Resolving the life cycle alters expected impacts of climate change

Abstract

Recent models predict contrasting impacts of climate change on tropical and temperate species, but these models ignore how environmental stress and organismal tolerance change during the life cycle. For example, geographical ranges and extinction risks have been inferred from thermal constraints on activity during the adult stage. Yet, most animals pass through a sessile embryonic stage before reaching adulthood, making them more susceptible to warming climates than current models would suggest. By projecting microclimates at high spatio-temporal resolution and measuring thermal tolerances of embryos, we developed a life cycle model of population dynamics for North American lizards. Our analyses show that previous models dramatically underestimate the demographic impacts of climate change. A predicted loss of fitness in 2% of the USA by 2100 became 35% when considering embryonic performance in response to hourly fluctuations in soil temperature. Most lethal events would have been overlooked if we had ignored thermal stress during embryonic development or had averaged temperatures over time. Therefore, accurate forecasts require detailed knowledge of environmental conditions and thermal tolerances throughout the life cycle.

Hotter nests produce hatchling lizards with lower thermal tolerance

“…Recent studies have highlighted the importance of understanding how heat stress influences early life stages in order to predict population-level consequences of warming (Levy et al, 2016(Levy et al, , 2015. In lizards, the embryos of some species may experience thermally stressful temperatures during summer heatwaves (Levy et al, 2015), which are predicted to occur more frequently in future (Cowan et al, 2014;Hansen et al, 2012).…”

“…Heatwaves have become more common in recent decades (Hansen et al, 2012), and are predicted to increase in frequency in the future (Cowan et al, 2014). Thus, embryos of some lizard species may experience periods of acute thermal stress during development in the future (Levy et al, 2015;Telemeco et al, 2016a).…”

“…Nearly all of the above studies have used incubation temperatures within the current temperature range found within natural nests, so we know very little about how embryos will respond to thermally stressful conditions that may be experienced in the future (Angilletta et al, 2013;Levy et al, 2015). Potentially, developmentally plastic shifts in thermal tolerance could allow lizards to rapidly adapt to climate warming (Hoffmann and Sgrò, 2011;Urban et al, 2014).…”

“…Reptiles are particularly vulnerable to climate warming because environmental temperatures directly affect their physiology and behaviour (Araújo et al, 2006;Huey et al, 2012;Sinervo et al, 2010;Tewksbury et al, 2008). Predicting the vulnerability of ectotherms to climate warming requires knowledge of how increases in temperature will affect subsequent life-history stages (Kingsolver et al, 2011;Levy et al, 2015;Radchuk et al, 2013). Unlike adult lizards, developing lizard embryos cannot thermoregulate (Telemeco et al, 2016b) and, consequently, they may experience thermally stressful temperatures in natural nests during summer (Shine and Elphick, 2001).…”

Transient window of resilience during early development minimizes teratogenic effects of heat in zebrafish embryos

“…Embryos of endothermic, ectothermic, and oviparous species are also subject to rising environmental temperatures with dramatic developmental and ecological consequences (Gendelman and Roth, 2012; Rosa et al, 2014; Levy et al, 2015; Griffith et al, 2016). Studies on teratogenic effects of heat in mammals have shown that embryos are heat susceptible early and acquire resilience at later developmental stages (Edwards et al, 1997a; Walsh et al, 1997; Hansen, 2009).…”