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Review

Effects of Agricultural Pesticides on Decline in Insect Species and Individual Numbers

1
Crop Protection Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Republic of Korea
2
CSIR-Savanna Agricultural Research Institute, Tamale P.O. Box 52, Ghana
3
Toxicity and Risk Assessment Division, National Institute of Agricultural Sciences, Rural Development Administration, Wanju 55365, Republic of Korea
4
International Technology Cooperation Center, Rural Development Administration, Jeonju 54875, Republic of Korea
*
Author to whom correspondence should be addressed.
Environments 2024, 11(8), 182; https://doi.org/10.3390/environments11080182
Submission received: 23 June 2024 / Revised: 12 August 2024 / Accepted: 16 August 2024 / Published: 21 August 2024

Abstract

:
As agricultural production increases, the use of chemical fertilisers, herbicides, and other synthetic pesticides has equally increased over the years. Inadequate pesticide application description and monitoring has generated a heated debate among governmental organisations, agricultural industries, and conservation organisations about pesticide effects on insect species richness and abundance. This review is therefore aimed at summarizing the decline in insects’ species and individual numbers as a result of extensive pesticide utilisation and recommends possible management strategies for its mitigation. This review revealed an average pesticide application of 1.58 kg per ha per year, 0.37 kg per person per year, and 0.79 kg per USD 1000 per year. Insects have experienced a greater species abundance decline than birds, plants, and other organisms, which could pose a significant challenge to global ecosystem management. Although other factors such as urbanisation, deforestation, monoculture, and industrialisation may have contributed to the decline in insect species, the extensive application of agro-chemicals appears to cause the most serious threat. Therefore, the development of sustainable and environmentally friendly management strategies is critical for mitigating insect species’ decline.

1. Introduction

Agricultural production has been under tremendous pressure in recent years to meet the demands of the increasing population growth, globally [1]. The current global population of 8.1 billion, for example, is expected to reach over 9.7 billion by 2050 [2]. As the population grows, so does agricultural production, leading to extensive pesticide trade and application. In 2020, the total pesticide trade reached approximately 7.2 million tonnes of formulated products, with a value of USD 41.1 billion [3]. Farmers are compelled to transition from subsistence farming to large-scale commercial farming. Agricultural production increased in Europe, North America, South America, Africa, and Asia during the twentieth century [4]. As agricultural production increases, the use of pesticides such as herbicides, insecticides, and other agro-chemicals also increases [1,5]. These chemicals are used extensively in agricultural production at both the subsistence and commercial levels around the world [6]. Extensive and indiscriminate pesticide application on a commercial scale affects insect species abundance and non-target organisms by interfering with their growth, development, behaviour, and other metabolic and physiological processes [7]. Some pesticides have been linked to a potential decline in insect species and non-target insects foraging on sprayed crops [8]. The indiscriminate use of pesticides also has a significant impact on microorganisms [9], plants [10], invertebrates [11], amphibians [12], birds [13], and some mammals [14].
Although encroachment on natural habitats has been blamed for insects’ species decline, the widespread use of pesticides in agricultural production has been identified as the primary cause of the overall loss of insect species and individual numbers [8]. A previous study found a 76% decline in the population of flying insects and a 78% decline in the number of ground-foraging arthropods, with higher annual losses [15]. Insect decline appears to be much greater than that observed in birds or plants, which could pose a significant challenge to global ecosystem management. For instance, in 71% of butterfly species in Britain, the total number of individuals has decreased over 20 years, compared to birds (54% over 20 years), and plants species (28% over 20 years) [16]. Inadequate pesticide application description and monitoring has sparked a heated debate among governmental organisations, agricultural industries, and conservation organisations about pesticide effects on organisms. Quantitative information on pesticides’ impact on insect species decline will aid in the implementation of national and international policy objectives, as well as the reversal of current declines. This is vital for the development of safety management techniques for residual chemicals in agro-food and agricultural environments. This review is therefore aimed at summarizing the decline in insects’ species and individual numbers as a result of extensive pesticide utilisation and recommends possible management strategies for its mitigation.

