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Spider orb web as bioassay for pesticide side effects
Abstract and Figures
Pesticides may affect the predatory and reproductive behaviour of beneficial arthropods short of having direct effects on their survival. We present a bioassay designed to test (ultimately in the field) such hidden effects of agrochemicals in their application concentrations. As a paradigm we chose the web-building behaviour of the cross spider Araneus diadematus Clerck (Araneidea, Argiopidae) and we selected four commonly used pesticides: Oleo Rustica 11E (mild insecticide), Fastac (pyrethroid insecticide), Bayfidan and Sportak (fungicides). Neither fungicides nor the mild insecticide seem to affect web-building behaviour significantly, whereas the pyrethroid insecticide suppressed web-building frequency and severely affected web size and building accuracy.
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... Insecticides can affect natural enemies, as well as other nontarget and target organisms, through lethal or sublethal exposure (Fernandes et al., 2010;Pekár, 2012;Walker, 2004). Although sublethal exposure does not result in death, it can alter the physiology, development and behaviours of arthropods (Desneux et al., 2007;Pekár, 2012;Samu & Vollrath, 1992). Whilst this may appear to be less detrimental to natural enemy populations, the effects are often comparable and perhaps of more importance than lethal exposures (Hanna & Hanna, 2013), especially when considering the greater rate of encounter in nature (Ricupero et al., 2020;Tahir et al., 2019). ...
... Spiders have been documented as the most abundant and important group of predatory invertebrates throughout many terrestrial ecosystems, including agroecosystems (Nyffeler & Benz, 1987;Nyffeler & Birkhofer, 2017;Samu & Vollrath, 1992). Spider populations naturally exist as an assemblage of several species, and as generalist predators they collectively stabilise invertebrate communities, regulating the density of other predators and herbivores (Branco & Cardoso, 2020;Milano et al., 2021), and even suppress pest populations, acting as essential biological controls (Sharma et al., 2013;Sunderland, 1999). ...
... Orb-weaving spiders are a particularly useful guild for sublethal studies of insecticides as the webs are a fixed record of complex behaviours that are governed by internal and external factors (Hesselberg, 2015;Samu & Vollrath, 1992). Many studies have utilised the orb-web and its ease of analysis to aid in understanding the effects of insecticides and other neurotoxins on associated web-building behaviours (Albín et al., 2014;Blackledge, 2011;Hesselberg & Vollrath, 2004). ...
Orb‐weaving spiders are abundant predators in agroecosystems and serve as key natural enemies for pest control. However, studies have demonstrated that many insecticides can negatively affect the predatory behaviours of spiders when exposed to sublethal concentrations, thus disrupting their biocontrol potential and subsequent ecosystem dynamics. Understanding how insecticides impact spiders is, therefore, of great importance.
This study investigated the effects of two conventional insecticides (thiamethoxam and deltamethrin), and a common biopesticide (neem oil) compared to a tap water control on the functional response of a common orb‐weaver Araneus diadematus .
Spiders were collected from the wild and maintained under laboratory conditions in containers (20 × 20 × 5 cm) to allow for web production. Spiders were then exposed to one of the four treatments and Drosophila melanogaster were added to the webs as prey at densities of 1, 3, 5, 10, 20, and 40, with the number of consumed prey quantified after 16‐h to determine the functional response.
Overall, A. diadematus exhibited a type II functional response when exposed to the control, thiamethoxam and neem oil treatments, with comparable consumption rates, search coefficients and handling times. This contrasted with deltamethrin‐treated spiders which exhibited a type III functional response and a lower consumption rate of prey compared to the control.
This study demonstrates that deltamethrin, unlike thiamethoxam and neem oil, is capable of negatively affecting the biocontrol potential of A. diadematus . However, further research is required to fully understand the impact insecticides have on the predatory behaviours of orb‐weaving spiders.
... This mode of use results in the presence of these insecticides in surface water, groundwater, soil, and even air (Aktar et al. 2009;Zhang et al. 2011;Yadav et al. 2015;Degrendele et al. 2016). This presence causes toxic effects on both target and nontarget organisms (Everts et al. 1991;Samu and Vollrath 1992). In addition, they cause behavioral changes and serious toxic effects in adults, and in juveniles and embryos during development of oviparous and viviparous organisms. ...
