Introduction
Recent evidence suggests that increasing agriculture to meet the growing
global food demand could simultaneously increase human infectious
diseases (Rohr et al., 2019), necessitating studies that identify means
of sustainably improving food production without increasing disease. One
such human disease that is positively associated with agricultural
expansion is schistosomiasis, a disease caused by parasites released
from freshwater snails, with an estimated 779 million people at risk
globally (Vos et al., 2016). Over 90% of global cases
(~200 million cases) occur in sub-Saharan Africa and
involve Biomphalaria and Bulinus snail species as
intermediate hosts (Gryseels, Polman, Clerinx, & Kestens, 2006;
Steinmann, Keiser, Bos, Tanner, & Utzinger, 2006). Schistosomiasis has
been positively linked to expanding snail habitat and loss of native
snail predators (Huang & Manderson, 1992; Savaya Alkalay et al., 2014;
Steinmann et al., 2006) because each infected snail host can release
thousands of cercariae, the human-infectious life stage, daily. Parasite
production by snails can be influenced by local aquatic factors
(Haggerty, Bakhoum, Civitello, et al., 2020), and thus, human infection
rates respond rapidly to changes in local ecological factors (Huang &
Manderson, 1992), emphasizing the importance of freshwater ecology in
infection dynamics.
Agrochemical pollution has the potential to influence ecological factors
that directly or indirectly influence schistosomiasis transmission. Both
fertilizers and herbicides can increase periphyton resources required
for snail growth and cercarial production (Halstead et al., 2014), and
have been linked to increased trematode infection intensities in frogs
in agricultural wetlands (Rohr et al., 2008). Herbicides kill
phytoplankton that absorb light from the water column, which can
indirectly increase growth of periphyton, attached algae that is a major
resource for snails (Halstead et al., 2018). Additionally, fertilizers
and herbicides can increase and decrease, respectively, submerged
vegetation that acts as primary habitat for snails and may influence
snail predation. Invertebrate predators that consume snails and help
regulate snail populations can be killed by some insecticides even at
environmentally relevant concentrations, leading to top-down insecticide
effects that increase snails (Halstead et al., 2014). Snail intermediate
hosts are difficult to control (Gryseels et al., 2006; Steinmann et al.,
2006), and understanding the strength of various agrochemicals on snails
might be key to understanding recent increases in human schistosomiasis
coincident with agricultural expansion and preventing any future surges
(Hoover et al., 2020).
Agrochemical use is predicted to increase 2-5 fold over the next few
decades (Foley et al., 2011; Tilman, Balzer, Hill, & Befort, 2011;
Tilman et al., 2001), yet laboratory studies of pesticides using species
in isolation could miss the net effects of pesticides in natural
communities (Clements & Rohr, 2009; Rohr & Crumrine, 2005; Rohr,
Kerby, & Sih, 2006). Submerged aquatic vegetation that acts as snail
habitat might decrease the toxicity of certain insecticides by changing
pH (Brogan & Relyea, 2014), or influence predation by providing refugia
(Davis, Purrenhage, & Boone, 2012). Thus, because agrochemicals in
natural environments are differently subject to the above influences,
simulating natural communities using mesocosm experiments is needed to
improve predictions of the direct and indirect effects of agrochemicals
on freshwater communities, such as those containing snail hosts (Rohr,
Salice, & Nisbet, 2016).
We created experimental natural freshwater pond communities to determine
the predictability of top-down effects of insecticides and bottom-up
effects of fertilizer or herbicides on the biomass of two genera of
snail hosts that can transmit schistosomiasis (Biomphalaria
glabrata and Bulinus truncatus ). More specifically, we examined
the top-down effects of six insecticides belonging to two insecticide
classes (the organophosphates chlorpyrifos, malathion, and terbufos, and
the pyrethroids esfenvalerate, λ-cyhalothrin, and permethrin), and the
bottom-up effects of both fertilizer and six herbicides belonging to two
herbicide classes (the chloroacetanilides acetochlor, alachlor, and
metachlor, and the triazines atrazine, propazine, and simazine) in the
presence of snail predators. We then performed a follow-up experiment
using all six herbicides but without snail predators to determine if
herbicide bottom-up effects on snails are only evident in the absence of
strong top-down effects. In the follow-up experiment, we also examined
if total parasite production by snails was predicted by their total
biomass, and, thus, whether snail biomass changes associated with
different agrochemical exposures could be related to human exposure to
parasites.