2. Pesticides Usage and Distribution in Agricultural Production

In 2022, the total pesticides used in agriculture was 3.70 million tonnes, representing a 4% increase from 2021, a 13% increase over a decade, and a doubling since 1990 [17]. These pesticides comprise herbicides (47.5%), insecticides (29.5%), fungicides (17.5%), and 5.5% others [17]. Furthermore, 610 chemical compounds containing organochlorin insecticides, which were banned due to resistance and safety concerns, are being replaced with newer chemical products [18]. Although several pesticide products are used, agricultural yield losses are estimated at 37% due to insects (13%), weeds (12%), and diseases [18]. The mode of action of pesticide active ingredients determines their specificity and toxicity, whereas their effectiveness on organisms is largely determined by the dose administered to them. Pesticides such as carbamates, neonicotinoid, organophosphorus, synthetic pyrethroid, and organochlorine are well-known neurotoxins that affect arthropods’ nervous systems. As a result, these products are assumed to disrupt the physiology of terrestrial and aquatic arthropods. Herbicides are among the most toxic pesticides to other organisms, particularly insects, because they disrupt their metabolic and reproductive systems. Fungicides are used to treat fungal infections and can also act as antibiotics against certain fungi. However, organomercurial products are considered neurotoxic and toxic to arthropods in several areas. As a result, the active ingredients in most pesticides affect a wide range of taxonomic groups rather than just the target species [18].
Europe and North America account for one-third and one-quarter of the total market, respectively [19,20]. Overall, herbicides are estimated to comprise half of pesticide applications in North America, followed by insecticides (19%), fungicides (13%), and others (22%). Some countries, such as India and South Africa, continue to use DDT and lindane to control mosquito vectors and tsetse flies as needed [21]. The global distribution of pesticide types varies by crop, with corn, soybean, and cotton having the highest herbicide usage (75% in the United States). Orchards predominantly use insecticides, whereas vineyards and vegetables plantations primarily use fungicides [20]. The average pesticide usage worldwide is estimated to be 4.4 kg/ha per year, with agriculture accounting for roughly one-fifth of the Earth’s land area [5]. As a result, insect diversity and other ecosystem services are severely threatened [20].

3. Global Pesticide Usage per Agricultural Value

A recent survey conducted in 2022 reported that pesticide usage remains constant at 2.7 million tonnes of products and 1.8 kg/ha per area. Pesticide usage per agricultural capita and value were estimated at 0.69 kg/1000 I$ and 0.37 kg/person, respectively. In 2020, the global pesticide trade was expected to be 7.2 million tonnes of formulated products worth USD 41.1 billion [3]. Despite efforts to regulate pesticide use, average pesticide usage increased by 50% over the last decade compared to the 1990s (Table 1). Crop pesticide use in recent decades has increased from 1.2 to 1.8 kg/ha. A survey conducted over the last three decades revealed an average pesticide application of 1.58 kg per ha per year, 0.37 kg per person per year, and 0.79 kg per 1000 I$ per year [3]. A recent survey showed that Asia had the highest pesticide usage of 3.7 million tonnes in 2020, equivalent to a value of USD 16.1 billion. The total average pesticide usage in Asia is estimated to be 0.6 million tonnes per value of agricultural production, 0.17 kg per person per year, 0.47 kg per 1000 I$ (International Dollars) per year, and 1.17 kg per ha per year [3]. Between the 1990s and the most recent decades, pesticide usage in agriculture in Europe increased by just 3%, most likely due to the strict pesticide control by the European Common Agricultural Policy department. The region has the lowest proportion of pesticide usage compared to other regions. In 2020, Europe pesticide usage per area of cropland was estimated at 1.6 kg/ha, below the world average [22,23]. USA applied cropland pesticides at rates of 2.83 kg per ha per year, 1.17 kg per person per year, and 1.43 kg per 1000 I$ per year per value of agricultural production. In particular, the most recent decade saw a higher application of herbicides (360 to 852 kt), fungicides (93 to 177 kt), and insecticides (159 to 181 kt) per year than previous decades [10,23]. Imports of pesticides in Africa are expected to reach 850 kt in 2020, worth USD 3.1 million. Africa uses 32% herbicides, 33% fungicides, 33% bactericides, and 27% insecticides. In the most recent decade, the region used low volumes of pesticides, with estimates of 0.11 tonne per year, 0.41 kg per ha per year on cropland, 0.11 kg per person per year on capita, and 0.42 kg per 1000 I$ per year for agricultural production value [23]. In 2020, USA utilised the most pesticides globally (408 kt), followed by Brazil (377 kt), China (273 kt), Argentina (241 kt), the Russian Federation (91 kt), Canada (79 kt), France (65 kt), Australia (63 kt), India (61 kt), and Italy (57 kt). Moreover, the countries with the highest pesticide usage on cropland in 2020 were Saint Lucia (20 kg/ha), the Maldives (17 kg/ha), Oman (16 kg/ha), Israel (15 kg/ha), Ecuador (14 kg/ha), Seychelles (12 kg/ha), Japan (12 kg/ha), Belize (11 kg/ha), the Netherlands (11 kg/ha), and the Republic of Korea (10 kg/ha). Pesticide usage appears to be more abundant in industrialised regions than in other regions [22,23].

4. Persistence of Residues and Their Bioavailability

Persistence determines how long a toxicant residue can remain on a surface over time. The half-life of persistence is the time it takes for half of the chemical to disappear, which usually occurs when the active ingredient is degraded. Nonetheless, some products, such as endosulfan sulphate, dieldrin, aldicarb sulfoxide, sulfone, and heptachlor epoxide, may remain toxic, affecting species richness and abundance. When some neurotoxic insecticides are applied, they degrade quickly through chemical or biological means. Current pesticides, such as herbicides and fungicides, degrade more easily than previous products, but some of these chemicals are more persistent than insecticides [25]. Presently, it is estimated that 50% of pesticides used have a half-life in either soil or water bodies. Most farmers prefer persistent pesticides because they can remain on plant surfaces for an extended period of time. However, this poses a threat to biodiversity for as long as they remain in the environment. Persistent chemical products with high toxicity, such as ‘old’ OCs, arsenic insecticides, and copper fungicides, may pose a threat. Chemical residues pose a significant threat to species richness and abundance because pesticide degradation rates decrease when compared to assimilation [25]. For instance, the efficacy of glyphosate requires plants to absorb its residues through their leaves or roots when applied [26]. However, if glyphosate is accidentally spread on the ground, it is absorbed into soil particles and may remain active, threatening other species if not absorbed by the plant. Furthermore, chemical residues such as hydrophobic insecticides, systemic and soluble insecticides, and herbicides leach into the top soil, posing a threat to soil-borne organisms, particularly insects [25,26].

