As bee populations are dramatically declining worldwide, fipronil has proven to be toxic for bees when they are exposed to the residual concentrations in the pollen and nectar of fipronil- treated plants (Holder et al., 2018). Unlike other pesticides, fipronil bioaccumulates with repeated exposure, becoming lethal to bees within days. Toxicity to beneficial species has been instrumental in banning fipronil for agriculture in the European Union since 2013 (Commission Implementing Regulation of the E.U., 2013) and restricting its use in the United States.
Fipronil has been used in Colombia since 1993. It is marketed in 60 local agricultural products and can be used on more than 40 crops, according to registrations with Instituto Colombiano Agropecuario (ICA, 2021). At least 64,000 hives (each can house 50,000 bees) died from pesticides in Colombia between 2016 and 2020 (ICA, 2021). Laboratory tests on 42 colonies found that 33 (73%) had fipronil and 19 (42%) chlorpyrifos traces. Due to pressure from beekeepers, in March 2021 ICA issued a resolution (No. 092101) suspending fipronil use on avocado, citrus, coffee, and passionflower crops, to be effective from September 2021 (ICA, 2021). The first three crops require pollinators, such as bees, for fertilization and to bear fruit. The six-month period between March and September was considered a grace period for manufacturers to exhaust their stocks; within that period they could apply for new registrations, excluding its use in the four crops mentioned. The ICA would cancel registration for all uses if the product label did not withdraw its usage for the four crops after the six-month grace period. Because the resolution did not prevent fipronil use in other crops, farmers could apply it on any uncontrolled plantations. Although bee mortality has been associated with these four crops, fipronil use would continue to affect other beneficial terrestrial and aquatic macroinvertebrates. A 2021 meta-analysis reported a synergistic increase in bee mortality from agrochemical-agrochemical interactions (Hedge’s d=69) and d=172) overall for six classes of interactions between parasites, agrochemicals, and nutrition (Siviter et al., 2021).
Numerous studies have demonstrated that fipronil is extremely toxic to aquatic and terrestrial invertebrates at the ppb concentrations found in municipal wastewaters, urban streams (Weston and Lidy, 2014; Mize et al., 2008; Zhang et al., 2020), and waterways receiving treated rice-field tailwater (USGW, 2003). A study of macroinvertebrates spanning seven taxonomic orders showed total abundance decreased nonlinearly with increasing fipronil concentration (Mize et al., 2008). Also, the total number of taxonomic groups (richness or diversity of species, Y) decreased linearly with the maximum fipronil concentration (μg/L, X), particularly in midge Chironominae and Orthocladinae subfamilies (Y = 25.45 ± 1.56 -2.36 ± 0.496X (R2 =0.58, our values digitized from Mize et al., 2008). The most notable response in the macroinvertebrate- community structure was a shift in dominance from insects (midges, mayflies, and caddisflies) to non-insects (scuds, snails, worms) as rice- cultivation intensity and concentration of fipronil compounds increased. Chironomids, a family of the order Diptera with more than 7,000 described species, are considered indicator species of pollution in river environments (Zhang et al., 2020) and decreased rapidly with small increases in fipronil concentration (Mize et al, 2008). Their larvae and pupae are food for fish, amphibians, and other aquatic animals. Fish and insectivorous birds also eat adults. Although most studies have concentrated on the impact of fipronil in the phylum Arthropoda (insects, arachnids and crustacea), it is also toxic for other taxa in the phyla mollusks and Cnidaria (Figure 1).
Laboratory studies of the coastal brown shrimp, Farfantepenaeus aztecus, estimated a fipronil 96-hr LC50 of 1.3 ppb (Al-badran et al., 2018). However, at concentrations from 0.1 to 10 ppb, survival was progressively reduced to the point that all individuals died after 28 days of exposure. The median lethal times (days for 50% of the animals to die) were 6.6 ± 3.51 at 0.1 ppb, 6.33 ± 3.78 at 1.0 ppb, 2.66 ± 1.15 at 3.0 ppb, 3.0 ± 1.0 at 6.4 ppb, and 1.66 ± 0.57 at 10 ppb. The coastal brown shrimp is a good sentinel of water quality, an important commercial species, and is in the diet of many other marine organisms. In 2016, its commercial value in the United States alone was 166,542 million dollars (National Marine Fisheries Service, 2017). The juvenile stages live in estuaries, making them potentially susceptible to pesticides from agriculture. The 96-h LC50 of fipronil (0.68 ppb) to larval grass shrimp (Palaemonetes pugio) is orders of magnitude smaller than imidacloprid (308 ppb), atrazine (>10,000 ppb), and the 3-component mixture was greater than the additive toxicity (Key et al. 2007).
Another crustacean that is highly sensitive to fipronil is the freshwater crayfish (Procambarus clarkki), which is of great economic importance as it is raised for consumption in the United States and other countries, and is also sold as commercial fish bait. It is also a favorite prey for many birds, including gray herons, cattle egrets, ciconids (storks), and larids (gulls, terns, skimmers). The use of fipronil-treated rice seeds has produced multiple mass mortality incidents of crayfish in the United States (USEPA, 2007). In 8 of 16 monitoring ponds, fipronil concentrations averaged 1.67 ppb and reached 3.2 ppb in some cases. This resulted in the United States banning fipronil use on rice seeds. In a 2020 EPA memorandum on review of fipronil registrations, the chemical company BASF Corporation stated that it would no longer market fipronil for use on rice crops within the United States but would continue its commercialization in other countries (USEPA, 2020).
Most fipronil products are marketed as 20% concentrated suspensions to be applied with spraying equipment. Technical sheets indicate that cattle should not enter the paddocks until 14 days after application. In Colombia, fipronil likely impacts numerous terrestrial species predatory on the target species. For example, fipronil is widely used in Kikuyu pastures in the high Colombian tropics to control the grass bug Collaria scenica. Expected non-target effects on pastures treated with fipronil are the disappearanceof the two main Collaria scenica enemies: the predatory beetle Eriopis connexa and spiders of the genus Alpaida.
The life cycle of Eriopis connexa is much longer than that of Collaria scenica: adults live 2-3 months compared to 3-4 weeks for C. scenica (Zazycki et al., 2015). In addition, the reproduction rate or replacement rate of E. connexa is 16 new individuals for each generation, while that of C. scenica is around 75 individuals per female (Zazycki et al., 2015). Therefore, it would be expected that if fipronil’s efficacy was 100%, Collaria scenica would recover more quickly than Eriopis connexa populations. Additionally, Elzen (2001) discusses fipronil’s effects on other beneficial organisms.
In conclusion, what is occurring with honeybees in Colombia is just the tip of the iceberg on the impacts fipronil has on non- target species. Both terrestrial and aquatic invertebrates have been affected by fipronil worldwide, leading to bans and restrictions of fipronil use in agriculture. In spite of the lack of studies in Colombia (except for honeybees), the harmful effect of fipronil on beneficial non-target species can also be expected to be occurring, as reported elsewhere. Therefore, Colombia should implement similar restrictions as those in other countries.