... Many spiders are specialized as snare builders, whereas others hunt their preys. Spraying of insecticides affects them because webs may absorb these insecticides, acting as collectors of agrochemical sprays (Samu and Vollrath 1992). Because silk is hydrophobic, it prevents the passage of insecticides in aqueous solution (Zhao et al. 2006) but not insecticides in solution in organic solvents such as acetone (Vetter 2015). ...
The use of pesticides for plague control in agroecosystems generates a threat to wildlife and a major problem for human health. Pesticide compounds are also an important source of water and atmosphere contamination. Although insecticides are effective on their target organisms, they often affect organisms that are not their target The aim of the present study was to research the effects of three types of neurotoxic insecticides—a pyrethroid (cypermethrin), a neonicotinoid (imidacloprid) and an organophosphate (chlorpyrifos)—on behavioral and physiological parameters of Pardosa saltans spider (Lycosidae). This study analyzed for the first time the exploratory behavior of the spider mothers in the presence of these three insecticides on their egg‐sacs and also on the ground. It was also evaluated the oxidative stress effects on the juveniles hatched in the egg‐sac protected by silk in relation to variations of detoxification enzymes (catalase, glutathione of action, such as spiders, which are agrobionts of great importance in agroecosystems. reductase, superoxide dismutase, glutathione‐S‐transferase and glutathione peroxidase) and lipid peroxidation (reactive oxygen species or ROS). The results show that these insecticides are repellents for mothers (cypermethrin is the most repellent) and maternal behavior is modified after detection of an insecticide on their egg‐sac but mothers do not abandon their egg‐sac. These neurotoxic insecticides affect the juveniles inside their egg‐sac. Cypermethrin and chlorpyrifos caused more oxidative stress in juveniles than did imidacloprid. The ROS generated by these insecticides seemed to be adequately eliminated by the juveniles’ antioxidant systems. This article is protected by copyright. All rights reserved.
... In addition, web-spinning spiders can be affected through their webs acting as collectors of agricultural spray. 11,12 The possible level of contamination via prey has been documented by the residues found in the bodies of bees that pollinate crops and are contaminated with pesticides. [13][14][15] Similar to bees, the number of other target or nontarget insects represents a potential contamination source of pesticides for predators. ...
... The prevalence of pesticides in webs and prey remnants indicates that this matrix is the source of contamination for the spider; the pesticide content in this matrix can be divided into the two components -the prey and webs acting as collectors. 11,12 We suggest that the pesticide content in spider females should correspond to the pesticides in the prey, and the difference between them is likely due to particles containing pesticides becoming attached to webs by wind drift. Furthermore, it appears that the mother spider transferred most of the pesticides to the cocoons. ...
Background:
Pesticides or plant protection products (PPPs) are risky for spiders in or near agricultural landscapes. However, the risks of pesticides to spiders are largely understudied compared to pollinators. Here, we investigated the distribution of PPPs in adult females, cocoons and webs with prey remnants of Phylloneta impressa.
Results:
The three sample types were collected from the tops of rapeseed on the 18th of July (before the harvest). Three different UHPLC-QqQ-MS/MS pesticide analyses were performed: (i) pesticides and selected metabolites screening; (ii) quaternary ammonium pesticides (quats); and (iii) pyrethroids. Overall, 23 compounds, 22 pesticides and the metabolite imidacloprid-urea were detected. The array of pesticides was largest in webs with prey remnants, and according to evaluation via redundancy analysis (RDA), the pesticides were similar in spiders and cocoons; however, individual data inspection revealed differences in pesticide distribution in these samples. Clothianidin was detected only in female spiders, while thiamethoxam prevailed in webs with remnants of prey, and acetamiprid, thiacloprid and imidacloprid were found in all three matrices. One of the most abundant compounds detected was chlormequat, indicating that quats should be considered a possible risk for these spiders. None of the pyrethroids were detected despite being applied in the sampling area, indicating rapid biodegradation. In contrast, some pesticides were detected despite not being applied in the field, indicating that the source of contamination is prey or particles carried by wind attached to webs.
Conclusion:
Overall, the results indicate the different distribution or behavior of several pesticides in the spider matrices. This article is protected by copyright. All rights reserved.