5. Impact of Pesticide Application on Insects’ Biodiversity

5.1. Direct Effect

Pesticides are known to be harmful to insects, with direct mortality frequently reported, with non-target insects being the most vulnerable when compared to other insects. These pesticides work directly by disrupting the insect’s nervous system or damaging its exoskeleton, causing paralysis and death. Pesticides affect both insects that migrate to sprayed fields and those present during treatments. Pesticides such as malathion, metamidophos, abamectin, acetamiprid, imidacloprid, and acephate are reported to be toxic to both target and non-target insects [27]. Moreover, the direct effects of metamidophos, cartap, and abamectin were found to cause high mortality among a group of insects [27]. Excessive use of insecticides such as organophores, carbamates, and purethroids also reduced hymenopteran and coleopteran populations, which are known to play an important role in food web and crop protection [28]. According to general scientific consensus, pesticides’ extreme direct impact has resulted in the decline in most beneficial insects and pollinators. For instance, neonicotinoids increased bee and butterfly mortality while reducing their behaviour and survival [29]. Glyphosate exposure caused changes in bees’ gut microbiome, leaving them vulnerable. In the United Kingdom, the direct effects of pesticides reduced butterfly species richness on conventional farms more than on organic farms. Carabid beetles and other non-target insects were more affected by conventional farm management than organic farms [30]. The direct effect of insecticide application affected bugs, wild bees, and moth populations, but not the target pests [30]. In the United Kingdom, organophosphates (42%), carbamates (29%), and pyrethroids (14%) were found to have a direct effect on the species richness and abundance of bees [31]. Pesticides used to control pests in wheat and sunflower fields, such as imidacloprid and clothianidin, resulted in high mortality rates among bumble and wild bees [32]. In France, imidacloprid significantly reduced the diversity of Lepidoptera, bugs, coleopterans, and other species when compared to the target pests [33].

5.1.1. Lepidoptera

Moths and butterflies are known to be vulnerable to habitat loss due to their unique host plant adaptation system [34]. Lepidoptera species are widespread and play important roles in ecosystem services and management [35]. In Belgium, 45 butterfly species declined by nearly 69% as a result of excessive agricultural pesticide use during the twentieth century [36]. In the Netherlands, 11 out of 20 cosmopolitan butterfly species are reported to be declining, while four local species (Lasiommata megera, Gonepteryx rhamni, Aglais io, and Thymelicus lineola) are critically endangered [37]. A corresponding report also showed an 85% decline in 733 moth species, with 38% threatened and 34% susceptible in the Netherlands [38]. In Sweden, a report indicated a drastic decline in (45%), endangerment of (22%), and extinct of (159 species) 269 species [39]. In Finland, farmland species experienced a greater decrease in biodiversity (60%) compared to forest species (40%) [40]. A population study in Spain revealed that 66 butterfly species were declining on farmlands, 15 were increasing, and 5 were stable in forest zones [41]. Out of 576 butterfly species in Europe, 71 are endangered and declining [42]. In comparison, cropland butterflies declined the most (19%), followed by wetlands (15%) and forests (14%). The greater decline observed in cropland butterflies could be attributed to the excessive use of pesticides compared to other habitats. This was confirmed by the observation that 80% of butterfly species have declined as a result of pesticide application [43]. According to extensive data from the United Kingdom, 41 cropland butterfly species are on the decline. This was attributed to agricultural expansion and the excessive use of pesticides and chemical fertilisers. There has been no comprehensive study on the trend of insect biodiversity in the United States. Nonetheless, a few studies revealed unstable species populations in Wisconsin and Iowa’s prairies and bogs. This was the result of climate change and agricultural intensification [44]. In 2012, agricultural intensification and widespread pesticide use reduced 67 butterfly species to 23. In 2010, the southern part of the state experienced an 80% population decline as a result of agricultural intensification and excessive pesticide use [45]. A detailed data base in Asia shows that the populations of butterfly species are threatened (15–20%) and endangered (80%), with two species on the verge of extinction in Japan [46]. A previous report in Malaysia revealed a 19% reduction in the moth population at Mount Kinabalu due to agricultural intensification and pesticide use (Table 2) [47]. In Great Britain, a previous study showed 28% decrease in larger moth total abundance [34]. Burnet moths also decreased from 117 species to 71, with most of them considered highly endangered in Germany [48]. A previous study in the UK showed a two-third decline in widespread and common macro-moths over 35 years of study [49]. The percentage of common macro-moth species showing a significant decrease was higher (54%) than those showing an increase (22%) in the UK [50]. A similar trend of moths’ species abundance and richness decrease has been reported in Scotland (46%) over a 24-year study [51]. A decrease in burnet moths’ total abundance was reported in Great Britain (50%) and Scotland (20%) [51].

