BOX 1: Enemy-risk effects and the biological control of the red
imported fire ant
The red imported fire ant, Solenopsis invicta, was inadvertently introduced from South America into the port city of Mobile, Alabama in the 1930’s. Expanding its range across much of the southern United States, it achieved exceptionally high densities (5-10 times greater than in their native range), displacing native ants, damaging agricultural production, and creating a sting hazard for anyone active outdoors (Porter & Gilbert 2004; Oi et al. 2015). After a massive and controversial insecticide-based eradication effort failed, attention turned to classical biological control. Studies in the native range of the ants revealed over 20 species of parasitoid flies in the genus Pseudacteon (family Phoridae), most of which appeared to be host specific and thus to be potentially acceptable in terms of low risk of non-target impacts. Pseudacteon spp. parasitoids lay eggs in adult worker ants, the resulting parasitoid larvae completing their development in the heads of their host ants, which fall off as the larvae develop (hence their common name: decapitating flies).
Early investigations of Pseudacteon spp. in the native ranges of the fire ants concluded, however, that they were poor candidates for effective biological control, because they achieved very low rates of parasitism (Jouvenaz et al. 1981). Extensive year-long sampling across multiple sites confirmed that parasitism was indeed rare, with only 0.24% of workers parasitized on average (Calcaterra et al. 2008). Retrospective analyses of the extensive literature on introductions of parasitoids as classical biological control agents by Hawkins et al. (1993) and Hawkins and Cornell (1994) suggested that a threshold for success exists: parasitoids that fail to achieve maximum parasitism rates of >32% in their native ranges, or >33-36% in their introduced ranges, have been unable to produce economically-acceptable levels of pest suppression. Because the entire Pseudacteon spp. complex exerted a maximum of only 2.81% parasitism in the native range (Calcaterra et al. 2008), the suggestion that these flies would be of “dubious value” for biological control (Jouvenaz et al. 1981) was not hard to understand.
However, as argued by Feener and Brown (1992) and Porter and Gilbert (2004), a reliance on parasitism rates alone might lead us to grossly underestimate the potential value of Pseudacteon spp. parasitoids as control agents. Earlier studies had shown that phorid parasitoids attacking a different ant, while also generating little parasitism, elicited dramatic anti-predator defenses. Ants responded to the presence of flies by fleeing back to the nest or by sheltering from fly attacks in the leaf litter, causing the ants to lose their status as competitive dominants in their interactions with other ants (Feener 1981). Subsequent studies of S. invicta revealed a similar pattern: in response to a fly’s arrival, workers retreated underground, took cover below sticks or pebbles, or adopted stereotypic defensive postures with their sting-bearing gasters raised (Orr et al. 1995; Porter et al. 1995). This eliminated their ability to recruit foragers to food sources, with other ants immediately exploiting the now-available resources. Just a single parasitoid could arrest the foraging activity of hundreds of fire ant workers (Porter et al. 1995). Thus, S. invicta display dramatic and costly anti-predator defenses, and the non-consumptive effects of phorid flies on fire ants may allow native ants to compete effectively with these invaders.
Thus, recognition of the potential importance of enemy-risk effects of Pseudacteon spp. motivated the decision to import these species as classical biological control agents. Six species have been introduced to the United States to date, with different species attacking different subsets of worker ants, based on ant size, time of activity, or foraging location (at the nest or at foraging trails; reviewed by Oi et al. 2015). Importantly, host-range testing included assessments not only of parasitism of non-targets, but also the attraction to worker ants and expression of the hovering attacks that elicit defensive responses (Porter & Gilbert 2004). Whether the enemy-risk effects will prove to be sufficient to control S. invicta in its invasive range remains, however, an open question, as Pseudacteon spp. continue to build their populations and expand their ranges while monitoring continues (Chen & Fadamiro 2018; Oi et al. 2019).