Published On: Tue, Mar 26th, 2019

Independent and combined effects of daytime heat stress and night-time recovery determine thermal performance [RESEARCH ARTICLE]

INTRODUCTION

Climate warming leads to a substantial increase in global mean temperatures as well as daily maximum and minimum temperatures worldwide (Karl et al., 1993; Easterling et al., 1997; IPCC, 2013), and it has resulted in significant impacts on species of many taxa (Easterling et al., 2000; Parmesan et al., 2000; Jiguet et al., 2011; Peng et al., 2013; Sørensen et al., 2016; Barton and Schmitz, 2018). Most previous studies concerning effects of temperature change are conducted under constant conditions (Easterling et al., 2000; Smith, 2011; Lloret et al., 2012; Reyer et al., 2013). However, ambient temperatures vary and most organisms experience fluctuating thermal environments in nature (Fischer et al., 2011; Colinet et al., 2015). Importantly, the effects of constant and fluctuating temperatures can be very different (Bozinovic et al., 2013; Zhao et al., 2014; Ma et al., 2015a). Compared to fluctuating temperatures, constant temperatures often overestimated or underestimated thermal effects on organismal performances, such as metabolism, locomotion, development, survival, reproduction and population growth (Du and Ji, 2006; Ragland and Kingsolver, 2008; Estay et al., 2014; Zhao et al., 2014; Ma et al., 2015a,b; Kingsolver et al., 2016). Thus, to mimic the effects of natural fluctuating temperatures, daily temperature fluctuations have received increased attention in recent years (Zhao et al., 2014; Ma et al., 2015a; Bozinovic et al., 2016).

Nevertheless, previous research concerning the effect of fluctuating temperatures focused mainly on either (1) changes in amplitudes of daily temperature variability with the same means (Lambrechts et al., 2011; Lyons et al., 2013; Xing et al., 2014) or (2) shifts in temperature means with the same variances (Paaijmans et al., 2010; 2013). In these studies, daily maximum and minimum temperatures were manipulated to shift concurrently in the same or opposite direction. That experimental design may not allow us to differentiate the effects of changes in temperature maxima from that in minima. However, changes in daily maximum or minimum temperatures can alter thermal performance curves and influence key fitness components including development, survival, fecundity and longevity (Zhao et al., 2014; Ma et al., 2015a,b).

Thermal performance curves show that increases in temperatures below optima have positive effects on organisms whereas increases in temperatures above optima have negative effects (Angilletta, 2009; Bozinovic et al., 2011; Speights et al., 2017). Terrestrial invertebrates often experience adverse thermal environments caused by daytime extreme high temperatures in summer days, especially in the context of ongoing climate warming (Clusella-Trullas et al., 2011; Gillespie et al., 2012; Sentis et al., 2013; Ma et al., 2015a,b; Kingsolver et al., 2016). Meanwhile, they are also expected to recover or repair themselves during the cooler intervals in between repeated exposure to high temperatures (Bozinovic et al., 2011; Colinet et al., 2015; Ma et al., 2015a; Speights et al., 2017). Hence, thermal effects of daily fluctuating temperatures may be divided into two biological processes (i.e. negative effects of daytime heat stress and positive effects of night-time recovery). So far, however, we still know little about the thermal effects of daytime heat stress and night-time recovery on organism performance.

Here we used a lady beetle Propylea japonica, a predatory insect species, as our model organism. First, we measured egg development rate and survival, key fitness components, under different combinations of daily temperature maxima and minima to differentiate the thermal effects of changes in daytime heat stress from those in night-time recovery. Then, we measured the critical thermal maximum (CTmax) of first-instar larva that had newly hatched either in the morning or in the evening in an effort to understand how changes in daytime heat stress and/or night-time recovery affect organism thermal performance.

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