5.1.2. Hymenoptera

Hymenopterans, which include ants, bees, wasps, and other insects, provide important ecosystem services. Bees contribute significantly to pollination, aside from their food, industry, and medicinal products [60]. According to studies conducted in Britain, agricultural intensification and widespread pesticide use have resulted in a significant decline in 18 bee species [59]. Reports from Denmark also revealed 12 extinct inherent species, as well as the native Bombus distinguendus, which is currently threatened [61]. In Central Europe, agricultural intensification and widespread pesticide use have resulted in the extinction of 48 out of 60 bee species, 30% of which are endangered [62]. Sweden reported a low crop yield due to insufficient pollination services at Swedish red clover fields, which was associated with a decline in the bee population [62]. Agricultural intensification, chemical fertilisers, and pesticide application have been identified as the primary causes of bee species richness and abundance declines in Sweden [63]. A comparable decline was observed in Europe (46% Bombus species), North America (50% of the 14 bumble bee species), Brazil (63%), Costa Rica (60%) and Finland (23%), China (3–13%), South Africa (29%), and Minnesota (11 stingless bees) as a result of extensive herbicide application [64]. Historical records from 382 geographical areas in the United States show that 3.5 million out of 6.0 million honey bee populations have declined, representing a 0.9% loss per year, which has been attributed to dichlorodiphenyl-trichloroethane (DDT) and other toxic product application for pest management on croplands [65]. The extensive application of DDT, neonicotinoids, and fipronil are reported to impede bee growth and development, particularly queen performance, resulting in reduced diversity [61]. Aside from bees, hymenopterans such as wasps, ants, and parasitoids have experienced significant biodiversity declines (Table 3). Nonetheless, species like B. bimaculatus, B. impatients, and B. rufocinctus have seen population growth in areas where pesticide use is regulated [61]. As a result, widespread pesticide use must be regulated because it has the potential to increase insect biodiversity.

5.1.3. Diptera

Hoverflies (Syrphidae) are well-known predators of most major insect pests and are also efficient pollinators. The diversity of this taxon varies significantly across Mediterranean countries, with 249 species reported in Greece [77] and 429 in Spain [78]. A similar trend of findings has been reported in the Netherlands and the United Kingdom [79]. In the Netherlands, a comprehensive study demonstrated an 80% and 44% hoverfly decrease over a 40-year (1982–2021) and 43-year (1979–2021) period, respectively [80]. Of the 303 species of hoverflies in Denmark, a recent report shows that 19% are threatened, 5 critically endangered, 24 endangered, and 26 vulnerable. Moreover, 18 were considered to have an information deficit, 32 as near threatened, and 10 as regionally extinct [81]. In Germany, a 26-year period study of hoverflies (1989–2014) showed 23% decreases in species richness [82]. A recent study from 2008 to 2022 also showed a declining trend in 147 types of hoverflies, compared to an increasing trend in 146 [82]. Although the decline was attributed to the degradation of tree features, loss of diverse habitat, and degradation of small water bodies, extensive pesticide application was considered the most threatening factor, as it causes direct mortality and reduces hoverflies’ fitness. Pesticides were reported to destabilise trophic service, hence affecting hoverflies indirectly [81,83].

5.1.4. Coleoptera

Coleopterans are biological pest control insects that play a significant role in ecosystem resilience [84]. They also play a significant role in the health of natural and human-modified ecosystems, such as nutrient cycling, seed dispersal, reducing livestock parasites, and promoting plant growth. [85]. The main causes of their biodiversity decline are agricultural intensification and pesticide use. A previous study found that carabids (34%) and xerophilic beetles (50%) were on the decline in Belgium, Denmark, and the Netherlands [86]. Of the 68 carabid species in the United Kingdom, a detailed survey shows 49 in decline, 26 endangered, 8 threatened, and 19 stable. This decline was attributed to urbanisation, agricultural intensification, and extensive pesticide use [70]. According to historical data, 12 species of carabid beetles are threatened in New Zealand, and ladybirds have declined by 68% in the United States and Canada [87]. Studies on the trend of coleopteran species showed a decline in six species in the Czech Republic [88], 19 dung beetle species in the Mediterranean regions of Europe [89], 9 species in Spain [90], 31% dung beetles in Italy [91], 9 Scarabaeidae in France [92], and saproxylic beetles in Europe [93]. Agricultural intensification, urbanisation, wood harvesting, and extensive pesticide application were reported as the main drivers of the decline [89].

5.1.5. Hemiptera

Hemipterans constitute one of the largest insect orders and are the largest among the hemimetabolous insects [77]. At the same study location, a comparative analysis was conducted between two time periods (1963–1967 and 2008–2010). This was investigated to determine the trend of hemipterans’ biodiversity, species abundance, and composition. The findings revealed that species biodiversity did not vary significantly, despite some variation in climatic conditions and population abundance. Nonetheless, 14 species declined, while 9 others increased. During the 47-year period, the population decreased from 679 to 231 individuals per site, representing a 66% median population decrease [78]. The decrease in species richness, abundance, and distribution was linked to soil acidification and extensive pesticide use [79].

