Discussion
Given that recent evidence indicates that increasing agriculture to meet
the growing global food demand could simultaneously increase human
infectious diseases (Rohr et al., 2019), such as human schistosomiasis,
we conducted a study to identify agrochemicals that could sustainably
improve food production without increasing schistosomiasis. Expanding
upon previous work on predators in isolation (Halstead, Civitello, &
Rohr, 2015), our study confirmed that most insecticides pose a high
toxicity risk to snail predators at environmental concentrations in
simulated aquatic communities. We identified that, within their
pesticide class, the organophosphate malathion and the pyrethroid
λ-cyhalothrin had the lowest risks of increasing Bu. truncatussnails that transmit urinary schistosomiasis in Africa. Bottom-up
effects of fertilizer on snail biomass in natural communities occurred
as fertilizers increased both snail food (periphyton) and habitat
(aquatic vegetation), whereas herbicides decreased snail habitat
(experiment one). Thus, fertilizer bottom-up effects are expected to be
generally stronger than those for herbicides in natural communities.
Positive bottom-up effects on snails for the herbicides atrazine and
acetochlor were found in the absence of aquatic macrophytes and snail
predators (experiment two), whereas some herbicides, such as alachlor,
were negatively associated with snails under the same conditions. We
found that snail biomass positively predicted their cercarial
production, suggesting that changes in snail biomass associated with
agrochemical pollution could have strong potential to influence human
exposure to schistosome cercariae. Our findings highlight that
maximizing the benefits of agricultural intensification, while
minimizing indirect costs on human health, will require identifying
bottom-up and top-down effects of agrochemicals within natural aquatic
communities where the snails that transmit schistosome parasites are
found.
Initial (24hr) mortality of the crayfish Procambarus alleni in
our mesocosm experiment generally matched expectations from previous lab
experiments, with the exception of the toxicity of some pyrethroids
being lower in outdoor mesocosms. We confirmed previous findings that
malathion is a low risk organophosphate, potentially because of its very
high LC50 values for P. alleni (Halstead et al.,
2015). Halstead et al. (2015) reported that all three of the pyrethroids
that we tested were highly toxic to P. alleni . However, we found
that λ-cyhalothrin, unlike other pyrethroids, did not lead to top-down
effects on snails in our natural communities when applied at
concentrations approximating the 96h LC50 for P.
alleni (Halstead et al., 2015). One potential reason for this result
may be that submerged vegetation, such as the H. verticillataused in our study, has been linked to reduced toxicity of pH-sensitive
insecticides, including malathion and λ-cyhalothrin (Brogan & Relyea,
2014; Leistra et al., 2004). While the organophosphate chlorpyrifos and
the pyrethroid esfenvalerate also exhibit pH-sensitive hydrolysis
(Hertfordshire, 2013), they were likely applied at sufficiently high
concentrations in our study (2x and 10x their respective 96h
LC50 estimates) to preclude any increased degradation
from mitigating acute toxicity to P. alleni . Thus, our findings
suggest that, of the insecticides we tested, malathion and λ-cyhalothrin
should represent the weakest top-down effects on snails in natural
communities with aquatic vegetation, and the lowest risk of increasing
snail biomass.
Fertilizers can increase submerged vegetation that acts as snail
habitat, potentially making fertilizers more likely to have positive
bottom-up effects on snails than herbicides and even modifying top-down
effects. Unlike other agrochemicals, fertilizers are both commercially
available and locally sourced via manure products, leading to their wide
application even by rural subsistence farmers. Consistent with previous
mesocosm experiments, we found that fertilizers can increase snails by
increasing attached algae that snails eat (Halstead et al., 2018).
However, we also documented that stronger bottom-up effects of
fertilizer exist by increasing the submerged vegetation that serves as
snail habitat. By increasing H. verticillata , fertilizers
indirectly benefited Bu. truncatus biomass by increasing both
snail reproduction and growth. In contrast, the same associations were
negative for Bi. glabrata , likely because of resource depletion
in some tanks given that Bi. glabrata infection rates and biomass
were both an order of magnitude greater than for Bu. truncatus .
In early weeks, algal food resources for snails fueled by fertilizer
would be high and available for snail reproduction, growth, and parasite
production by infected snails (Civitello et al., 2018). As Bi.
glabrata populations quickly grew, per-capita resources in tanks
decline such that snail populations crash as periphyton resources become
limiting in microcosms (Civitello et al., 2018; Rohr, Halstead, &
Raffel, 2012). Thus, aquatic vegetation likely fueled snail reproduction
for both snail species, but Bi. glabrata biomass outpacedBu. truncatus biomass, likely increasing the likelihood of
population crashes (negative associations) toward the end of our
experiment. We know of no available studies documenting that such
resource limitations occur in aquatic systems where schistosomiasis is
transmitted to humans. In fact, available field studies suggest that
aquatic vegetation is highly beneficial to both Bu. truncatus andBi. glabrata populations in natural systems and to their parasite
production (Haggerty, Bakhoum, Civitello, et al., 2020).
