The effects of thermal stress on the early development of the lizard Anolis sagrei

Abstract

Across the globe terrestrial ectotherms-amphibians and non-avian reptiles-are facing a range of emerging challenges. Increasing global temperatures, in particular, are affecting all aspects of ectotherm biology and life history. Embryonic development is a thermally sensitive period of the organismal lifecycle, yet the impacts of thermal stress on the early development of ectotherms have significantly lagged behind studies of later stages and adult thermal physiology. Morphogenesis, the stage where the major anatomical systems are actively forming, is particularly sensitive to thermal stress, yet is not studied as often as later stages where growth is the primary process happening within the egg. Here, we focus on the effects of thermal stress on the first 12 days of development, the stages of morphogenesis, in the lizard Anolis sagrei. We examine the resiliency of the early developmental stages to heat stress by incubating eggs at temperatures that parallel conditions observed today and predicted over the next 50-100 years of projected climate change. Our results suggest that some anole nests are currently at the thermal limits for which the early embryonic stages can properly develop. Our results emphasize the importance of studying early embryonic stages of development and the importance of studying stage-specific effects of thermal stress on squamate development.

Introduction to the special issue—Developmental plasticity in reptiles: Physiological mechanisms and ecological consequences

“…() demonstrated that snapping turtle embryos are negatively affected by shaded conditions in agricultural fields, as well as by mercury pollution at these sites. Sanger, Kyrkos, Lachance, Czesney, and Stroud () demonstrated that increasing temperatures negatively affect embryo survival during the stages of morphogenesis in brown anoles, and suggest that climate change will likely negatively affect egg survival given that nests in the field are currently at the thermal limits. Ma et al.…”

“…First, Thompson et al (2018) demonstrated that snapping turtle embryos are negatively affected by shaded conditions in agricultural fields, as well as by mercury pollution at these sites. Sanger, Kyrkos, Lachance, Czesney, and Stroud (2018) demonstrated that increasing temperatures negatively affect embryo survival during the stages of morphogenesis in brown anoles, and suggest that climate change will likely negatively affect egg survival given that nests in the field are currently at the thermal limits. Ma et al (2018) exposed embryos of two sympatric lizard species (that occupy different microhabitats) to climate warming scenarios and show that the impact of climate warming on these species is dependent upon preferred microhabitats.…”

Thermal sensitivity of lizard embryos indicates a mismatch between oxygen supply and demand at near-lethal temperatures

“…Given that nest temperatures often fluctuate above the critical thermal maximum for some species (e.g. Angilletta et al, 2013; Sanger et al, 2018) and that global change will cause nest temperatures to rise in both mean and variance, more studies of acute exposure to thermal stress are needed.…”

“…Protocols for their captive husbandry are established (Sanger et al, 2008a), they are relatively fecund in captivity allowing for robust sample sizes (Hall et al, 2018), and their developmental staging series has been described (Sanger et al, 2008b). Females construct shallow nests across a diversity of habitats; thus, in the wild, embryos experience relatively large thermal variation during incubation (Sanger et al, 2018; Tiatragul et al, 2019) and temperature has important effects on embryo development, egg survival, and hatchling phenotypes (Pearson and Warner 2018). Moreover, daily fluctuations in nest temperature often reach extremely warm temperatures (> 40 °C, Sanger et al, 2018); indicating that embryos might have physiological mechanisms for ameliorating the adverse effects of acute exposure to high temperatures.…”

“…To determine the acute lethal temperature (T LETHAL ) for embryos, we exposed eggs to 1-hour heat shocks of increasingly high temperatures. To quantify embryo physiology, we measured embryo heart rates and oxygen consumption (henceforth VO 2 ) across temperatures from 22 to 47 °C, which encompasses the complete range of nest temperatures recorded for this species (Sanger et al, 2018; Tiatragul et al, 2019). To understand the effect of repeated exposures to sublethal temperatures, we subjected eggs to four exposures of an extreme fluctuation in nest temperature and measured aspects of embryo physiology, hatchling morphology, growth, and survival in the laboratory.…”