5.1.6. Orthoptera

A long-term study in Germany on grasshopper and cricket species biodiversity found small variations in species populations and unstable species richness over four decades [94]. Moreover, the study found that the population of bare soil grasshoppers (Myrmeleotettix maculatus) decreased while Tettigonia viridissima and Phaneroptera falcate species increased slightly. In Germany, only a few species were observed to be declining; however, 50% were highly threatened and vulnerable [90].

5.1.7. Odonata

These are small insect taxa that make a significant contribution to biological pest control and nuisance mosquito management [90]. A previous study found that 118 aquatic insect species were threatened, with Odonata species accounting for 90% [72]. A long-term comprehensive study found that 52 species of dragonflies and damselflies are declining in the United States, 15% of Odonata species are endangered, with two species of damselflies and dragonflies being highly vulnerable to extinction in Europe, and 57 Odonata species are declining in Japan [95].

5.2. Indirect Effects

Toxicants show indirect effects when other organisms become susceptible to the pesticides’ active ingredients. Pesticides’ indirect effects could be considered as side effects that influence the ecological structure of the affected species rather than the specific mode of action of the various chemicals. Diverse individual toxicants may also have adverse effects on species diversity and their interactions in the ecosystem [96]. Several studies show that most of the pesticides used in agriculture contribute significantly to the decline in insect biodiversity due to side effects on non-target species [5]. Although efforts have been made to classify each type of pesticide and its target organisms, such as birds, plants, insects, and other arthropods, the indirect effects of these pesticides on trophic-level interactions among diverse groups of organisms have not been addressed. For example, some herbicides that were approved through risk assessment for their safety to the environment and other organisms were later discovered to reduce non-target plants that provide food for pollinators and other beneficial insects. As a result, the trophic interactions that underpin biodiversity could be depleted [97].

5.2.1. Herbicides’ Indirect Effects

Herbicides and weed management destroy insect host plants, threatening their survival and development [98]. Insects within cultivated fields are reported to be vulnerable to herbicide drift due to the long half-life of these herbicides in the soil [98]. Several studies confirmed the reduction in insect populations as a result of extensive herbicide side effects on host plant populations [99]. This eliminates pollen, nectar, shelter, plant hosts, and pollinator and other insect nesting sites [100,101]. The synergistic effects of 2,4-Dichlorophenoxyacetic acid and other biological agents reduced the insect population due to a higher insecticide lethal dose than what was required for the target weed [102]. Most herbicides are not acutely toxic to other organisms; however, some, such as TCA-sodium, monuron, triazine, and dinitroaniline, have been reported to have an indirect effect on insect biodiversity at higher doses. Dichlobenil (10%) reduced the aphid reproductive rate and population abundance, while 54% of some selected herbicides affected parasitic wasp populations [103]. The antifeedant constituents of simaxine and pronamide inhibited the growth of several phytoghagous insect pests [103]. In Europe, excessive herbicide use has resulted in a decline in insects and other weed species [104]. The synergistic effect of glyphosate and 2, 4-D reduced cricket, ground beetle, and mite populations, while atrazine reduced springtail abundance [105]. Some herbicides may contain little or no direct effect on insects; however, paraquat and terbacil decreased wasp, predatory, and parasitoid species, which indirectly influenced other insect species populations [105]. Previous studies also attributed the decline in carabid beetles to the reduction in food and cover due to herbicide application [104]. It appears that modifying the ecological composition affects the diversity of several insects. Weed control could also indirectly affect insects’ larvae, egg-laying, or larval survival [104]. In UK, herbicides’ indirect effects are considered a major driver of butterfly and bee decline. An investigation on cereal fields treated with fungicides, herbicides, and insecticides found 13 fewer butterfly species than the 270 on unsprayed fields [105]. In America, the use of genetically modified glyphosate-tolerant corn and glyphosate caused a decline in milkweeds, which consequently led to a decline in the monarch butterfly population [105].

5.2.2. Insecticides’ Indirect Effects

Poisoning of Non-Target Insects

Studies have shown a decline in target insect pests and non-target insects as a result of insecticide application. This is because predatory insects may suffer secondary intoxication while feeding on prey that was contaminated with pesticides while still alive. For instance, the spined soldier bug (Podisus maculiventris) population was reduced by feeding on diamond moths in a cabbage field treated with imidacloprid [106]. Laboratory and field experimental findings confirmed the poisoning of non-target insects. The lacewing population was reduced when feeding on bollworm larvae treated with azadirachtin [107]. Other experiments also showed a reduction in lacewing lavae when fed lettuce aphids that had been treated with imidacloprid insecticides [67]. Both field and laboratory experiments also showed a high mortality of the ladybug, Cycloneda sanguinea, which fed on aphids treated with thiamethoxam, whereas Pterostichus madidus, Nebria brevicollis, and P. melanurius showed significant mortality when feeding on aphids [108]. This is an indication that non-target insects are vulnerable when exposed to poisoned or contaminated preys. Wasp populations were reduced when their larvae fed on an insecticide-sprayed field. Some of these insecticides affect insects’ eggs and larvae rather than their adults [108]. The population of non-target mycophagous insects including the ladybeetle, Phyllobora vigintimaculata, declined when feeding on plant tissues contaminated with fungi and insecticides. These ladybugs were indirectly poisoned by pathogenic fungi, which grew on treated plants, acting as reservoirs of the applied insecticides. Insects such as the predatory bug, Orius insidious, and lacewing, Chrysoperla carnea, were affected indirectly by insecticides when feeding on plant sap and extra-floral nectar contaminated with systemic insecticides [109].

