Discussion
We show that the success and failure of predatory biocontrol of
schistosomes depends on key ecological mechanisms, namely resource
competition, increased infectiousness with resource uptake, and
size-dependent host mortality. These combined mechanisms result in
overcompensation of parasite output to predator biocontrol on
intermediate hosts and thus a unimodal response of ecological risk of
human schistosome exposure. Compared to no predators (Fig. 1A & 2A),
weak to moderate predator biocontrol performs increasingly worse (Fig.
1B & 2B) before eventually succeeding at extremely high levels of
investment (Fig. 1D & Fig. 2D). Here, low predation pressure reduces
resource competition and enables some juvenile snails to more rapidly
grow, reach an invulnerable size, and produce more parasites, i.e.
escape an otherwise strong juvenile bottleneck (de Roos and Persson
2013). Therefore, low predator stocking densities backfire because they
only partially reduce host density, which relaxes competition for food
and triggers a trophic cascade to facilitate higher parasite yields from
fewer remaining hosts. In contrast, high predator densities kill more
hosts to control parasite output, first by reducing infected snail
lifespan below the prepatent, i.e. developmental period of schistosomes
(~4 weeks), and then by extirpating snail populations
(Fig. 1C & 2C). This result is consistent when predation is
size-independent or categorically depends on host size (discrete
host mortality ). The consistent pattern of backfiring until ultimate
success exemplifies the challenges of ‘do or do not’ biocontrol by
highlighting overcompensation based on resource competition as a primary
driver.
Size-dependent predation drives parasite output by introducing a host
size refuge from predation. We show when predators are gape limited
(discrete host mortality ), biocontrol success depends on
the upper limit of the binary host vulnerability window: there is a
strong relationship between the upper limits to this window and a
successful predator stocking density because predator gape limits shift
the infected host size distribution to larger, more prolific hosts (Fig.
3, lighter curves). When predators kill almost all hosts (0–25 mm
vulnerable; HCmax = 25 mm), they trigger host
overcompensation and thus boost parasite output for both algae and
detritus until eventually succeeding at high predator stocking densities
(Fig. 3). In contrast, predator densities below this critical threshold
not only underperform, but become increasingly worse and riskier the
closer they approach it (Fig. 3, darker curves). However, when predators
are unable to consume intermediate or large snail hosts,
(HCmax = 5, 10, or 15 mm), total parasite
production increases linearly. In other words, even at unrealistically
high densities, predators that are small-snail specialists reduce
resource competition, but do not eliminate large, prolific hosts.
Therefore, if predator biocontrol programs fail to target large,
disproportionately infectious hosts, they may be prone to backfire,
regardless of management intensity.
In addition to a binary host vulnerability window, we also simulatedcontinuous host mortality , where predation risk follows a
continuous negative-exponential function derived from experiments
(Sokolow, Lafferty, and Kuris 2014). Under this scenario, amassing
predator stocks fails to suppress parasite density until reaching
unrealistic predator densities (Fig. 4), even when compared with
densities simulated in a recent study that tested these prawns
experimentally (dotted line; (Sokolow, Lafferty, and Kuris 2014)) and
the maximum recommended density for aquaculture practice (dashed line;
(Upstrom 1986)). Here, large snails are never completely invulnerable to
predation, but experience a substantially lower risk than smaller
individuals. Cumulative parasite output in these scenarios also stems
from overcompensation. As seen previously, parasite output increases
with resource supply rate (Civitello et al. 2018; Malishev and Civitello
2019) and overcompensation emerges under two conditions: whenever
resource supply is high enough to support any parasite production and
when the steepness of this response increases with supply rate.
Combined, these results confirm how the aforementioned mechanisms shape
overcompensation and further suggest resource type and supply exacerbate
its role in size-dependent mortality under predator biocontrol.
Our model results contrast other simulations of predatory biocontrol of
schistosomes (Sokolow et al. 2015; Hoover et al. 2019) that predict
consistent success with increasing predator stocking density. Despite
several differences between our individual-based model and these
ordinary differential equation (ODE) models, one central difference
drives these divergent forecasts: the positive effect of resource uptake
on schistosome production by individual infected snails. Indeed, an
extremely simplified ODE model of snail-schistosome dynamics illustrates
how resource-dependent cercariae output can drive overcompensation due
to increased background mortality (Civitello et al. 2018), supported by
the SIDEB model. The positive effects of food quantity and quality are
pervasive among schistosomes and other trematodes, infecting snails
(Keas and Esch 1997; Civitello et al. 2018), suggesting a critical need
to incorporate this general phenomenon when analysing disease mitigation
strategies involving snails.
Given these divergent conclusions and the stakes involved in control
intervention exacerbating or eliminating infection risk in vulnerable
human populations, it is critical to evaluate existing evidence.
Currently, only one published field study evaluates prawn-based
biocontrol of human schistosomes (Sokolow et al. 2015). However, the
study introduced an unspecified density of prawns into a water access
point at one village in the Senegal River Basin and suggested this
lowered schistosome infection in the following year compared to a
control village not receiving prawns. While encouraging, these data
cannot rigorously attribute this effect to the prawn manipulation, given
the sample size of one per treatment and no follow up estimation of
realized prawn density or survival. Despite a dearth of laboratory
studies evaluating the population dynamics of snails and schistosomes in
response to a range of prawn densities, one laboratory study shows
gape-limited predation by prawns can relax competition in populations of
uninfected snails, yielding fewer, larger individuals that produce many
eggs, consistent with predictions from the SIDEB model (Sokolow,
Lafferty, and Kuris 2014). Although this experiment did not incorporate
infection, recent experiments on resource competition and food supply
suggest these conditions could promote high parasite yields from the
remaining larger hosts (Civitello et al. 2018, 2020). Data on predator
densities, feeding selectivity, dynamics of snail population densities
and size-structure, cercariae shedding, and human infection are needed
to critically evaluate these alternative hypotheses and thus effective
predator biocontrol of human schistosomes.