... When the unlucky prey fly into the orb web, they get stuck and cannot break free; this increases the foraging success of the spider [28]. In addition, spiders use their orb webs very economically, and orb webs are ingested by the spider for recycling [29,30]. ...
In this review, we discuss the use of time–of–flight secondary–ion mass spectrometry (TOF–SIMS) technology for analyzing the viscous glue (is called aggregate glue droplets) of spider orb webs and examine the results obtained. Element distribution images of the aggregate glue droplets were observed by TOF–SIMS. A uniform element distribution is seen for suspended pristine aggregate glue droplets, and a differential spreading of aggregate glue components is seen for attached aggregate glue droplets. We also observed TOF–SIMS images of water in aggregate glue droplets, where water was observed to be consistent with the distribution of oozing salt. We also found that the alkali metal in the aggregate glue droplets showed similar characteristics by feeding cesium carbonate to spiders.
... When the unlucky prey fly into the orb web, they get stuck and cannot break free; this increases the foraging success of the spider [28]. In addition, spiders use their orb webs very economically, and orb webs are ingested by the spider for recycling [29,30]. ...
In this review, we discuss the use of time-of-flight secondary-ion mass spectrometry (TOF-SIMS) technology for analyzing the viscous glue (is called aggregate glue droplets) of spider orb webs and examine the results obtained. Element distribution images of the aggregate glue droplets were observed by TOF-SIMS. A uniform element distribution is seen for suspended pristine aggregate glue droplets, and a differential spreading of aggregate glue components is seen for attached aggregate glue droplets. We also observed TOF-SIMS images of water in aggregate glue droplets, where water was observed to be consistent with the distribution of oozing salt. We also found that the alkali metal in the aggregate glue droplets showed similar characteristics by feeding cesium carbonate to spiders.
... The reduced food intake of Araneus diadematus in recent years (Table S2) is likely to have negatively impacted the fecundity and survival of this spider [42,43], which in turn may have led to the abundance decline documented in this study (Table 1). Sublethal effects of chemical pollution may have additional negative impacts on this spider's survival [44][45][46][47][48][49]. ...
Aerial web-spinning spiders (including large orb-weavers), as a group, depend almost entirely on flying insects as a food source. The recent widespread loss of flying insects across large parts of western Europe, in terms of both diversity and biomass, can therefore be anticipated to have a drastic negative impact on the survival and abundance of this type of spider. To test the putative importance of such a hitherto neglected trophic cascade, a survey of population densities of the European garden spider Araneus diadematus—a large orb-weaving species—was conducted in the late summer of 2019 at twenty sites in the Swiss midland. The data from this survey were compared with published population densities for this species from the previous century. The study verified the above-mentioned hypothesis that this spider’s present-day overall mean population density has declined alarmingly to densities much lower than can be expected from normal population fluctuations (0.7% of the historical values). Review of other available records suggested that this pattern is widespread and not restricted to this region. In conclusion, the decline of this once so abundant spider in the Swiss midland is evidently revealing a bottom-up trophic cascade in response to the widespread loss of flying insect prey in recent decades.
... Spiders typically produce new orb webs after ingesting and recycling used orb webs. 16,17 We predicted that cesium (Cs), which is also an alkali metal, should also be recycled and reused in this process. ...
Spiders capture prey by applying sticky coating substances to the spiral line of their orb webs. The main constituents of these sticky substances are glycoproteins and salts. This sticky substance is an intelligent material. Salt plays a key role regarding the properties of the sticky substance. Spiders typically weave a new orb webs by recycling used orb webs, and salts, typically salts of the alkali metals sodium and potassium, were therefore assumed to be recycled in this process. Here, we fed cesium (Cs) carbonate (which is an alkali metal salt) to spiders (Araneus ventricosus) to test this hypothesis. After feeding, we mapped the sticky substance in the spiders' orb web using an in‐house time‐of‐flight secondary ion mass spectrometer with high lateral resolution. The results showed that Cs ion was ingested and integrated into the sticky substance, and it showed properties similar to those of sodium ion and potassium ion.
