealed that pathotypes: ECD 16/31/31 and 16/14/31; 4, 6 and 7; and P1 and P3, respectively, are predominant in central Europe. Several populations were found that could overcome the resistance of cv. Mendel, the first cultivar of OSR bred for resistance to clubroot.
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Insecticide formulations can cause mortality in natural enemies or have sublethal effects on them, which include alterations in their behaviour and development. Here, we investigated the effect of a bioinsecticide (azadirachtin) and predator cues on mating in a biocontrol spider, Philodromus cespitum. Firstly, adult males were exposed to cues from ants (as predators) or conspecific juveniles (as controls) and those from virgin adult females combined with insecticide residues and we then recorded their selection of the respective surfaces. In an insecticide-free environment, males spent significantly more time on the surface with cues from juveniles and virgin females than on the surface with cues from ants and virgin females. In the environment with ant cues, males did not spend significantly more time on the surface treated with water or insecticide residues. Secondly, adult male and female spiders were exposed to cues from predators and conspecifics and fresh insecticide residuals and we recorded mating behaviour. The presence of ant cues nor the presence of insecticide residues had a significant effect on the mating behaviour. However, the frequency of females biting males was significantly lower on the surface with insecticide residues and ant cues and highest on the surface with ant cues and water treatment. The size of mating plugs (applied to female genitals by males during mating) was not different between ant cues and control, but the plugs were significantly larger on the surface with insecticide residues. We conclude that azadirachtin affected only slightly the perception of predation risk and consequently mating behaviour in P. cespitum. Similarly, presence of ant cues had little effect on mating.
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Four species from three families of spiders were exposed to sublethal concentrations of the neurotoxic pesticide malathion: Schizocosa ocreata (Hentz 1844), Rabidosa rabida (Walckenaer 1837), Frontinella communis (Hentz 1850), and Salticus scenicus (Clerck 1757). Spider activity was recorded using a proprietary computer vision system equipped with artificial intelligence routines. Exposure to malathion changed the spiders' propensity to move, levels and patterns of activity, and distance moved. Dosed spiders increased their activity between 12 and 40%, depending on the species. Continuous recordings for ≥ 24 h revealed the peak activity for dosed R. rabida and S. scenicus was shifted ∼ 1 h earlier than controls. Spiders exposed to malathion also significantly increased the distance they moved per locomotory bout. This is consistent with the action of an organophosphate neurotoxin acting as an acetylcholinesterase inhibitor. Thus, exposure to sublethal doses of malathion appears to affect the neural basis for these spider's normal diel periodicities, time budgets, and patterns of locomotion, probably reducing their efficiency as agents of biological control.
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• Mixtures of organophosphorus and pyrethroid insecticides are widely used to combat resistance in agricultural pests, although few studies have been conducted on the effects of pesticide mixtures on beneficial nontarget organisms. • In the present study, we exposed adult females (F0) of Hylyphantes graminicola (Araneae: Linyphiidae) to fenvalerate, dimethoate and their commercially available 1 : 1 mixture (by mass). We investigated the acute toxicity of these pesticides to the exposed adults, as well as sublethal effects on reproduction and acetylcholinesterase and carboxylesterase activity. We also studied the effects of parental exposure on the size, development and enzyme activity of unexposed offspring. • All three formulations were acutely toxic to H. graminicola, with synergism between dimethoate and fenvalerate leading to greater toxicity in the 1 : 1 mixture than for the two insecticides alone. The sublethal effects of direct pesticide exposure were a reduction in acetylcholinesterase and carboxylesterase activity and a reduction in the number of egg sacs produced by exposed spiders relative to the control spiders. The unexposed offspring of the fenvalerate and mixture exposed spiders were smaller and took longer to mature than the control spiders. Offspring of all exposed spiders also had significantly reduced carboxylesterase activity relative to control spiders. • We concluded that the effects of parental exposure on the offspring were likely to increase their susceptibility to future pesticide exposures, and reduce the capacity of this spider to serve as a pest control agent.
