A brown anole emerging from the egg.

There is much talk these days about how human land use (e.g. urbanization) impacts wildlife. Although anoles have often taken center stage in this discussion (Winchell et al. 2016; Tyler et al. 2016;  Chejanovski et al. 2017; Lapiedra et al. 2017; Winchell et al. 2018), most of this work has focused on measuring phenotypes of adult males. Very little work has been done to understand how massive habitat alteration impacts early life stages even though we know that these stages are extremely sensitive to environmental disturbance and have the potential to impact population dynamics (Carlo et al 2018). Embryos are particularly sensitive to changes in the environment because they lack the ability to respond to unfavorable conditions by adjusting their behavior (i.e., they can’t run away). Since the 1980’s, we’ve known that egg mortality can have massive effects on population densities and even determine how these densities cycle from year to year (Andrews 1982; Andrews 1988; Chalcraft and Andrews 1999). Still, comparatively little attention is given to embryo development and egg survival when considering how habitat alteration impacts species.

In a newly published paper (Hall & Warner 2018), we sought to understand how extreme ground temperatures in cities and suburbs (i.e., the urban heat island effect) influence patterns of embryo development. Due to a lack of canopy cover (i.e., trees) and an abundance of heat-absorbing surfaces (e.g., concrete), cities and suburbs tend to be much warmer than adjacent forested areas, and this means nest temperatures are higher in urban and suburban areas compared to adjacent forested sites (Tiatragul et al. 2017).  Warm temperatures often have positive effects on embryo development; however, extremely warm temperatures can cause mortality and even slow developmental rates (Sanger et al. 2018).

Figure 1. An overview of our experimental design to understand how urban incubation regimes impact embryo development and survival. Eggs from both forest and city populations were factorially distributed into forest and city incubation treatments. At approximately a quarter of the way through development, some eggs were exposed to a spike in temperature measured from the field (either 39 or 43 °C peak). Eggs completed development at their assigned incubation profile (city vs. forest) and hatchling growth and survival were monitored in the lab for three months.

We collected breeding pairs of Puerto Rican crested anoles, bred them in the lab, and subjected their eggs to various incubation regimes that mimicked nest temperatures in forest and city habitats (see Figure 1 for experimental design). Some of our incubation treatments exposed embryos to an acute thermal stress (i.e. thermal spike) measured from the field (Fig. 2).

Figure 2. Thermal spikes in ground temperature measured in areas where lizards nest. We used the warmest thermal spike measured in our study area (peak of 43 °C) and one less extreme spike (39 °C peak) in our experiment. Other thermal spikes (grey lines) and mean daily nest temperatures in the city (blue) and forest (green) are provided for reference.

We found that the warmest thermal spikes can reduce egg survival as much as 24%; however, less extreme spikes (39 °C peak) had little impact on survival. Additionally, thermal spikes had a tendency to slow developmental rates. Even though eggs only experienced a thermal spike on a single day during development, incubation periods were longer for eggs experiencing a spike than controls (no spike) (Fig. 3).  Although developmental rates increase with temperature, embryos may slow or stop development at extremely high temperatures (i.e. diapause).

Figure 3. Incubation periods for each treatment. Green boxes show results for eggs incubated at cooler, forest temperatures and blue show results for eggs incubated at warmer, city temperatures. Controls experienced no thermal spike. Temperatures in parentheses are the peak temperature of the thermal spike for experimental groups. Lowercase letters denote statistical significance.

To better understand how embryo metabolism was impacted by thermal spikes, we measured heart rates of embryos before, during, and after a thermal spike. Heart rates skyrocketed during a thermal spike (Fig. 4a), which makes us doubt that diapause is the reason for reduced rates of development. However, heart rates were depressed by as much as 10% for up to 24 hours after a thermal spike (Fig. 4b). Thus, the reason for the reduction in developmental rates may be due to metabolic depression that comes after and not necessarily during the thermal spike. Although we’ve known for some time that extremely high temperatures slow development, our results show that extreme temperatures can have a lasting effect on developmental rates. What is needed now is to know exactly how long this metabolic depression lasts. Based on data collected since this study was conducted, it lasts at least 48 hours post-exposure.

