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.