Too Hot to Nest? In a Hot Summer the Tortoise Chersina angulata Can Switch From Nesting to Facultative Viviparity

Abstract

In a captive colony of Chersina angulata in Cape Town, South Africa, we observed in 2015/16 retention of the last egg clutch inside the female until the hatching stage was reached, conforming to the generally accepted definition of viviparity. Retrospective climatic analysis indicates egg retention until the hatching stage co-occurred with unusually hot summer weather: the average air temperatures in December 2015 and January and February 2016 were higher than during the preceding five and the following 5 years when facultative viviparity could not be observed. Late December and January appears to be the critical period for females to either deposit their last clutch of the nesting season into a nest, or to retain the last clutch for embryonic development inside the female. Over the 28 December to 24 January period the minimum, average and maximum air temperatures in 2015–16 were about 3°C higher than in the five following years. This association of facultative viviparity with unusual summer heat suggests that hot ambient temperatures at the end of the nesting season may cue females to switch from oviposition to facultative viviparity. Compared to incubation in a nest this phenotypic plasticity of the reproductive mode—to retain during hot summers the season’s last clutch inside the female—may buffer the developing embryos from excessive heat exposure: females can thermo-regulate by moving among microhabitats whereas sun exposed shallow nests cannot escape high ground temperatures. This novel reproductive strategy has the potential to enhance the resilience of species to global warming.

A global analysis of viviparity in squamates highlights its prevalence in cold climates

“…For instance, the evolution of shelled (cleidoic) eggs promoted the expansion of tetrapods into terrestrial habitats (D'Alba et al, 2021), and the retention of eggs inside the body of the parent significantly improved embryo survivability (Sadleir, 1973;Shine, 2014). Live-bearing [viviparity, herein used to include ovoviviparity (i.e., retention of eggs in utero almost until hatching)] evolved across all major vertebrate clades, except archelosaurs (birds, crocodilians and turtles; Blackburn, 2015a;Shine, 2005; but see Kuchling & Hofmeyr, 2022). Viviparity is widespread in squamates (observed in c. 20% of lizard and snake species; Meiri et al, 2021;and see below).…”

A Review: Comparative Genomics and Physiology of Parity Mode Evolution in Amniotes

“…Additionally, Saiphos equalis is a reproductively bimodal skink that has an oviparous population with incubation times as short as 5 days, thus embryos spend significant time in utero with an eggshell (Smith et al, 2001). Another surprising example of eggshells being compatible with full embryonic development includes a report of a captive tortoise that retained viable eggs until the hatching stage (Kuchling & Hofmeyr, 2022).…”

Honoring the Legacy of Professor Margaretha Delina Hofmeyr (1950–2020)

“…Retha's keen intellect and robust foundation in physiological ecology and integrative biology (e.g., Gericke et al 1978; Hofmeyr 1985; Schumann et al 2005) helped her tackle the challenge of southern Africa's rich tortoise diversity, with 14 native taxa, many endemic, and several endangered species (Fritz et al 2022). Fostered by collaborations with esteemed colleagues Ernst Baard, Gerald Kuchling, and Uwe Fritz, Retha authored or coauthored more than 60 peer-reviewed chelonian articles with topics ranging from morphometrics and physiology to reproductive ecology, behavior, forensics, phylogeography, phylogenetics, genetics, evolution, and conservation (e.g., Hofmeyr 2004, 2009; Hofmeyr et al 2005; Leuteritz and Hofmeyr 2007; Loehr et al 2007; Fritz et al 2011; Henen et al 2013; Rhodin et al 2018; Kuchling and Hofmeyr 2022). Retha and colleagues also published 12 International Union for the Conservation of Nature Red List assessments for sub-Saharan chelonians in 2015 and 2018, and 9 tortoise assessments for South Africa's 2014 Atlas and Red List Assessments for South African Reptiles .…”

“…December through February; Hofmeyr 2004). There is evidence that C. angulata exhibit facultative viviparity (Kuchling and Hofmeyr 2022). Facultative viviparity in C. angulata is supported further here (Kuchling and Hofmeyr, this issue) via flexible embryonic development, including diapause and preovipositional development to Yntema stage 12.…”