... The reduced food intake of Araneus diadematus in recent years (Table S2) is assumed to have negatively impacted the fecundity and survival of this spider [36,37) which in turn led to the abundance decline documented in this study (Table 1). Sublethal effects of chemical pollution may have additionally negatively affected this spider's survival [38][39][40][41][42][43]. ...
Aerial web-spinning spiders (including large orb-weavers) depend, as a group of insectivores, completely on flying insects as a food source. The recent widespread loss of flying insects across large parts of western Europe, both in terms of diversity and biomass, can therefore be anticipated to have a drastic negative impact on survival and abundance of this type of spiders. To test the putative importance of such a to date neglected trophic cascade, a survey of population densities of the European garden spider Araneus diadematus (a large orb-weaving spider) was conducted in late summer 2019 on twenty sites of the Swiss midland. The data from this survey were compared with published population densities for this species from the previous century. The study verifies above-mentioned hypothesis that this spider's present-day overall mean population density has declined alarmly to densities much lower than can be expected from normal population fluctuations (0.7% of the historical densities). Review of other available records suggests this pattern is widespread and not restricted to this region. In conclusion, the here documented abundance decline of this once so abundant spider in the Swiss midland is evidently revealing a bottom-up trophic cascade in response to the widespread loss of flying insect prey in recent decades.
... For rappelling, spiders must produce an "anchor-rope" system that allows the safe descent from elevated spots 38 . Silk secretion and spinning are easily disrupted by biocides as shown by numerous authors when evaluating the size and/or design of webs produced by orb weavers [18][19][20][21][22][23]39 . In orb-weavers, the effects of neonicotinoids include the down-regulation of silk strength, toughness, and extensibility, the alteration of mechanical properties, structure, and amino acid composition, Figure 3. Effects of treatments with neonicotinoid insecticides on the ballooning activity of Oedothorax apicatus (a,b) and Phylloneta impressa (c,d) after 1 h and 24 h post-exposure periods. ...
Agroecosystems are subject to regular disturbances that cause extinction or migration of much of their fauna, followed by recolonization from surrounding refuges. In small-sized aeronaut spiders, such recolonization is potentiated by their ability to rappel and balloon. These are complex behaviors that we hypothesized to be affected by neurotoxins, namely, neonicotinoids. We tested this hypothesis using two common farmland spider species, Oedothorax apicatus (Linyphiidae) and Phylloneta impressa (Theridiidae). The spiders were topically exposed by dorsal wet application or tarsal dry exposure to commercial neonicotinoid formulations Actara 25 WG, Biscaya 240 OD, Mospilan 20 SP and Confidor 200 OD at concentrations that are recommended for application in agriculture. Contact exposure to neonicotinoids suppressed the ability of spiders to produce the major ampullate fiber and anchor it to the substratum by piriform fibrils. Contact exposure to neonicotinoids also suppressed the ballooning behavior that was manifested by climbing to elevated places, adopting a tiptoe position and producing silk gossamer in the wind. Impaired ability of affected common farmland spiders to quickly recolonize disturbed agroecosystems by silk-mediated dispersal may explain their decline in multiple farmland ecosystems, in which neonicotinoids are applied.
Debates over the ecological and public health impacts of aerial pesticide sprays are increasing. This is particularly true for controlling Monochamus beetles, which are vector insects of pinewood nematodes. In 2017, adult female orb-web spiders, Trichonephila clavata, were sampled from pine forests in Yangsan-si, Gyeongsangnam-do, Korea, where the aerial pesticide spray, fenitrothion or thiacloprid, was used for several decades. The biological traits of the spiders (body weight, body length, carapace width, and total hind leg length) were compared among treatment sites (no-spray, sprayed three times, and sprayed five times), and differences were observed. The body length, carapace width, and total hind leg length of the spiders in the sprayed areas were significantly shorter than in the no-spray area, but there were no differences between the area sprayed three or five times. These results indicate that repeated exposures to an aerial pesticide spray can alter morphological parameters, which influences population-level fitness. Future studies should monitor the spider long-term responses to pesticides (a direct effect) and prey availability (an indirect effect). This is an Open-Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Two toxic and bitter-tasting cardenolides (cardiac-active steroids) were sequestered by the brightly colored oleander aphid,Aphis nerii B. de F., from the neotropical milkweed host plantAsclepias curassavica L. After feeding on milkweed-reared aphids, the orb-web spiderZygiella x-notata (Clerck) built severely disrupted webs and attacked fewer nontoxic, control aphids, whereas the webs of spiders fed only nontoxic aphids remained intact. The regularity and size of the prey-trapping area of webs were reduced significantly in proportion to the amount of toxic aphids eaten. The effects of toxic aphids on spider web structure were mimicked by feeding spiders the bitter-tasting cardenolide digitoxin, a cardenolide with similar steroidal structure and pharmacological activity to the two aphid cardenolides. These results show that the well-known effects of psychoactive drugs on spider web structure are more than interesting behavioral assays of drag activity. Similar effects, produced by plant-derived chemicals in the spider's aphid prey, are relevant to the ecology and evolution of interactions between prey defense and predator foraging.
