Functional and morphological plasticity of crocodile (Crocodylus porosus) salt glands

Abstract

SUMMARYThe estuarine crocodile, Crocodylus porosus, inhabits both freshwater and hypersaline waterways and maintains ionic homeostasis by excreting excess sodium and chloride ions via lingual salt glands. In the present study, we sought to investigate the phenotypic plasticity, both morphological and functional, in the lingual salt glands of the estuarine crocodile associated with chronic exposure to freshwater (FW) and saltwater (SW) environments. Examination of haematological parameters indicated that there were no long-term disruptions to ionic homeostasis with prolonged exposure to SW. Maximal secretory rates from the salt glands of SW-acclimated animals (100.8±14.7·mol·100·g ). There were no differences in the mass-specific metabolic rate of salt gland tissue slices from FW-and SW-acclimated animals (558.9±49.6 and 527.3±142.8·l·O 2 ·g -1 ·h -1 , respectively). Stimulation of the tissue slices from SW-acclimated animals by methacholine resulted in a 33% increase in oxygen consumption rate. There was no significant increase in the metabolic rate of tissues from FW-acclimated animals in response to methacholine. Morphologically, the secretory cells from the salt glands of SW-acclimated animals were larger than those of FW-acclimated animals. In addition, there were significantly more mitochondria per unit volume in secretory tissue from SW-acclimated animals. The results from this study demonstrate that the salt glands of C. porosus are phenotypically plastic, both morphologically and functionally and acclimate to changes in environmental salinity.

Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands ofCrocodylus porosusfollowing chronic saltwater acclimation

“…The in vitro oxygen consumption rate of salt gland tissue slices was measured to determine both the energy costs associated with chronic SW acclimation and the relative energy costs associated with maintaining NKA activity in the tissue. Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008).…”

“…Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008). The absence of any increase in the rate of oxygen consumption by salt gland slices from SW-acclimated C. porosus contrasts with results from the avian literature which show that salt loading correlates with a marked increase in tissue oxygen consumption rates (Hootman and Ernst, 1980).…”

“…In addition, NKA a-subunit mRNA abundance increased following squid ingestion; mRNA transcript abundance gradually increased over the first 2 days following feeding, peaked at 5 days (90% more than in controls), and at day 10 there was still 50% more transcript in the rectal glands of fed animals relative to fasted controls (MacKenzie et al, 2002). In the present study, animals were fed neonate mice, which have a Na + content within the range of diets naturally experienced by animals living in hypersaline environments (Grigg et al, 1986;Cramp et al, 2008). However, for the purposes of other experiments not reported here animals were killed several days after the ingestion of the last meal.…”

Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands ofCrocodylus porosusfollowing chronic saltwater acclimation

“…The in vitro oxygen consumption rate of salt gland tissue slices was measured to determine both the energy costs associated with chronic SW acclimation and the relative energy costs associated with maintaining NKA activity in the tissue. Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008).…”

“…Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008). The absence of any increase in the rate of oxygen consumption by salt gland slices from SW-acclimated C. porosus contrasts with results from the avian literature which show that salt loading correlates with a marked increase in tissue oxygen consumption rates (Hootman and Ernst, 1980).…”

“…In addition, NKA a-subunit mRNA abundance increased following squid ingestion; mRNA transcript abundance gradually increased over the first 2 days following feeding, peaked at 5 days (90% more than in controls), and at day 10 there was still 50% more transcript in the rectal glands of fed animals relative to fasted controls (MacKenzie et al, 2002). In the present study, animals were fed neonate mice, which have a Na + content within the range of diets naturally experienced by animals living in hypersaline environments (Grigg et al, 1986;Cramp et al, 2008). However, for the purposes of other experiments not reported here animals were killed several days after the ingestion of the last meal.…”

Effects of chronic exposure to 12‰ saltwater on the endocrine physiology of juvenile American alligator (Alligator mississippiensis)

“…Whether that reduced salivary secretion rate is unknown, but data from this study support that lingual glands in juvenile alligators do not become functional salt glands in saline environments. Results contrast findings from SW-acclimated C. porosus where increases in secretory tubule size, increased mitochrondrial numbers and plasma membrane surface area were correlated with increased functional activity of lingual salt glands (Cramp et al, 2007(Cramp et al, , 2008.…”

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

“…Further, juvenile C. porosus in captivity successfully acclimate to FW as well as hypersaline water and maintain near-constant osmoregulatory balance. We demonstrate that, in addition to the well-documented plasticity of the lingual salt glands (Cramp et al, 2010;Cramp et al, 2008;Franklin and Grigg, 1993), the mucosal epithelium of the urodaeum is also plastic and that both organs change to accommodate salt and water balance in hyperosmotic environments. Marked stimulation of an absorptive I sc by the urodaeum supports previous suggestions of enhanced solute-coupled water absorption (Kuchel and Franklin, 1998) in this cloacal segment of SW-exposed C. porosus.…”

Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands ofCrocodylus porosusfollowing chronic saltwater acclimation