In our first experiment, presence of H. verticillata in the tank
provided an alternative resource for crayfish (Lodge, Kershner, Aloi, &
Covich, 1994), in addition to providing potential refugia and increased
resource availability for snails (Bronmark, 1989). Crayfish of the
genera Procambarus and Oronectes have been associated with
declines in both submerged macrophytes and snails (Lodge et al., 1994;
Rodríguez, Bécares, & Fernández-Aláez, 2003). Reductions in macrophytes
by crayfish occur through both consumptive and non-consumptive removal
of plant biomass (Lodge et al., 1994; Rodríguez et al., 2003), while
reductions in snails are primarily consumptive (Hobbs, Jass, & Huner,
1989). We found that crayfish were negatively associated with H.
verticillata cover, consistent with crayfish consuming this macrophyte.
However, submerged plants actually were associated with reduced final
crayfish counts, possibly by providing refugia for snails thus reducing
crayfish predation rates on this primary protein source. In addition to
providing potential refugia from snail predators, macrophytes provide
increased surface area for epiphytic periphyton growth, and grazing of
epiphytes by snails can, in turn, increase macrophyte growth (Bronmark,
1989; Lodge et al., 1994; Schmidt, Koehler, & Alfermann, 2011;
Underwood, 1991). Nutrients, particularly ammonia, released by snails
can also facilitate macrophyte growth (Underwood, 1991). Thus, aquatic
vegetation can increase snails by both providing resources to snails and
reducing predation rates on snails. In contrast to the potential for
fertilizers to foster the mutualism between snails and vegetation, we
found that effects of herbicides on snails in natural communities were
generally weaker, potentially due to a negative association between
herbicides and submerged plants in experiment one.
Herbicides generally had negative effects on snails by reducing aquatic
vegetation, with positive bottom-up effects of atrazine and acetochlor
only in the absence of aquatic vegetation and snail predators. The
positive association that we found between some herbicides, such as
atrazine, one of the most common herbicides globally, and snails in our
second experiment is consistent with previous studies (Halstead et al.,
2018; Rohr et al., 2008). Halstead et al. (2018) actually detected
positive atrazine effects while controlling for crayfish density.
However, Halstead et al. (2018) did not include submerged aquatic
vegetation, which likely increased the chances of detecting bottom-up
herbicide effects because it omits the negative herbicide effects on
snail habitat that we found in experiment one. Atrazine and other
herbicides can increase snails by killing phytoplankton that competes
with periphyton algae eaten by snails (Halstead et al., 2018). Instead
of such mechanisms leading to consistent positive effects on snails
among herbicides, we found positive and negative effects in our study
for acetochlor and alachlor, respectively. As algae absorb available
nutrients, both periphyton and snails that consume these nutrients,
eventually hit a carrying capacity after which their populations can
decline or even crash (Rohr et al., 2012). Herbicide effects can be
negative overall when considering only data points at the end of the
experiment after snail populations exceed carrying capacity and
populations subsequently crash (Rohr, 2017). Thus, we think that
variation in snail population growth among tanks likely influenced
alachlor and acetochlor associations with dead and total snails,
respectively, when measured at the end of our second experiment.
Nonetheless, our results suggest that fertilizers are far more likely
than herbicides to have positive bottom-up effects on snails, and
especially in communities where snail predators are present. Our finding
that fertilizers can increase snail habitat and resources is consistent
with field observations in sub-Saharan Africa that revealed positive
associations between fertilizer use and snail habitat, snail abundance,
and human schistosomiasis infections (Haggerty, Bakhoum, Chamberlin, et
al., 2020).
The importance of other functional groups, such as aquatic vegetation,
in mediating the indirect effects of contaminants on snails that
transmit the parasites causing schistosomiasis in humans underscores the
need to include these relationships when assessing environmental risk of
contaminants. This becomes even more critical when assessing the risk of
contaminant mixtures. The combined indirect effects of multiple
contaminants can either mitigate or exacerbate the predicted effects of
a single-contaminant scenario (Halstead et al., 2014). Our study
inferences are restricted to observing chemicals individually and we
could not simulate all biotic components of the aquatic communities that
occur in transmission sites that might influence snail responses to
agrochemicals. For example, eutrophication from long-term fertilizer
inputs could cause unpredictable changes to snail populations or species
richness, potentially eliminating important functional redundancies that
can alleviate losses in functionally-important sensitive species (Hooper
et al., 2005). Thus, the extent to which changes in biodiversity and
abiotic conditions can mediate indirect effects of contaminants (either
individually or as mixtures) on Biomphalaria and Bulinussnails warrants further study. This is especially true given that
changes in snail biomass associated with agrochemicals that we found
appear very likely to change parasite production. Further, human
co-infection by parasites released by Biomphalaria andBulinus snails is not uncommon in Africa.
Overall, our findings suggest the need to identify low risk
insecticides, such as malathion, that could reduce crop pests without
increasing snails. For example, our findings recommend against
pesticides that harm crayfish, because these predators reduce
transmission directly by consuming snails and indirectly by consuming
snail habitat. The more consistent and stronger positive impact of
fertilizers on snails than herbicides, by increasing both their food and
habitat, highlights that the removal of aquatic vegetation could offer
important public health benefits by limiting its bottom-up effects on
schistosomiasis risk.