Comparative aspects of calcium metabolism in embryonic reptiles and birds

Packard, Mary J.; Packard, Gary C.

doi:10.1007/978-94-009-6536-2_11

Cited by 60 publications

(29 citation statements)

References 61 publications

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“…Previous research on patterns of calcium provision to embryonic oviparous amniotes identified differences among archosaurian, chelonian and squamate reptiles in the distribution of calcium in oviposited eggs and in the contribution of these sources to embryonic nutrition (Packard and Packard, 1984;Packard, 1994;Packard and Clark, 1996). The defining characteristics for oviparous squamates that emerged from this work are the production of calcium-rich yolk as a primary source of calcium for embryonic development and calcium-poor eggshells.…”

Section: Discussionmentioning

confidence: 79%

Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara

Stewart

Ecay

Heulin

2009

Journal of Experimental Biology

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SUMMARYEmbryos of oviparous squamate reptiles typically obtain calcium from both yolk and eggshell but differ from other oviparous amniotes (turtles, birds and crocodilians) because they are heavily dependent on calcium-rich yolk. Eggs of viviparous squamates lack calcareous eggshells, and embryos receive calcium solely from yolk or from both yolk and placenta. The pattern of calcium mobilization by amniote embryos has been predicted to influence the evolution of viviparity if embryos are dependent on calcium from the eggshell and calcium placentotrophy evolves subsequent to viviparity. We studied the pattern of maternal provision and embryonic utilization of calcium of an oviparous and a viviparous population of the reproductively bimodal lizard Lacerta vivipara to test the hypotheses: (1) oviparous embryos are not dependent on eggshell calcium and (2) calcium content of viviparous hatchlings does not differ from oviparous hatchlings. Our findings do not support either of these hypotheses because oviparous females oviposited eggs with heavily calcified shells and calcium-poor yolk, and embryonic mobilization of shell calcium was greater than for other oviparous squamates. The calcium content of yolk from viviparous females did not differ from oviparous yolk, but viviparous eggs lacked calcareous eggshells. Uterine secretion by viviparous females compensated for the low calcium content of yolk, and placental calcium transfer was among the highest recorded for squamates. The pattern of calcium provision in these two populations suggests that dependence on uterine calcium, either stored temporarily in an eggshell or transferred directly across a placenta, did not constrain the evolution of reproductive mode in this lineage.

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Section: Discussionmentioning

confidence: 79%

Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara

Stewart

Ecay

Heulin

2009

Journal of Experimental Biology

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“…The chick CAM is formed as the result of the progressive fusion of the chorionic and allantoic membranes so that it consists of 3 distinct cellular layers : an ectodermal epithelium adjacent to the eggshell, a mesodermal middle layer belonging to both chorion and allantois, and an endodermal epithelium lining the allantoic cavity (Leeson & Leeson, 1963 ;Packard & Packard, 1984). By incubation d 10-11, the CAM surrounds the embryo and adheres to the acellular inner shell membrane (Freeman & Vince, 1974).…”

Section: mentioning

confidence: 99%

Specialised cell types in the chorioallantoic membrane express carbonic anhydrase during chick embryogenesis

et al. 2001

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The expression of carbonic anhydrase in the chorioallantoic membrane (CAM) of the chick embryo was investigated by means of the histochemical localisation of the enzyme catalytic sites and the immunohistochemical identification of its isoenzymatic forms. The results show that carbonic anhydrase is developmentally expressed in a subset of cells both in the ectodermal and the endodermal epithelium. The distribution patterns from both methodological approaches indicated that carbonic anhydrase is a marker of the villus cavity cells and the mitochondria-rich cells in the ectodermal and the endodermal epithelium, respectively. Such a cell-specific pattern of the enzyme expression provides a further contribution to characterising the heterogeneous cell population of the chick CAM and supports specific functional involvement for the distinct cell types in CAM-mediated processes, such as calcium transport, maintenance of acid-base balance and water and electrolyte reabsorption, during chick embryogenesis.

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“…Alternatively, squamate eggs are thinner and are largely composed of a fibrous layer (Lacerta vivipara: 50-70 /xm total, 87%-89% fibrous layer; A. childreni: 67-99 fim, 92'K)-96% fibrous layer; Heulin et al 2002; Table I). This difference is functionally significant because colubrid snake eggshells contribute only 23%-28% of hatchling calcium requirements, with the remainder being supplied by yolk (Packard and Packard 1984;Stewart et al 2004). Conversely, bird eggshells meet 62%-92% of hatchling calcium requirements (Packard and Packard 1984).…”

Section: Discussionmentioning

confidence: 97%

“…This difference is functionally significant because colubrid snake eggshells contribute only 23%-28% of hatchling calcium requirements, with the remainder being supplied by yolk (Packard and Packard 1984;Stewart et al 2004). Conversely, bird eggshells meet 62%-92% of hatchling calcium requirements (Packard and Packard 1984). Heavy deposits of calcium in the shell drastically reduce permeability and allow birds to use a broad range of nest sites (Paganelli 1991).…”

Section: Discussionmentioning

confidence: 98%

The Role of Python Eggshell Permeability Dynamics in a Respiration‐Hydration Trade‐Off

Stahlschmidt¹,

Heulin²,

DeNardo³

2010

Physiological and Biochemical Zoology

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Parental care is taxonomically widespread because it improves developmental conditions and thus fitness of offspring. Although relatively simplistic compared with parental behaviors of other taxa, python egg-brooding behavior exemplifies parental care because it mediates a trade-off between embryonic respiration and hydration. However, because egg brooding increases gas-exchange resistance between embryonic and nest environments and because female pythons do not adjust their brooding behavior in response to the increasing metabolic requirements of developing offspring, python egg brooding imposes hypoxic costs on embryos during the late stages of incubation. We conducted a series of experiments to determine whether eggshells coadapted with brooding behavior to minimize the negative effects of developmental hypoxia. We tested the hypotheses that python eggshells (1) increase permeability over time to accommodate increasing embryonic respiration and (2) exhibit permeability plasticity in response to chronic hypoxia. Over incubation, we serially measured the atomic and structural components of Children's python (Antaresia childreni) eggshells as well as in vivo and in vitro gas exchange across eggshells. In support of our first hypothesis, A. childreni eggshells exhibited a reduced fibrous layer, became more permeable, and facilitated greater gas exchange as incubation progressed. Our second hypothesis was not supported, as incubation O(2) concentration did not affect the shells' permeabilities to O(2) and H(2)O vapor. Our results suggest that python eggshell permeability changes during incubation but that the alterations over time are fixed and independent of environmental conditions. These findings are of broad evolutionary interest because they demonstrate that, even in relatively simple parental-care models, successful parent-offspring relationships depend on adjustments made by both the parent (i.e., egg-brooding behavioral shifts) and the offspring (i.e., changes in eggshell permeability).

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Comparative aspects of calcium metabolism in embryonic reptiles and birds

Cited by 60 publications

References 61 publications

Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara

Calcium provision to oviparous and viviparous embryos of the reproductively bimodal lizard Lacerta (Zootoca) vivipara

Specialised cell types in the chorioallantoic membrane express carbonic anhydrase during chick embryogenesis

The Role of Python Eggshell Permeability Dynamics in a Respiration‐Hydration Trade‐Off

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