Introduction
Predators have important impacts on ecosystems through direct effects on
prey and indirect effects on the species that interact with the prey
(Pace et al. 1999, Ripple et al. 2016) . The importance of top-down
control in terrestrial systems has been debated (Wootton 1994, Shurin et
al. 2002), and these arguments are complicated because the relative
importance of top-down control may vary among experiments in different
years even within the same systems and locations (e.g., Meserve et al.
2003, Noemi Mazia et al. 2004, Barton et al. 2009). Thus, while
empirical studies often report different findings, synthesis across
years and systems reveals that trophic cascades are context dependent
and influenced by the abiotic environment (Chamberlain et al. 2014,
Rosenblatt and Schmitz 2014). This is alarming, of course, because
humans are rapidly altering Earth’s environment in innumerable ways, and
higher trophic levels are often the most sensitive to perturbations
(Voigt et al. 2003, Ripple and Van Valkenburgh 2010). Thus, it is likely
that the nature and strength of top-down control will continue to change
in the Anthropocene.
Inherent in a climate change study is the assumption that researchers
are interested in understanding the effects of contemporary climate
change occurring on Earth, and less interested in understanding the
effects of a climate change that is not expected to occur on our planet.
Thus, given that species interactions are context dependent and that
subtle changes in abiotic factors can influence outcomes, climate change
studies must be as realistic as possible if they are to facilitate a
predictive understanding of contemporary climate change. However,
implementing realistic warming treatments, especially in the field, can
be difficult because of logistical constraints (De Boeck et al. 2015).
For example, electricity is not always available, and therefore warming
treatments are often created with passive chambers that rely on solar
energy to increase temperatures (Aronson and McNulty 2009). These
designs tend to disproportionately warm during the day when solar energy
is high, and they produce relatively little warming during the night
(Speights et al. 2018). This is concerning because, on average, Earth’s
minimum temperatures are increasing at a faster rate than maximum
temperatures (Easterling et al. 1997, Davy et al. 2017) and organisms
are expected to respond differently to day and night warming (Speights
and Barton 2019). Consequently, experiments that use unrealistic warming
treatments may come to unrealistic conclusions and contribute to
misleading predictions about the effects of climate change (Speights et
al. 2017).
The impacts of diel asymmetries in warming on ecosystems is vastly
understudied (Gaston 2019). Research comparing day and night warming has
mostly focused on the direct effects of warming on plants (e.g., Peng et
al. 2004, Bai et al. 2012, Fan et al. 2015, García et al. 2015, Loka and
Oosterhuis 2015, Fu et al. 2016, Rossi and Isabel 2017). Fewer studies
have investigated the effects of night warming on predators and their
interactions with lower trophic levels. However, Barton and Schmitz
(2018) demonstrated that spiders had different responses to day- and
night-warming that resulted in opposite indirect effects on plant
communities. Similarly, Speights and Barton (2019) showed that day and
night warming can have different impacts on lady beetle development,
predation, and respiration rates. Although these examples are limited,
there is consistent evidence that the timing of warming matters and can
dramatically influence conclusions.
We report here a comparison of the effects of constant, day, and night
warming on a food chain comprising predatory lady beetles
(Harmonia axyridis ); their prey, pea aphids (Acyrthosiphone
pisum ); and fava bean (Vicia faba ) host plants. These species
have a proven record for testing other hypotheses about the top-down
effects of warming (e.g., Harmon et al. 1998, Murrell and Barton 2017,
Higashi et al. 2020). We hypothesized that the different timing of
warming would alter the effects of warming on these species.
Specifically, we expected day warming to increase top-down control by
lady beetles. Studies have reported both positive and negative effects
of day warming on pea aphid population growth rates (Harmon et al. 1998,
Ryalls et al. 2013). However, in general, predation rates by lady
beetles are expected to increase with warming (Barton and Ives 2014,
Schwarz and Frank 2019) and therefore are likely to ameliorate any
positive effects of day warming on aphid abundance. In contrast, we
expected night warming to decrease top-down control by lady beetles.
While night warming has been shown to increase pea aphid population
growth rates (Miller et al. 2017), H. axyridis lady beetles rely
on vision to find prey and therefore consume fewer aphids in low-light
conditions (Harmon et al. 1998). Thus, darkness was expected to preventH. axyridis lady beetles from increasing predation rates in night
warming treatments, and therefore result in different effects of day and
night warming on aphid abundance and plant biomass.