Try not. Do or do not. There is no try.
— Jedi Master Yoda
When young Luke Skywalker was in Jedi training, the great Yoda imparted simple wisdom to help him surpass his own limitations: ‘Try not. Do or do not. There is no try.’. For disease control, ecologists should also heed master Yoda’s lesson—either doing nothing or committing fully could achieve the best outcome. Growing evidence of failed efforts to control ecological pests and parasites illustrates how weak or moderate intervention can backfire, leading to worse efforts than doing nothing or extremely intense control (Zipkin et al. 2009). One critical challenge when implementing these ‘do or do not’ control scenarios is anticipating their outcome from simple, general theory that often guides successful management recommendations (Shea et al. 1998; Punt 2006). Therefore, failed interventions are only diagnosed after the damage has been dealt, eroding the environment and our confidence in ecological and epidemiological science (Howarth 1991; Simberloff and Stiling 1996; Louda et al. 2005).
To prevent these ecological mismanagement disasters, ecologists should evaluate interventions with models that incorporate general ecological principles known to trigger target populations to either compensate or overcompensate in response to control. Overcompensation is central to ‘do or do not’ control scenarios for ecological pests and parasites. That is, increasing rates of mortality can counterintuitively increase biomass or production rates in some life stages or the total population (Choisy and Rohani 2006; Holt and Roy 2007; Schröder, Persson, and De Roos 2009). The driving force of overcompensation is resource competition, whereby eliminating competitors rewards remaining individuals energetically, enabling them to grow larger and reproduce more (De Roos et al. 2007; Ohlberger et al. 2011). For management, pest populations that compensate from resource competition are less sensitive to weak or moderate control (Pardini et al. 2009), whereas overcompensation generates a unimodal backfiring phenomenon where pest or pathogen problems worsen with increasing control until sufficiently intense measures are reached (Moe, Stenseth, and Smith 2002; de Roos and Persson 2013; Preston and Sauer 2020; Zipkin et al. 2009). For example, recent work simulating different pesticide control scenarios in a snail-trematode system shows intense and frequent control as a ‘do or do not’ design can suppress infected host and parasite output, whereas moderate one-off intervention or weak application backfires and triggers parasite rebounds due to host populations overcompensating (Malishev and Civitello 2020). These failed attempts suggest that managers and ecologists should rigorously evaluate the merits of a binary strategy: do not intervene unless sufficiently intense actions can be sustained.
We use a case study of predatory biocontrol in a snail-trematode system to explore this binary strategy. The native African river prawn,Macrobrachium vollenhovenii, is a natural predator of snails and, recently, its local population collapse coincided with a large outbreak of human schistosomiasis in the Senegal River Basin (Sokolow, Lafferty, and Kuris 2014; Sokolow et al. 2015).We identify and evaluate three key ecological mechanisms that drive ‘do or do not’ control responses in parasites and vectors. First, strong laboratory and field evidence shows snail populations compete over resources (Perez-Saez et al. 2016; Preston and Sauer 2020; Civitello et al. 2020). Second, production of human-infectious cercariae per snail increases steeply with resources (Civitello et al. 2018), increasing host infectiousness with access to more food, as seen broadly for trematodes of humans and wildlife (Johnson et al. 2007). If moderate predator biocontrol reduces resource competition, then it can drive overcompensation in total cercarial production, the ecological dimension of human risk of exposure. In other words, the few remaining well-fed hosts could be more infectious than many starving hosts at high densities (Malishev and Civitello 2019). Third, like many predators, prawns are gape limited and disproportionately target individuals of smaller size ranges. Therefore, upper limits to prey intake size could promote overcompensatory parasite transmission from size-dependent host mortality (Ohlberger et al. 2011; de Roos and Persson 2013) that reduces competition experienced by prolific hosts large enough to escape predation risk. Combined, we hypothesize that these ecological mechanisms, namely (1) host competition for resources, (2) resource uptake promoting infectiousness, and (3) size-dependent mortality from gape limited predators can drive backfiring of weak or moderate biocontrol compared to ‘do or do not’ designs.
To test this hypothesis, we used an individual-based model of schistosome transmission based on bioenergetics theory to simulate size-dependent predation risk and examine potential biocontrol success and failure. We simulated two size-dependent predation scenarios (host mortality) over a range of predator densities: discrete host mortality, where hosts were categorized as either within or outside of the predator gape limits; and continuous host mortality, where predation risk was a decreasing function of host size based on experimental data. We propose both mortality scenarios present two constraints to biocontrol success: 1) a host vulnerability window to predation introduces the potential for a non-linear response to predator stocking density, where increasing densities first fail before reaching a successful threshold for eliminating infected hosts; and 2) a size class refuge from predation suggests predator gape limits can lead to failed biocontrol by shifting the infected host size distribution to larger, more prolific hosts. Our simulations propose management scenarios that attribute the success of ‘do or do not’ biocontrol designs to how gape limited biocontrol interacts with ecological mechanisms, while identifying common practices central to robust biocontrol success, i.e. no predator stocking vs. high stocking. Using these testable ecological mechanisms to explore the drawbacks, thresholds, and success of biocontrol design can explicitly evaluate management plans and features of potential biocontrol agents for enhancing pest and parasite control more broadly.