Pathogens in Insect Pollinators

Research shows that extensive and consistent application of insecticides stimulates the incidence of viral diseases and pathogens among insect pollinators. For instance, honey bees that fed on a neonicotinoid- and fipronil-treated field experienced higher pathogen infestation, reducing their population [110]. A variety of insecticide residues are found in flowers, crops, weeds, and trees. Insects that feed on the pollen or nectar of these flowers stimulate detoxifying enzymes in response to the ingested sublethal dose, stressing them [111]. The detoxification mechanism is known to weaken their immune system, leaving them vulnerable to pathogens, parasites, and diseases [88,89]. A previous report showed a significant increase in microsporidian gut parasite Nosema infection in honey bees, Apis mellifera, when exposed, to sublethal effect [112]. However, the indirect effect of insecticides is reported to be highly dependent on the insect species and type of chemical [113]. For instance, the application of imidacloprid did not show sublethal effects on bumble bee gut microbiome [93]. Honey bees that fed on a thaiamethoxam-treated field had significantly higher mite Varroa sp. and pathogen loads compared to those feeding on the untreated fields, reducing their population [114]. Neocotinoid acetamiprid- treated fields of blueberries increased their vulnerability to pathogens and diseases, which eventually declined their population [115]. In East Anglia, a significantly higher prevalence of Microsporidia parasites in leaf-cutter bees, Megachile sp., was observed when they fed on insecticide-treated fields compared to the untreated fields [116]. A report on fungicides also showed a direct effect on fungivorous mites, yet they indirectly reduced the population of predatory mites by exposing them to fungal pathogens [117].

6. Ban on Harmful Pesticides and Alternative Techniques for Agricultural Production

Pesticides pose significant threats to the environment, harming non-target species and threatening biodiversity [118,119]. This has raised a major concern among United Nations agencies and international communities [120]. Banning hazardous pesticides can help to recover insect biodiversity and improve ecosystem services [121]. Although concerns about the potential impact of pesticides on crop yields are raised, previous research in India has shown that sustainable agricultural production strategies, such as integrated pest management and agroecology, significantly increased yield compared to conventional farming strategies [121]. Following the previous national ban of 16 pesticides in 2018, the India national government proposed a ban on 27 pesticides in 2020 [122]. Kerala banned 14 highly hazardous pesticides in 2011, following the 2005 ban on organochlorine insecticides and endosulfan [123]. These efforts demonstrated the potential for safer and more sustainable agricultural practices, which would reduce pesticide threats to plant and insect biodiversity [124]. Moreover, the ban of harmful pesticides in Srilanka [125], India [126], Taiwan [126], Bangladesh [127], and South Korea [128] increased plant and pollinator species richness. Other studies showed that organic farming had five times higher plant biodiversity and 20 times higher insect species richness compared to conventional fields [129]. The EU banned pesticides classified as mutagens, carcinogens, reproductive toxicants, or endocrine disruptors [130]. Similarly, China banned highly hazardous pesticides and revised certain pesticide use regulations for both sellers and users [131]. The Chinese Ministry of Agriculture banned 50 pesticides and further proposed restricting another 30 pesticides [132]. The Brazilian Ministry of Agriculture (MOA), Health Regulatory Agency, and Ministry of Environment incorporated a more protective hazard assessment to ban teratogenic, hormone disrupting, and mutagenic pesticides [133]. Although multiple factors have limited the effectiveness of this regulation, the Brazilian Ministry of Agriculture (MOA) and Health Regulatory Agency managed to ban some pesticides that threaten ecosystem services and the environment [134]. It is recommended that using safer formulations or natural farming strategies could significantly minimise the adverse effects of pesticides on biodiversity [135].

7. Insect Biodiversity Decline and Its Contributing Factors

The decline in insect populations poses a threat to the United Nations Sustainable Development Goal of conserving natural populations and preventing extinctions [136]. Available data indicate a widespread decline in insect biodiversity [124]. For instance, a 50% decline in European grassland butterfly individual numbers was reported in 2011 [124]. Similar trends are observed in well-studied insect groups such as bees and moths. However, anthropogenic modification of global landscapes is presently contributing to insect population decline [137,138], with reduced diversity threatening the sustainability of ecosystem services provided by insects [139]. Climate change, habitat destruction, habitat fragmentation, deterioration of habitat quality, invasive species, pesticide use, and pollution are all contributing to the global biodiversity decline [140]. However, a pan-European long-term study on plant and insect biodiversity identified pesticide use as a major factor in insect species decline [141]. These factors endanger the sustainability of ecosystem services, necessitating immediate action to address these threats and protect insect populations [142]. The combination of these factors leads to habitat loss and degradation, eventually driving insect populations towards decline and extinction [143]. For instance, the blowfly species Neta chilensis may have become extinct due to the cumulative effects of multiple stressors [144]. To effectively conserve insects, policies must consider the synergistic effects of these threats. In the Northern Hemisphere, particularly in Europe, changes in insect populations’ diversity and abundance have raised concerns about a potential global trend [145]. Geographical areas such as Brazil’s Cerrado and Atlantic forests, the Caribbean, Central Chile, and Mesoamerica are considered crucial biodiversity hotspots, due to pesticide use and several other factors [146].