Methods have been developed for rearing Oedothorax apicatus (Aranaea, Erigonidae) and for testing of the initial toxicity of residues of pesticides to spiders of this and related species (Erigonidae, Linyphiidae) according to IOBC/WPRS standards. Deltamethrin, fenitrothion and maneb appeared to be harmless to moderately harmful to males and females of O. apicatus in a preliminary initial toxicity test using this method.
Methode zur Bestimmung der Toxizität von Pestiziden auf Spinnen der Familien Erigonidae und Linyphiidae
Entsprechend den Richtlinien der IOBC/WPRS wurden eine Zuchtmethode für Oedothorax apicatus und ein Verfahren zur Prüfung der Anfangstoxizität von Pestizidrückständen auf diese und verwandte Spinnenarten (Erigonidae, Linyphiidae) entwickelt. Deltamethrin, Fenitrothion und Maneb, die nach diesem Verfahren getestet wurden, erwiesen sich als schonend bis mittelstark schädigend (nach der Bewertungsskala der IOBC/WPRS) für Männchen und Weibchen von O. apicatus.
The life history of any animal is greatly influenced by three factors (Stearns 1976): the need to grow and reach maturity, the need to feed in order to accumulate the energy necessary for growth, and finally, the need to reproduce. Reproduction is often seasonal, and often the reproductive success depends greatly on body size and physical fitness (Thornhill and Alcock 1983). Hence, the effectiveness of foraging, the efficiency of growth and the timing of maturation all directly affect reproductive fitness. Accordingly, we would expect natural selection to have sharpened the animal’s process of making optimal decisions regarding foraging and growth.
In Quebec commercial apple orchards, spider populations are shown to have been depressed numerically by current pest management practices. Hunting species appeared to be more sensitive to insecticides than web-building species. There were large differences in spider distribution among orchards and years, although some consistent patterns were observed. Specimens from the following families were captured: Theridiidae, Linyphiidae, Lycosidae, Araneidae, Erigonidae, Clubionidae, Tetragnathidae, Dictynidae, Salticidae, Philodromidae, and Thomisidae. In orchards treated only for scab control or with only a single insecticide application for apple maggot control, spiders attained their maximal numbers in August. With two treatments for apple maggot control, spiders attained their maximal numbers towards the end of September.
In spite of the large number of studies about the ecology of spiders carried out in the last two decades in different types of ecosystems all over the world, the significance of these animals as natural control agents is still largely unknown. In this paper the literature about that subject is reviewed. Totally 300 scientific papers, published between 1920 and 1984, are cited here.
Several European and American studies have provided evidence, that in undisturbed grassland ecosystems and forest ecosystems spiders can play an important ecological role as predators of insects and other invertebrates. Also in orchards, not treated with pesticides, that are to a certain degree comparable with forest ecosystems, spiders can be abundant predators.
In contrast to that, the opinion about the predatory importance of spiders inhabiting cultivated fields is controversial. The results of some European studies indicate, that the foliage‐dwelling spiders of cultivated fields, because of their low population densities, are of minor importance as predators of insects. Other European studies show, that the ground‐dwelling spiders of cultivated fields are concerning their abundance a dominant predator group, those significance as control agents still is largely unknown up to the present. In rice fields (swamp ecosystems) in Asia, receiving little or no pesticides, as well as in European and American swamp ecosystems, spiders may be an important predator group.
In houses in South Africa spiders were used successfully as biological control agents against flies.