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The effect of a pyrethroid insecticide, deltamethrin, on water loss, metabolic rate and immobilisation was studied, using the epigeal spider Oedothorax apicatus (Blackwall) (Linyphiidae) as a test species. Water loss was measured gravimetrically at different temperatures, air humidities, and doses of deltamethrin. Metabolic rate and immobilisation were measured at different temperatures and doses. Immobilisation was measured at different relative humidities and temperatures. Water loss due to evaporation increased linearly with vapour pressure deficit. The slope of the latter relationship increased with temperature, indicating an increase in cuticle permeability with temperature. In addition to water loss by evaporation, deltamethrin treatment induced water excretion. This was positively related to dose and temperature, but independent of air humidity. Metabolic rate increased with temperature and dose. Immobilisation was highest at low temperatures in combination with low air humidity. The consequences of pesticide-induced water excretion are discussed with respect to field- and laboratory-based dose-effect relationships for pyrethroids presented in the literature. The present results seem to offer an explanation for hitherto unexplained minima in temperature-response curves in pyrethroid toxicity in some arthropod species. It is concluded that simultaneous measurements of metabolic rate, water-loss rate and pesticide effects are a prerequisite for an understanding of the effects of pesticides on arthropods.
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Spiders are among the most important predators of insect pests in all types of agricultural situations. The activity of three systems of detoxification enzymes, glutathione transferase (GST) and two glutathione peroxidases (GSH-Px), was measured in cypermethrin-treated wolf spiders (Pardosa amentara) collected at three different times in relation to hibernation. On each occasion separate groups of spiders had been treated by topical application with four doses of cypermethrin and compared to controls. The results indicate different responses of these enzymes with respect to life cycle variation and inducibility by cypermethrin. GST responded only slightly to cypermethrin, activity being reduced at high doses. It showed a remarkable seasonal variation, with winter season activity reduced to half that of active periods. GSH-Px(H2O2) and GSH-Px(TBH) had very low basal activity in autumn, but higher activity could be induced by cypermethrin. In winter, basal levels of these systems were high and cypermethrin reduced their activity. In spring GSH-Px(H2O2) returned to the autumn pattern. GSH-Px(TBH) maintained a high basal level that could be further induced. Our findings indicate that during hibernation spiders have several detoxification systems that are active, while during active phases they rely more on inducibility.
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Laboratory and field experiments were conducted to examine whether a sublethal dosage application of imidacloprid can induce physiological or ecological resurgence in the green leafhoppers Nephotettix virescens and Nephotettix cincticeps. Fecundity of N. virescens and N. cincticeps exposed to imidacloprid-treated rice seedlings was reduced to one-third and one-half, respectively, that of insects not exposed. Effect of imidacloprid on egg parasitoids of N. virescens was not detected because the percentage parasitism of JV. virescens eggs was very low. The number of N. virescens adults consumed by a lycosid spider Pardosa pseudoannulata which was exposed to imidacloprid-treated rice seedlings for the last 24 h before experiment was significantly lower than that on untreated ones. However, the number consumed by a spider fed prey treated directly with imidacloprid was not significantly different from that of untreated prey. Survivorship of the mirid bug Cyrtorhinus lividipennis and the proportions of N. cincticeps eggs preyed on by bugs exposed to imidacloprid-treated seedlings or fed on eggs laid in the stems of treated seedlings were significantly lower than those of untreated ones. The results suggest that a sublethal dosage application of imidacloprid does not cause physiological resurgence in both green leafhopper species but it does induce ecological resurgence.
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Field experiments have revealed that some species of spiders are more sensitive to insecticides than others. Among many factors influencing their susceptibility, foraging mode seems to play an important role. Aspects of foraging mode that appear to be relevant are whether the spider is diurnal or nocturnal, a hunter or a web-maker. Six spider species, Araniella opisthographa, Clubiona neglecta, Dictyna uncinata, Pardosa agrestis, Philodromus cespitum and Theridion impressum were used in the study. P agrestis and P cespitum are diurnal hunters that may come into direct contact with insecticide. C neglecta is nocturnal and so is exposed to residues only. The remaining three species are web-makers building webs that vary in the extent to which they can protect the spider from direct spray. The effect of sprays was tested under laboratory