Figure 4. Heart rates of anole embryos at the peak temperature of thermal spikes (Panel A) as well as 24 hours before (closed circles) and 24 hours after (open circles) a thermal spike (Panel B). Asterisks denote statistical significance for spiked treatments compared to controls (A) and for heart rates after a thermal spike compared to before (B).

It is important to note that no embryo could survive if incubated at either of these peak temperatures for an extended period of time. In fact, constant temperatures in excess of 34 °C likely result in total mortality. Reptile nest temperatures often exceed the maximum constant temperature that would allow for successful development (Angiletta et al 2013; Sanger et al 2018). Indeed, a followup study by Putter Tiatragul shows that anole nest temperatures in Miami regularly exceed 34 °C. Despite this knowledge, very little work has been done to discover how brief exposures to extreme nest temperatures influence patterns of development. Our work provides an ecologically meaningful and novel evaluation of how extreme temperatures impact development and advances our understanding of the impacts of urbanization on wildlife.

Andrews, R.M., 1982. Spatial variation in egg mortality of the lizard Anolis limifrons. Herpetologica, pp.165-171.

Andrews, R.M., 1988. Demographic correlates of variable egg survival for a tropical lizard. Oecologia, 76(3), pp.376-382.

Angilletta, M.J., Zelic, M.H., Adrian, G.J., Hurliman, A.M. and Smith, C.D., 2013. Heat tolerance during embryonic development has not diverged among populations of a widespread species (Sceloporus undulatus). Conservation physiology, 1(1).

Carlo, M.A., Riddell, E.A., Levy, O. and Sears, M.W., 2018. Recurrent sublethal warming reduces embryonic survival, inhibits juvenile growth, and alters species distribution projections under climate change. Ecology letters, 21(1), pp.104-116.

Chalcraft, D.R. and Andrews, R.M., 1999. Predation on lizard eggs by ants: species interactions in a variable physical environment. Oecologia, 119(2), pp.285-292.

Chejanovski, Z.A., Avilés-Rodríguez, K.J., Lapiedra, O., Preisser, E.L. and Kolbe, J.J., 2017. An experimental evaluation of foraging decisions in urban and natural forest populations of Anolis lizards. Urban Ecosystems, 20(5), pp.1011-1018.

Hall, JM, Warner, DA. 2018. ​Thermal spikes from the urban heat island increase mortality and alter physiology of lizard embryos. Journal of Experimental Biology . 221, jeb181552. doi:10.1242/jeb.181552

Lapiedra, O., Chejanovski, Z. and Kolbe, J.J., 2017. Urbanization and biological invasion shape animal personalities. Global change biology, 23(2), pp.592-603.

Sanger, T.J., Kyrkos, J., Lachance, D.J., Czesny, B. and Stroud, J.T., 2018. The effects of thermal stress on the early development of the lizard Anolis sagrei. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology.

Tiatragul, S., Kurniawan, A., Kolbe, J.J. and Warner, D.A., 2017. Embryos of non-native anoles are robust to urban thermal environments. Journal of thermal biology, 65, pp.119-124.

Tyler, R.K., Winchell, K.M. and Revell, L.J., 2016. Tails of the city: caudal autotomy in the tropical lizard, Anolis cristatellus, in urban and natural areas of Puerto Rico. Journal of Herpetology, 50(3), pp.435-441.

Winchell, K.M., Reynolds, R.G., Prado‐Irwin, S.R., Puente‐Rolón, A.R. and Revell, L.J., 2016. Phenotypic shifts in urban areas in the tropical lizard Anolis cristatellus. Evolution, 70(5), pp.1009-1022.

Winchell, K.M., Carlen, E.J., Puente‐Rolón, A.R. and Revell, L.J., 2018. Divergent habitat use of two urban lizard species. Ecology and evolution, 8(1), pp.25-35.

 

Joshua Hall
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