Endocrinology of salt glond function

The journey of life, from primordial protoplasm to a complex vertebrate form, is a tale of survival against incessant alterations in climate, surface topography, food chain, and chemistry of the external environment. Kidneys present with an ensemble embodiment of the adaptations devised by diverse life-forms to cope with such challenges and maintain a chemical equilibrium of water and solutes, both in and outside the body. This minireview revisits renal evolution utilizing the classic: From Fish to Philosopher; the story of our internal environment, by Prof. Homer W. Smith (1895–1962) as a template. Prof. Smith’s views exemplified the invention of glomeruli, or its abolishment, as a mechanism to filter water. Moreover, with the need to preserve water, as in reptiles, the loop of Henle was introduced to concentrate urine. When compared to smaller mammals, the larger ones, albeit having loops of Henle of similar lengths, demonstrated a distinct packing of the nephrons in kidneys. Moreover, the renal portal system degenerated in mammals, while still present in other vertebrates. This account will present with a critique of the current concepts of renal evolution while examining how various other factors, including the ones that we know more about now, such as genetic factors, synchronize to achieve renal development. Finally, it will try to assess the validity of ideas laid by Prof. Smith with the knowledge that we possess now, and understand the complex architecture that evolution has imprinted on the kidneys during its struggle to survive over epochs.

The Unocal–Metrolink oil spill of 21 February 1995 resulted in approximately 7800 barrels of San Joaquin crude oil being deposited into the San Gabriel River in Huntington Beach, CA, USA. In order to determine long-term pathological effects of oil exposure and rehabilitation, hematological and serum biochemical parameters for both rehabilitated (RHB) American coots (Fulica americana) and reference (REF) coots were examined every 3–4 weeks (56, 81, 108 and 140 days post oil exposure) after birds were cleaned, rehabilitated and soft-released. Most significant differences in monthly comparisons between RHB and REF birds occurred 56 days following oil exposure. Total white blood cell (WBC) count, albumin:globulin (A:G) ratio and calcium concentration were higher in RHB birds compared to REF birds 56 days post oil exposure. In addition, mean cell hemoglobin (MCH), mean cell hemoglobin concentration (MCHC), alkaline phosphatase, alanine aminotransferase, aspartate aminotransferase and creatine kinase activities, and creatinine, total protein (TP) and globulin concentrations were lower in RHB birds. Blood results from 56 days post oil exposure for RHB coots which subsequently died were compared to blood results from days 108 and 140 for REF coots which survived. Oiled and rehabilitated birds which died had significantly higher WBCs, packed cell volume, TP and globulin concentrations, and lower A:G ratio, MCH, MCHC, glucose and sodium concentrations compared to REF birds which survived. Blood result differences detected at 3–4-week intervals between RHB and REF survivors, and differences detected between RHB coots which died and REF coots which survived, suggested that RHB coots developed an inflammatory response (infectious or non-septic) and, concurrently, may have experienced decreased immune responsiveness. Additionally, RHB coots experienced either an iron (Fe) utilization or Fe metabolism problem. These pathophysiological mechanisms were consistent with increased hemosiderin (stored Fe) present in the liver, spleen and kidney of necropsied RHB birds, and may have contributed to RHB coot mortality. When blood parameter differences were examined for their impact on survival time, it was determined that RHB coots had shorter survival times if they had very high cholesterol (⩾449 mg/dl) or chloride (⩾110 MEQ/l) concentrations on day 56 post oil exposure. Interestingly, the lack of differences between RHB and REF coots from day 81 through day 140 suggested that, from a hematologic and clinical chemistry perspective, coots which were oiled, rehabilitated, released and survived at least 3.5 months could not be differentiated from wild (REF) coots. From these findings it appears that blood analysis, coupled with post-release survival data, may help discern reasons for increased mortality of oiled and rehabilitated birds, compared to non-oiled reference birds.

This chapter describes structure, innervation, and functional control of avian salt glands. These supraorbitally located glands represent one of the most effective organs in the vertebrate kingdom involved in the epithelial transport of ions (sodium and chloride) against a marked concentration gradient. These glands are able to highly concentrate sodium and chloride from the perfusing bloodstream, thereby eliminating excess salt from body fluids at low water losses. In an orchestrated system together with the kidneys they help to maintain avian-body fluid homeostasis, and marine and estuarine birds cannot survive without them. The exact location of the avian salt-secreting gland in the head region differs depending on the species or its habitat. The avian salt gland represents a compound tubular gland, with its main excretory ducts branching into primary and secondary ducts forming the central canals of secretory lobes, which are composed of numerous radially arranged secretory tubules with small lumina merging into these central canals. The typical secretory tubule of the avian salt gland comprises five to eight cells radially arranged around a central lumen of 1–1.5 μm in diameter, thus forming a monolayered epithelial sheath.

Salt glands of ducks were induced to secrete sodium through the ingestion of salt water. In salt-adapted animals the administration of melanocyte-stimulating hormone (MSH) produced a rise in the sodium excreted by the salt gland, an effect which was not mimicked by adrenocorticotropin. Studies in vitro using incubations of gland slices and radioactive sodium ion showed that MSH increased sodium efflux, indicating that it acted directly upon the gland. We have previously observed that MSH has no effect on the pigmentary system of the duck. It is proposed that in the evolutionary process this hormone has acquired new target tissues in these birds.

Salt-adapted Pekin ducks were observed during 2-week period following adrenalectomy so as to test the hypothesis that NaCl secretion by the nasal salt glands depends on adrenocortical steroids. Three days after adrenalectomy the total inputs of fluid and Na⁺ during a 90-min iv infusion of 1000 mOsm/kg NaCl were 77 and 80% respectively, of those in the sham-operated controls; 7 days after adrenalectomy they were 88 and 90%. Two weeks after adrenalectomy, cardiovascular function had deteriorated slightly and the total outputs of fluid and Na⁺ had fallen to 65 and 64%, respectively, of the control outputs. The onset of cardiovascular deterioration was delayed by feeding the ducks 0.9% NaCl drinking water ad libitum for 1 month before, and 2 weeks after, adrenalectomy. Adaptive hypertrophy of the nasal salt glands was not steroid-dependent since there was no measurable decrease in the weight of the glands during a 2-week period following adrenalectomy.

• 1.

  1. One week after adrenalectomy, the total output of fluid and osmolytes by the nasal salt glands were 82 and 84% of the respective outputs by sham-adrenalectomized controls.

• 2.

  2. Three days after adrenalectomy, the total volume of solute-free water gained by the nasal salt glands was 77% of that gained by the sham-adrenalectomized controls; after 7 days it was 80%. Two weeks after adrenalectomy, the ducks lost some of their strength and the total volume decreased to 65%.

• 3.

  3. It was concluded that the primary secretion of NaCl and the conservation of solute-free water by the nasal salt glands are not regulated primarily by adrenocortical steroids.