8. Sustainable Management Strategies to Safeguard Insect Biodiversity Declines

The findings of this review have confirmed that extensive use of pesticides has significantly contributed to the decline in insect biodiversity, despite the fact that pesticides play an important role in crop protection. Pesticide applications endanger farmers’ health and destabilise the ecosystem by reducing insect biodiversity [73]. In general, biodiversity is a key driver of ecosystem services, which lead to sustainable agricultural management, and thus it must be protected for current and future generations [147]. Although some studies attribute insect biodiversity decline to urbanisation as a result of the increasing global population, the current review clearly shows that the main threat is the wide range of pesticide application due to extensive agricultural production [148]. Therefore, the development of sustainable and environmentally friendly management strategies is critical for mitigating insect biodiversity decline. The approach to conserve insects’ biodiversity involves the enforcement of government policies, sustainable farming practices, and crop heterogeneity.

8.1. Organic Agriculture and Integrated Pest Management Strategies

Researchers have explored alternative farming methods to reduce pesticide use while increasing insect species abundance and richness. Organic farming is regarded as a promising alternative, with studies indicating that it can increase species richness by approximately 34% and abundance by around 50% [149]. Organic farming promotes biodiversity by increasing the abundance and variety of plant and insect species [30]. This, in turn, can lead to enhanced biological control, as more predators can help regulate pest populations [150]. A comparison of arthropod populations in various farming systems showed that organic farming had the highest relative density over three seasons. Similarly, a study in Thailand discovered that organic rice fields supported a diverse range of insect species, with a higher proportion of natural enemies (23 species) than pest species (11 species), highlighting organic farming’s potential to promote ecological balance [151]. A previous study found that organic fields had a higher relative insect density than conventional fields, indicating potential pesticide-related effects. Moreover, organic farming practices produced the highest Shannon–Wiener index, indicating greater biodiversity [152]. Other studies have found that organic fields promote greater insect richness and abundance [152], whereas pesticide applications can harm certain species, such as spiders and dragonflies [153,154]. Meyling et al. [155] discovered that organic vegetable farming supported a greater diversity of natural enemies. This suggests that reducing pesticide use may increase insect species abundance in open-field ecosystems. Similarly, Reddy and Giraddi [156] discovered that pesticide use patterns influenced insect pest biodiversity in vegetable fields, including cabbage, with the Simpson index higher in sprayed fields compared to unsprayed fields. Cutworms and P. xylostella were found to have higher relative densities in cabbage ecosystems, highlighting the effects of pesticide use on insect biodiversity. According to studies on rice and cabbage production systems, organic farming or minimal chemical use (IPM) leads to increased biodiversity [157]. Also, organic rice fields showed increased complexity and changes in community structure under various management practices. This suggests that organic farming has the potential to preserve biodiversity, ecosystem services, and effectively manage pests [152]. As a result, reducing or eliminating chemical use in fields can improve agro-ecosystem diversity while offsetting potential trade-offs and losses and mitigating the environmental damage caused by indiscriminate pesticide application in agriculture.

8.2. Sustainable Farming Practices

Ecological restoration is required to improve habitat connectivity when a degraded ecosystem is unable to restore itself [158]. Sustainable agricultural production plays a major role in biodiversity management and conservation. Result-Oriented Measures that focus on biodiversity fluctuations caused by farmers’ management practices have been established, targeting biodiversity restoration [159]. Agricultural sustainability, coupled with innovative technologies, could ensure consistent ecosystem service resilience. This strategy could also contribute to global food security for both the present and future generations [159]. Farmers are expected to increase output while protecting natural resources, biodiversity habitats, and the environment. Unfortunately, a recent survey found that most farmers are unaware of timely insect pest infestations and thus use a variety of management techniques, including indiscriminate pesticide application, which kills non-target insects [1]. These practices disrupt ecosystem services, potentially resulting in a decline in insect biodiversity and the spread of other pests. Thus, crop rotations, intercropping, agroforestry, reduced tillage, and proper pesticide application rates are recommended as ways to ensure sustainable agriculture and stable insect biodiversity. Moreover, strategic development of integrated pest management could reduce the extensive use of toxic pesticides [160].

8.3. Crop Heterogeneity

Mix cropping systems are beneficial to agriculture and biodiversity management, therefore farmers need to be motivated to implement them [161]. Higher biodiversity of insects and other arthropods was reported in crop genetic diversity fields. This was attributed to diverse range of food sources and crop heterogeneity structure. Therefore, strategic implementation of multiple cropping and crop rotation systems could support to sustain insect biodiversity [161]. Landscape conservation, crop rotation, minimal pesticides application, mix cropping, intercropping, and others are among the proposed environmental agricultural practices for biodiversity conservation includes [162].

