Salt-water acclimation of the estuarine crocodile Crocodylus porosus involves enhanced ion transport properties of the urodaeum and rectum

ABSTRACT Estuarine crocodiles, Crocodylus porosus, inhabit freshwater, estuarine and marine environments. Despite being known to undertake extensive movements throughout and between hypo-osmotic and hyperosmotic environments, little is known about the role of the cloaca in coping with changes in salinity. We report here that, in addition to the well-documented functional plasticity of the lingual salt glands, the middle of the three cloacal segments (i.e. the urodaeum) responds to increased ambient salinity to enhance solute-coupled water absorption. This post-renal modification of urine serves to conserve water when exposed to hyperosmotic environments and, in conjunction with lingual salt gland secretions, enables C. porosus to maintain salt and water balance and thereby thrive in hyperosmotic environments. Isolated epithelia from the urodaeum of 70% seawater-acclimated C. porosus had a strongly enhanced short-circuit current (an indicator of active ion transport) compared with freshwater-acclimated crocodiles. This enhanced active ion absorption was driven by increased Na+/K+-ATPase activity, and possibly enhanced proton pump activity, and was facilitated by the apical epithelial Na+ channel (ENaC) and/or the apical Na+/H+ exchanger (NHE2), both of which are expressed in the urodaeum. NHE3 was expressed at very low levels in the urodaeum and probably does not contribute to solute-coupled water absorption in this cloacal segment. As C. porosus does not appear to drink water of salinities above 18 ppt, observations of elevated short-circuit current in the rectum as well as a trend for increased NHE2 expression in the oesophagus, the anterior intestine and the rectum suggest that dietary salt intake may stimulate salt and possibly water absorption by the gastrointestinal tract of C. porosus living in hyperosmotic environments. Summary: The crocodile Crocodylus porosus responds to increased salinity by enhancing solute-coupled water absorption in the urodaeum; this response serves to conserve water and enables them to thrive in hyperosmotic environments.

[1]  G. Grigg,et al.  Biology and Evolution of Crocodylians , 2015 .

[2]  H. Onken,et al.  Osmoregulation and excretion. , 2014, Comprehensive Physiology.

[3]  C. Franklin,et al.  Home Range Utilisation and Long-Range Movement of Estuarine Crocodiles during the Breeding and Nesting Season , 2013, PloS one.

[4]  C. Franklin,et al.  Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands of Crocodylus porosus following chronic saltwater acclimation , 2010, Journal of Experimental Biology.

[5]  C. Franklin,et al.  Ecological and physiological determinants of dive duration in the freshwater crocodile , 2010 .

[6]  Shu-chen Wu,et al.  Ammonium-dependent sodium uptake in mitochondrion-rich cells of medaka (Oryzias latipes) larvae. , 2010, American journal of physiology. Cell physiology.

[7]  C. Wood,et al.  A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins , 2009, Journal of Experimental Biology.

[8]  Hamish A. Campbell,et al.  Remote monitoring of crocodilians: implantation, attachment and release methods for transmitters and data-loggers , 2009 .

[9]  C. Franklin,et al.  Functional and morphological plasticity of crocodile (Crocodylus porosus) salt glands , 2008, Journal of Experimental Biology.

[10]  Gordon C. Grigg,et al.  Satellite Tracking Reveals Long Distance Coastal Travel and Homing by Translocated Estuarine Crocodiles, Crocodylus porosus , 2007, PloS one.

[11]  N. Møbjerg,et al.  Application of the Na+ recirculation theory to ion coupled water transport in low- and high resistance osmoregulatory epithelia. , 2007, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[12]  Sheng Zhao,et al.  Comprehensive Algorithm for Quantitative Real-Time Polymerase Chain Reaction , 2005, J. Comput. Biol..

[13]  E. Cragoe,et al.  Amiloride and its analogs as tools in the study of ion transport , 1988, The Journal of Membrane Biology.

[14]  L. Taplin Sodium and water budgets of the fasted estuarine crocodile,Crocodylus porosus, in sea water , 1985, Journal of Comparative Physiology B.

[15]  L. Taplin Homeostasis of plasma electrolytes, water and sodium pools in the Estuarine Crocodile, Crocodylus porosus, from fresh, saline and hypersaline waters , 1984, Oecologia.

[16]  G. Grigg Plasma homeostasis and cloacal urine composition inCrocodylus porosus caught along a salinity gradient , 1981, Journal of comparative physiology.

[17]  C. Wood,et al.  Copper uptake across rainbow trout gills: mechanisms of apical entry. , 2002, The Journal of experimental biology.

[18]  C. Franklin,et al.  Morphology of the cloaca in the estuarine crocodile, Crocodylus porosus, and its plastic response to salinity , 2000, Journal of morphology.

[19]  S. Nedergaard,et al.  Role of lateral intercellular space and sodium recirculation for isotonic transport in leaky epithelia. , 2000, Reviews of physiology, biochemistry and pharmacology.

[20]  C. Wood,et al.  Mechanism of branchial apical silver uptake by rainbow trout is via the proton-coupled Na+channel. , 1999, American journal of physiology. Regulatory, integrative and comparative physiology.

[21]  S. Nedergaard,et al.  Sodium Recirculation and Isotonic Transport in Toad Small Intestine , 1999, The Journal of Membrane Biology.

[22]  C. Wood,et al.  Mechanism of branchial apical silver uptake by rainbow trout is via the proton-coupled Na(+) channel. , 1999, The American journal of physiology.

[23]  C. Franklin,et al.  Kidney and Cloaca Function in the Estuarine Crocodile (Crocodylus porosus) at Different Salinities: Evidence for Solute-linked Water Uptake , 1998 .

[24]  G. Grigg,et al.  Differences in renal-cloacal function between Crocodylus porosus and Alligator mississippiensis have implications for crocodilian evolution , 1997, Journal of Comparative Physiology B.

[25]  C. Franklin,et al.  Increased vascularity of the lingual salt glands of the estuarine crocodile, Crocodylus porosus, kept in hyperosmotic salinity , 1993, Journal of morphology.

[26]  L. Taplin Drinking of fresh water but not seawater by the estuarine crocodile (Crocodylus porosus) , 1984 .