GENERAL
AND
COMPARATIVE
Hormones
ENDOCRINOLOGY
25,
249-258 (1975)
and Osmoregulation
in Marine
Birds1,2
W. N. HOLMES Department of Biological Sciences, University of California, Santa Barbara, California 93106 Accepted October 15, 1974 The neural and hormonal mechanisms responsible for the control of electrolyte excretion by the nasal glands of marine birds are outlined. At least three stages in the sequence of events leading to excretion, and therefore successful adaption to the marine environment, are sensitive to the presence of environmental pollutants and pathogens. The initiation and continuation of nasal gland function depends on the development of increased rates of Na+ and water transfer across the small intestinal mucosa. This adaptive response is sensitive to the presence of crude oil and crude oil distillation fractions and ingestion of these substances may prevent the development of increased rates of intestinal transfer. Degradation products of DDT may also inhibit the normal pattern of adrenal steroid biosynthesis and thus lead to impaired nasal gland function. Ingestion of the neurotoxin produced by Clostridium botulinum inhibits the release of acetylcholine and therefore blocks the essential visceral motor impulses to the nasal gland function. Thus, when intoxicated birds are fed either hypertonic saline or “pothole” drinking water derived from many prairie sloughs and lakes, they show higher rates of mortality than do similarly intoxicated birds given fresh drinking water.
In the freshwater-maintained duck, hyperosmotic urine is produced rarely, even under conditions of extreme antidiuresis (Holmes and Adams, 1963; Holmes, Fletcher, and Stewart, 1968; Bradley, Holmes, and Wright, 1971). Upon exposure to a diet containing hypertonic saline drinking water, however, the pattern of renal excretion changes and a urine which is slightly hyperosmotic with respect to plasma is produced (Holmes et a/., 1968). The mean osmotic pressure of this urine is approximately 0.4 Osm/liter, but the available osmotic space is such that the limiting isorrheic concentration of Na+ is always less than that necessary 1 This work was supported by research grants from the U.S. National Science Foundation (Grant No. GB 20806), Committee on Research, University of California and the American Petroleum Institute, Washington, DC. * A report based on this paper was given at the Seventh Symposium on Comparative Endocrinology, Tsavo National Park, Kenya in July 1974.
to excrete all of the ingested Na+ via the kidneys (Holmes et al., 1968). Thus, the osmotic imbalance which may occur in a hypothetical bird attempting to excrete via the kidneys all of the osmotic activity in 1 liter of ingested seawater is depicted in Fig. 1. Clearly, a supplementary or extrarenal excretory mechanism is necessary to ensure homeostasis in a marine bird or a freshwater bird adapting to a diet where the drinking water is hyperosmotic. The extrarenal excretory organs in birds are developed from paired nasal glands situated in the orbit. In terrestrial and freshwater species, these glands may be nonfunctional, but, in coastal and pelagic birds, aquatic birds living in regions where lake water is alkaline and hyperosmotic, and in some species of terrestrial birds living in arid environments, the glands are functional excretory organs and their degree of development is commensurate with the osmotic load the species must excrete extrarenally. Although early investigators ob249
Copyright @ 1975 by Academic Press, Inc. AU rights of repmduction in my form reserved.
250
W.
Total Net
excretion: loss:
1.5 liter
1.0
Orm
N.
in 2 5 liter
welter
1.0
Orm
FIG. 1. A representation of the osmotic imbalance which would occur in a marine bird attempting to excrete the electrolyte contained in ingested seawater via the renal pathway alone.
served that the size of the nasal gland declined when marine birds were fed fresh water (Heinroth and Heinroth, 1927; Schildmacher, 1932), their physiological significance was not realized until 1958. At that time Schmidt-Neilsen and his coworkers described the excretory function of the nasal glands in the cormorant (Phafacrocorax auritus), and later their observations were confirmed in other species of marine birds including the duck (Flnge, Schmidt-Neilsen, and Robinson, 1958; Schmidt-Neilsen, Jorgensen, and Osaki, 1958; Scothorne, 1959; Schmidt-Neilsen, 1960). When functioning, the glands secrete a hyperosmotic fluid containing Na+, K+, and Cl- at concentrations higher than those found in seawater, and their ability to excrete a large fraction of the electrolytes ingested complements the limited, although essential, excretory capacity of the kidneys. Thus, the combined activities of the renal and extrarenal pathways will not only enable a bird to excrete all the electrolytes in 1 liter of ingested seawater, but will also yield sufficient free water to balance the respiratory and fecal water losses (Fig. 2). The essential role of the extrarenal pathway in birds fed hyperosmotic drinking water is emphasized when the
HOLMES
nasal glands are removed surgically (Ballantyne and Wood, 1968; Bradley and Holmes, 1972). Such birds seldom survive more than 4 days, and during the first 3 days after exposure to hypertonic drinking water they become severely dehydrated, lose body weight, and show a continuous increase in the concentration of total osmotically active material in plasma. Since the glandless birds can only osmoregulate via the kidneys, the volume of urine necessary to excrete the ingested electrolytes exceeds the volume of water drunk. Therefore, the birds become progressively dehydrated as outlined previously in Fig. 1. Even though functional nasal glands may be present in a species, they will normally remain inactive as long as adequate quantities of fresh water are available. Soon after hypertonic drinking water is ingested for the first time, however, the glands begin to secrete fluid and prolonged exposure to this diet causes them to enlarge, differentiate structurally, and become more efficient as excretory organs. Changes in the protein, DNA, and RNA content of these developing nasal glands indicate that both hypertrophy and hyperplasia of the tubular secretory cells contribute to their growth (Ellis, Goertemiller, Total Net
excretion: win:
0
1.0
Orm
in 0.85
liter
15 liter water
litw
containing
:: . .