conditions (Potter tower) with three commercial insecticides, an insect growth regulator (hexaflumuron), a selective organophosphorus (phosalone) and a non-selective pyrethroid insecticide (permethrin) using a four-day exposure period. Data were analysed using bootstrap method and randomization tests. The results obtained showed that hunting spiders were more susceptible to the insecticides tested than web-makers (in their webs). Diurnal hunting spiders (Philodromus and Pardosa) were severely affected only by permethrin. A high mortality was observed for the nocturnal hunter, Clubiona, after application of phosalone and permethrin. This species appears to be very sensitive to residues of both insecticides. Comparing the effect on web-making spiders, with and without webs, it was observed that the sparse orb-web of Araniella did not protect its owner at all, but the dense cribellate and frame-webs of Dictyna and Theridion, respectively, reduced the mortality caused by permethrin significantly in comparison with specimens without webs. Of other factors studied, posture (normal and upside-down position) did not influence the susceptibility. Mortality increased slightly with body size after permethrin application.© 1999 Society of Chemical Industry
Article
Sublethal effects of four pesticides (Pirimor®, active ingredient [a. i.] pirimicarb; Decis®, a. i. deltamethrin; Alaxon® D, a. i. diazinon; Kelthane® EC, a. i. dicofol) on the web building behaviour of the common gray cross spider Larinioides sclopetarius (Clerck) were investigated with the spider test of Witt and Peters. Pirimicarb applied in a dose of 0.64 μg/mg (corresponding to the application of 1.28 μg/mg Pirimor®) caused neither mortality nor aberrations in web geometry. Alaxon® D led in a dose of 5×10−4 μl/mg to a mortality rate of 17.6 %. Web building activity was only slightly affected. The webs themselves showed some changes. The area of the webs was reduced to 62 % of the original size. The regularity of the catching spiral and the median angles of the radii were also affected but in a lesser degree. Decis® applied in a low dose of 5×10−5 μl/mg caused 10 % mortality. Web building activity was affected (average delay in web building was 2.32 days). The area of the webs was reduced to 72 %, the number of radii was reduced by 17 %, the median angle of the radii was enlarged by 21 % and the regularity of the angles was reduced by 36%. Kelthane® EC, in a high dose of 9.6×10−3 μl/mg, resulted in 10% mortality. No negative influence on web building activity was recorded. The webs themselves were hardly affected: only the number of radii was reduced by 5 %. The efficiency of the various pesticides can be ranked as follows: Decis® (deltamethrin) » Alaxon® D (diazinon) > Kelthane® EC (dicofol) Pirimor® (pirimicarb). Substance specific differences of the effects are discussed. Zur Wirkung einiger Pestizide auf das Netzbauverhalten von Larinioides sclopetarius (Clerck) (Araneae, Araneidae) Die Wirkung der vier Pestizide Pirimicarb (Handelsname Pirimor®), Decis® (Wirkstoff Deltamethrin), Alaxon® D (Wirkstoff Diazinon) und Kelthane® EC (Wirkstoff Dicofol) auf den Netzbau der Brückenspinne Larinioides sclopetarius (Clerck) wurde mit Hilfe des Spinnentests von Witt und Peters untersucht. Pirimicarb verursachte in einer Dosierung von 0,64 μ/mg (dies entspricht einer Dosis von 1,28 μg/mg Pirimor®) weder Mortalität noch irgendwelche Änderungen im Netzbau. Alaxon® D (Diazinon) verursachte mit 5×10−4 μl/mg eine Mortalität von 17,6%. Die Netzbauaktivität war kaum vermindert. Die Netze selber waren jedoch um 38 % verkleinert. Die Regelmäßigkeit der Fangspirale und der mediane Winkel der Radien zeigten ebenfalls Veränderungen; diese waren allerdings nicht so gravierend wie bei der Netzfläche. Decis®, appliziert in einer Dosis von 5×10−5 μl/mg, bewirkte eine Mortalität von 11,4%. Die Netzbauaktivität war deutlich reduziert, betrug doch die durchschnitt-liche Netzbaupause 2,32 Tage. An den Netzen konnten folgende Veränderungen festgestellt werden: Die Netzfläche wurde um 28 % verkleinert, die Anzahl der Radien um 17 % reduziert, die medianen Winkel um 21 % vergrößert und die Winkelregelmäßigkeit um 36 % vermindert. Kelthane® EC in einer Dosis von 9.6×10−3 μl/mg verursachte eine Mortalität von 10%. Die Netzbauaktivität war hingegen nicht betroffen. Auch die Netze selber zeigten kaum Veränderungen; nur die Anzahl der Radien wurde leicht um 5 % vermindert. Aufgrund der Resultate konnten die Pestizide nach ihrer Wirksamkeit auf das Spinnverhalten rangiert werden: Decis® (Deltamethrin) ≫ Alaxon® D (Diazinon) > Kelthane® EC (Dicofol) Pirimor® (Pirimicarb). Substanzspezifische Unterschiede der registrierten Effekte werden in der Arbeit diskutiert.
Article
The effects of exposure to a single sublethal dose of the pesticide malathion on the courtship and mating behavior of the lycosid, Rabidosa rabida (Walckenaer 1837) is explored. Animals were tested in combinations where one or both sexes were exposed to the insecticide. The data indicate that while there was no effect on the patterning of courtship behavior, control males initiated courtship more rapidly than dosed animals. Mating behavior was severely disrupted and resulted in most dosed males being killed by females without achieving copulation.