“…The in vitro oxygen consumption rate of salt gland tissue slices was measured to determine both the energy costs associated with chronic SW acclimation and the relative energy costs associated with maintaining NKA activity in the tissue. Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008).…”

“…Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008). The absence of any increase in the rate of oxygen consumption by salt gland slices from SW-acclimated C. porosus contrasts with results from the avian literature which show that salt loading correlates with a marked increase in tissue oxygen consumption rates (Hootman and Ernst, 1980).…”

“…In addition, NKA a-subunit mRNA abundance increased following squid ingestion; mRNA transcript abundance gradually increased over the first 2 days following feeding, peaked at 5 days (90% more than in controls), and at day 10 there was still 50% more transcript in the rectal glands of fed animals relative to fasted controls (MacKenzie et al, 2002). In the present study, animals were fed neonate mice, which have a Na + content within the range of diets naturally experienced by animals living in hypersaline environments (Grigg et al, 1986;Cramp et al, 2008). However, for the purposes of other experiments not reported here animals were killed several days after the ingestion of the last meal.…”

Effects of chronic exposure to 12‰ saltwater on the endocrine physiology of juvenile American alligator (Alligator mississippiensis)

“…Whether that reduced salivary secretion rate is unknown, but data from this study support that lingual glands in juvenile alligators do not become functional salt glands in saline environments. Results contrast findings from SW-acclimated C. porosus where increases in secretory tubule size, increased mitochrondrial numbers and plasma membrane surface area were correlated with increased functional activity of lingual salt glands (Cramp et al, 2007(Cramp et al, , 2008.…”

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

“…Further, juvenile C. porosus in captivity successfully acclimate to FW as well as hypersaline water and maintain near-constant osmoregulatory balance. We demonstrate that, in addition to the well-documented plasticity of the lingual salt glands (Cramp et al, 2010;Cramp et al, 2008;Franklin and Grigg, 1993), the mucosal epithelium of the urodaeum is also plastic and that both organs change to accommodate salt and water balance in hyperosmotic environments. Marked stimulation of an absorptive I sc by the urodaeum supports previous suggestions of enhanced solute-coupled water absorption (Kuchel and Franklin, 1998) in this cloacal segment of SW-exposed C. porosus.…”

Activity, abundance, distribution and expression of Na+/K+-ATPase in the salt glands ofCrocodylus porosusfollowing chronic saltwater acclimation

“…The in vitro oxygen consumption rate of salt gland tissue slices was measured to determine both the energy costs associated with chronic SW acclimation and the relative energy costs associated with maintaining NKA activity in the tissue. Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008).…”

“…Consistent with a previous study (Cramp et al, 2008), chronic SW acclimation had no impact on the in vitro mass-specific metabolic rate of salt gland tissue slices. Used as an indirect measure of salt gland activity, the rate of oxygen consumption by isolated salt gland tissue slices from SW-acclimated crocodiles suggests that there was no apparent increase in cellular activity levels from that seen in FW-acclimated crocodiles, despite an increased capacity for salt secretion (Cramp et al, 2008). The absence of any increase in the rate of oxygen consumption by salt gland slices from SW-acclimated C. porosus contrasts with results from the avian literature which show that salt loading correlates with a marked increase in tissue oxygen consumption rates (Hootman and Ernst, 1980).…”

“…In addition, NKA a-subunit mRNA abundance increased following squid ingestion; mRNA transcript abundance gradually increased over the first 2 days following feeding, peaked at 5 days (90% more than in controls), and at day 10 there was still 50% more transcript in the rectal glands of fed animals relative to fasted controls (MacKenzie et al, 2002). In the present study, animals were fed neonate mice, which have a Na + content within the range of diets naturally experienced by animals living in hypersaline environments (Grigg et al, 1986;Cramp et al, 2008). However, for the purposes of other experiments not reported here animals were killed several days after the ingestion of the last meal.…”

Effects of chronic exposure to 12‰ saltwater on the endocrine physiology of juvenile American alligator (Alligator mississippiensis)

“…Whether that reduced salivary secretion rate is unknown, but data from this study support that lingual glands in juvenile alligators do not become functional salt glands in saline environments. Results contrast findings from SW-acclimated C. porosus where increases in secretory tubule size, increased mitochrondrial numbers and plasma membrane surface area were correlated with increased functional activity of lingual salt glands (Cramp et al, 2007(Cramp et al, , 2008.…”

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

“…Further, juvenile C. porosus in captivity successfully acclimate to FW as well as hypersaline water and maintain near-constant osmoregulatory balance. We demonstrate that, in addition to the well-documented plasticity of the lingual salt glands (Cramp et al, 2010;Cramp et al, 2008;Franklin and Grigg, 1993), the mucosal epithelium of the urodaeum is also plastic and that both organs change to accommodate salt and water balance in hyperosmotic environments. Marked stimulation of an absorptive I sc by the urodaeum supports previous suggestions of enhanced solute-coupled water absorption (Kuchel and Franklin, 1998) in this cloacal segment of SW-exposed C. porosus.…”