Zusammenfassung
Spinnen in der natürlichen und biologischen Schädlingsbekämpfung: Ein Literaturüberblick
Weltweit wurden in den letzten 20 Jahren in verschiedenen Ökosystem‐Typen zahlreiche Studien über die ökologische Bedeutung der Spinnen als Prädatoren durchgeführt. Trotz der großen Zahl durchgeführter spinnenökologischer Studien ist die Funktion der Spinnen als Prädatoren von Insekten und anderen Invertebraten heute noch weitgehend ungeklärt. In vorliegender Arbeit wird die Literatur über dieses Thema (insgesamt sind 300 wissenschaftliche Arbeiten, die zwischen 1920 und 1984 über dieses Thema publiziert wurden, aufgeführt) analysiert.
Mehrere europäische und amerikanische Studien haben gezeigt, daß Spinnen in unbewirtschafteten Grasland‐Ökosystemen und Forst‐Ökosystemen eine große ökologische Bedeutung als Prädatoren von Insekten haben können. Auch in ungespritzten Obstanlagen, die man bis zu einem gewissen Grad mit Forst‐Ökosystemen vergleichen kann, stellen Spinnen manchmal eine häufige Prädatorengruppe dar. Im Gegensatz dazu ist die ökologische Bedeutung der in Kulturfeldern lebenden Spinnen als Insektenvertilger noch weitgehend umstritten. Einige europäische Studien deuten darauf hin, daß den in der Vegetationsschicht von Kulturfeldern lebenden Spinnen ihrer niedrigen Populationsdichten wegen wahrscheinlich keine große Bedeutung als Prädatoren von Insekten zukommt. Aus anderen europäischen Studien geht hervor, daß die epigäischen Spinnen der Kulturfelder bezüglich ihrer Abundanz eine dominante Prädatorengruppe darstellen, deren Funktion als Kleinräuber allerdings noch weitgehend unbekannt ist. In asiatischen Reisfeldern, die nicht oder wenig mit Pestiziden behandelt wurden, können Spinnen eine wichtige Bedeutung als Prädatoren von Schädlingen haben. Reisfelder sind Sumpf Ökosysteme; auch in europäischen und amerikanischen Sumpfökosystemen können Spinnen eine abundante Prädatorengruppe darstellen.
In Südafrika wurden Spinnen erfolgreich bei der biologischen Bekämpfung von Fliegen in Häusern eingesetzt.
Interspecific competition between two orb-weaving spiders, Metepeira grinnelli (Coolidge) and Cyclosa turbinata (Walckenaer), was investigated by selective removal of the predators. The estimated predation rate of small prey was higher where Cyclosa was alone than where both species were present, because when Metepeira was removed the density of Cyclosa became higher than the combined density of Metepeira and Cyclosa where both species were present and because the consumption rate of small prey by Metepeira was very low compared with that of Cyclosa. The study suggests that, in some circumstances, a subset of predator species could be more effective in reducing prey populations than the entire natural guild.
THE orb web of the garden spider Araneus diadematus, like those of other ecribellate orb spiders, relies on the remarkable extensibility of its sticky capture spiral to intercept and entrap prey1,2. The spiral strands consist of core fibres and an all-enveloping aqueous coat, which forms into a pattern of droplets3. The core fibres are paired and probably made of typical spider silk4,5. The aqueous solution droplets are more or less evenly spaced6 and are required to allow the special mode of extension of the fibres3,7. Knowledge of the chemical composition and general physical properties of this liquid phase is necessary to understand its function in web mechanics and prey capture8. We have now investigated the chemical composition of this aqueous solution and found the droplets to be a concentrated solution of hygroscopic substances related to neurotransmitters. We offer an explanation as to the function and origin of this solution.
Nephila clavipes inhabiting adjacent habitats showed differences in rate and ratio of growth. Spiders inside the forest fed less, grew slower and stayed smaller than those at the forest edge, a richer environment. The mortality rate in this habitat was about 1% per day, the mortality of vagrant males was even higher. Experimentally fed spiders did not shift their webs readily, even starving individuals stayed much longer than expected. The spiders avoided frequent moves and in a poor site grew more slowly and in smaller size increments. It seems that the costs of small adult size are less than the risks of active foraging.