Eggshell structure in Caiman latirostris eggs improves embryo survival during nest inundation

Abstract

Egg inundation often results in poor hatching success in crocodylians. However, how tolerant eggs are to submergence, and/or how eggshell ultrastructure may affect embryo survival when inundated, are not well understood. In this study, our objective was to determine if embryo survival in Caiman latirostris is affected by eggshell surface roughness, when eggs are submerged under water. Tolerance to inundation was tested early (day 30) versus late (day 60) in development, using eight clutches (four per time treatments), subdivided into four groups: (N ¼ 9 per clutch per treatment; 9 Â 4 ¼ 36 eggs per group). 'Rough' eggshell represented the natural, unmodified eggshell surface structure. 'Smooth' eggshell surface structure was created by mechanically sanding the natural rough surface to remove surface columnar elements and secondary layer features, e.g. irregularities that result in 'roughness'. When inundated by submerging eggs under water for 10 h at day 30, 'smooth' eggshell structure resulted in more than twice as many dead embryos (16 versus 6, smooth versus rough; N ¼ 36), and fewer than half as many healthy embryos (6 versus 13, smooth versus rough, respectively; N ¼ 36). By contrast, at day 60, inundation resulted in very low hatching success, regardless of eggshell surface structure. Only two hatchlings survived the inundation, notably in the untreated group with intact, rough eggshells. Inundation produced a high rate of malformations (58% at day 30), but did not affect hatchling size. Our results indicate that eggshell roughness enhances embryo survival when eggs are inundated early in development, but not late in development. Apparently, the natural surface 'roughness' entraps air bubbles at the eggshell surface during inundation, thereby facilitating gas exchange through the eggshell even when the egg is submerged under water.

Comparative crystallography suggests maniraptoran theropod affinities for latest Cretaceous European ‘geckoid’ eggshell

“…Schleich & Kästle ; Cedillo‐Leal et al . ). The crystals forming crocodylian eggshell are usually wedge shaped (Mikhailov ; Choi et al .…”

“…Experimental approaches to test its possible role(s), such as those implemented by Cedillo‐Leal et al . () for crocodylian eggshells, as well as detailed observations on the nesting microenvironments of megapodes and Gekko gecko , compared with those of other avian and gekkotan taxa, could help to clarify the evolutionary significance of eggshell ornamentation. This in turn might offer further insights into the reproductive palaeobiology of other dinosaurian and squamate clades with ornamented eggshells (Mikhailov ; Fernandez et al .…”

“Intracascaral space” an eggshell structure of Caiman latirostris eggs

“…Through the magnifying glass and SEM, we were able to distinguish structures already reported in previous studies for C. latirostris, such as the calcite layer crossed by pores and remains of protein membrane 3,6,7 . We also observed that eggshells had an ornamentation, made up of columnar structures, some of them joined by bridges (Fig.…”

Nesting environment may drive variation in eggshell structure and egg characteristics in the Testudinata

“…Interestingly, there is evidence that the morphology of the eggshell changes during incubation. The outer surfaces of crocodilian eggshells develop erosion craters as incubation progresses in association with an acidic environment created by rotting vegetation that forms the nest mound (Cedillo-Leal et al, 2017;Ferguson, 1981Ferguson, , 1985Schleich & Kästle, 1988). Avian eggs lose calcium carbonate due to embryonic dissolution of the inner part of the eggshell (Simkiss, 1980), which can even lead to changes in eggshell gas conductance as seen in megapode eggs (Booth & Thompson, 1991).…”

“…If the postulated hypothesis that shell thickness reflects the nesting environment has any validity then it should also apply to other reptilian taxa. Crocodilian eggshells are also thick for their egg mass (Figure 3) and the outer surface is regularly etched by the acidic conditions created by the decomposing nest materials (Cedillo-Leal et al, 2017;Ferguson, 1981Ferguson, , 1985Schleich & Kästle, 1988). Unincubated eggs or those incubated artificially outside of vegetation do not exhibit this erosion of the outer shell surface (Marzola, Russo, & Mateus, 2015).…”