Birds that lay long clutches (series of eggs laid sequentially before a "pause day"), among them the high-producing, strongly-calcifying Gallus gallus domesticus (domestic hen) and Coturnix coturnix japonica (Japanese quail), transfer about 10% of their total body calcium daily. They appear, therefore, to be the most efficient calcium-transporters among vertebrates. Such intensive transport imposes severe demands on ionic calcium (Ca2+) homeostasis, and activates at least two extremely effective mechanisms for Ca2+ transfer from food and bone to the eggshell. This review focuses on the development, action and regulation of the mechanisms associated with paracellular and transcellular Ca2+ transport in the intestine and the eggshell gland (ESG); it also considers some of the proteins (calbindin, Ca2+ATPase, Na+/Ca2+ exchange, epithelial calcium channels (TRPVs), osteopontin and carbonic anhydrase (CA) associated with this phenomenon. Calbindins are discussed in some detail, as they appear to be a major component of the transcellular transport system, and as only they have been studied extensively in birds. The review aims to gather old and new knowledge, which could form a conceptual basis, albeit not a completely accepted one, for our understanding of the mechanisms associated with this phenomenon. In the intestine, the transcellular pathway appears to compensate for low Ca2+ intake, but in birds fed adequate calcium the major drive for calcium absorption remains the electrochemical potential difference (ECPD) that facilitates paracellular transport. However, the mechanisms involved in Ca2+ transport into the ESG lumen are not yet established. In the ESG, the presence of Ca2+-ATPase and calbindin--two components of the transcellular transport pathway--and the apparently uphill transport of Ca2+ support the idea that Ca2+ is transported via the transcellular pathway. However, the positive (plasma with respect to mucosa) electrical potential difference (EPD) in the ESG, among other findings, indicates that there may be major alternative or complementary paracellular passive transport pathways. The available evidence hints that the flow from the gut to the ESG, which occurs during a relatively short period (11 to 14 h out the 24- to 25.5-h egg cycle), is primarily driven by carbonic anhydrase (CA) activity in the ESG, which results in high HCO3(-) content that, in turn, "sucks out" Ca2+ from the intestinal lumen via the blood and ESG cells, and deposits it in the shell crystals. The increased CA activity appears to be dependent on energy input, whereas it seems most likely that the Ca2+ movement is secondary, that it utilizes passive paracellular routes that fluctuate in accordance with the appearance of the energy-dependent CA activity, and that the level of Ca2+ movement mimics that of the CA activity. The on-off signals for the overall phenomenon have not yet been identified. They appear to be associated with the circadian cycle of gonadal hormones, coupled with the egg cycle: it is most likely that progesterone acts as the "off" signal, and that the "on" signal is provided by the combined effect of an as-yet undefined endocrine factor associated with ovulation and with the mechanical strain that results from "egg white" formation and "plumping". This strain may initially trigger the formation of the mammillae and the seeding of shell calcium crystals in the isthmus, and thereafter initiate the formation of the shell in the ESG.