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.