9. Conclusions

This comprehensive review reveals that insects face greater diversity decline within a few decades unless farmers adopt new sustainable agricultural strategies. Although other factors such as urbanisation, deforestation, monoculture, and industrialisation may have contributed to the decline in insect species, extensive pesticide usage appears to be the most serious threat. Apparently, protecting threatened species in natural reserves does not guarantee their survival, as indiscriminate pesticide use and agricultural intensification continue to rise. This is due to most farmers’ desire to meet the global food demand as the population grows, so they ignore the risks of pesticides’ effects on human health and non-target insects [160]. To mitigate species richness loss, habitat conservation and restoration combined with a significant reduction in agrochemical use in intensive agriculture areas must be prioritised globally. Apparently, excessive application of pesticides does not increase yield and instead contributes to pest resistance, endangers farmer’s and consumer’s lives, and leads to insects’ species decline. Over time, the development of integrated pest management (IPM) in Europe and developing African and Asian countries has increased crop yields. Therefore, developing safety management techniques for residual chemicals in agro-food and agricultural environments, guided by integrated pest and weed management approaches, is the most effective way to increase insect species richness and abundance.

Author Contributions

Conceptualization, P.Q.; writing—original draft preparation, P.Q.; writing—review and editing, P.Q., L.K., M.K., K.L., F.K., and I.-h.J.; funding acquisition, I.-h.J.; supervision I.-h.J. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the research project of Rural Development Administration, Investigation of insecticide resistance to major crop pests (RS-2022-RD010420).

Acknowledgments

We show appreciation to the Korea–Africa food and Agriculture Cooperation Initiative (KAFACI), National Institute of Agricultural Sciences (NAS), and Rural Development Administration (RDA) for their support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Pesticides used by region and category. Source: [24].
Table 1. Pesticides used by region and category. Source: [24].
HerbicidesFungicidesInsecticidesOthers
Africa30503010
America60102010
Asia40304010
Europe39451015
Oceania6010205
Table 2. Proportion of declining and threatened species per taxa according to IUCN criteria.
Table 2. Proportion of declining and threatened species per taxa according to IUCN criteria.
Insect TaxonDeclining (%)Threatened (%)Reference
Coleoptera4934[52]
Diptera250.7[53]
Ephemeroptera3727[54]
Hemiptera8n.a[55]
Hymenoptera4644[56]
Lepidoptera5334[16]
Odonata3713[57]
Orthoptera49n.a[58]
Plecoptera3529[59]
Trichoptera6863[53]
Table 3. Insects’ species status of some insects’ taxa and their geographical locations.
Table 3. Insects’ species status of some insects’ taxa and their geographical locations.
TaxonAbundanceDeclineLocationReference
Hymenoptera
Bumble bees18 species7 speciesEngland[66]
Bumble bees14 species8 speciesCanada[64]
Bumble bees60 species48 speciesCentral Europe[67]
Honey bees6 m colonies3.5 m coloniesUSA[68]
Wild bees 52% populationBritain[69]
Wild bees 67% populationNetherlands[70]
Wild bees 32% populationNorth America[68]
Cuckoo wasps 23% populationFinland[70]
Stingless bees30 species11 speciesUSA[71]
Orchid bees24 species64% speciesBrazil[68]
Parasitic wasps48 species23% speciesFinland[70]
Coleoptera
Ground beetles419 species34% speciesBelgium, Denmark[72]
Ground beetles49 species16% speciesUK[51]
Ladybird beetles 68% speciesUSA[72]
Dung beetles 31% populationItaly[73]
Saproxylic beetles436 species57% speciesEurope[70]
Odonata
Dragonflies52 species65% populationUSA[71]
Odonata species200 species57 speciesJapan[72]
Odonata species155 species13 speciesSouth Africa[73]
Plecoptera
Stoneflies14 species5 speciesCzech Republic[74]
Stoneflies77 species29% speciesUSA[75]
Ephemeroptera
Mayflies107 species43% speciesCzech Republic[76]
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Quandahor, P.; Kim, L.; Kim, M.; Lee, K.; Kusi, F.; Jeong, I.-h. Effects of Agricultural Pesticides on Decline in Insect Species and Individual Numbers. Environments 2024, 11, 182. https://doi.org/10.3390/environments11080182

AMA Style

Quandahor P, Kim L, Kim M, Lee K, Kusi F, Jeong I-h. Effects of Agricultural Pesticides on Decline in Insect Species and Individual Numbers. Environments. 2024; 11(8):182. https://doi.org/10.3390/environments11080182

Chicago/Turabian Style

Quandahor, Peter, Leesun Kim, Minju Kim, Keunpyo Lee, Francis Kusi, and In-hong Jeong. 2024. "Effects of Agricultural Pesticides on Decline in Insect Species and Individual Numbers" Environments 11, no. 8: 182. https://doi.org/10.3390/environments11080182

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