. LL
Y N.rol
Urine 0.25
liter
containing
1.0 Orm
0 1 Own
0.6
her
gland coMc2ininQ
flwd
0.9 Own
2. A representation of the osmotic balance which is achieved when a marine bird utilizes both the renal and the extrarenal pathways to excrete the electrolytes in ingested seawater. FIG.
OSMOREGULATION
DeLellis, and Kablotsky, 1963; Holmes and Stewart, 1968). Early in the adaptive process, the secretory cells of the developing nasal gland also show increases in the activities of some mitochondrial and cytoplasmic enzyme systems, and increases in the activity of an Na+-K+-dependent adenosine triphosphatase (ATPase) system in the membranes is correlated closely with the ability of the glands to secrete Na+, K+, and Cl- (Ellis et al., 1963: Hokin, 1963; Bonting, Caravaggio, Canady, and Hawkins, 1964; Chance, Lee, Oshino, and Van Rossum, 1964; Ernst, Goertemiller, and Ellis, 1967; Fletcher, Stainer, and Holmes, 1967; Ballantyne and Wood, 1968, 1970; Stainer, Ensor, Phillips, and Holmes, 1970). Indeed, the gland seems to be functionally dependent upon the activity of this ATPase system for, when G-strophanthin is injected into the nasal gland of the Herring gull, the positive potential which exists between the excretory fluid and the blood is abolished and the secretion of Na+ ceases (Van Rossum, 1966). When fully adapted birds are returned to a fresh water diet, the nasal glands once more assume the characteristics of those in birds maintained continuously on fresh water and, if these birds are given hypertonic drinking water for a second time, high levels of enzyme activity in the tissue and high rates of electrolyte excretion by the gland are reestablished rapidly (Fletcher et al., 1967; Holmes and Stewart, 1968). Although osmotic loads administered parenterally will elicit a secretion of nasal gland fluid, stimulation occurs normally through the reabsorption of hypertonic fluid from the gastrointestinal tract. The small intestine is the principal site of this reabsorption, and any decrease in its absorptive properties will affect adversely the initiation of nasal gland function and the ultimate adaptation of the organism to a marine environment. For example, the intestinal uptake mechanisms of the duck
IN MARINE
251
BIRDS
become impaired following thyroidectomy and, when a single oral load of hypertonic saline is given to these birds, the onset of nasal gland secretion is delayed and the secretory response of the glands is diminished (Ensor, Thomas, and Phillips, 1970). Further, chronic exposure to a hypertonic saline diet causes the mucosal transfer rates of Na+ and water to increase (Fig. 3). These increases occur first in the anterior segments of the small intestine but later the more posterior segments show similar increases and after 2 days the mucosal transfer rates throughout the whole of the small intestine are 60-100% higher than those found in the corresponding segments from ducklings maintained continuously on fresh water (Fig. 3). These characteristic increases in mucosal transfer rates, however, do not occur if the ducklings are treated with spironolactone before transfer to the hypertonic drinking water and the nasal glands in these birds do not seem- to become fully functional (Fig. 4; Cracker and Holmes, 1971). Therefore, not only are normal absorptive properties in the intestinal mucosa dependent on the action of the thyroid, but also the development of the adaptive response Frerhwoter --*
0
I
2
Seawater
3
4
5
Freshwater
6
7
8
9
10
.
I1
12
T,me (doyrl
FIG. 3. The percentage increase in water transfer across the small intestinal mucosa of ducklings during the period of adaptation to hypertonic saline and freshwater regimens. The rate of mucosal transfer is uniform along the length of the small intestine of freshwater-maintained birds, but during adaptation of the bird to hypertonic saline the increment in mucosal transfer is greater in the anterior than in the posterior segments of the small intestine (from Cracker and Holmes, 1971).
252
W.
N.
4. The effect of spironolactone on the transfer of water across the small intestinal mucosa of ducklings maintained for 24 hr on hypertonic saline equivalent to 60% seawater. The values represent mean transfer rates for the whole of the small intestine (from Cracker and Holmes, 1971). FIG.
in this tissue may depend on the direct action of an adrenocortical steroid. Since seawater-adapted ducklings ingest each day the same volume of water as freshwater-maintained birds, the adaptive significance of an increased mucosal transfer rate is not immediately apparent. The following hypothesis, based mainly on mammalian studies, is an attempt to explain this paradox in terms of the sequence of events occurring in the gastrointestinal tract following the ingestion of drinking
HOLMES
water (Cm-ran and Solomon, 1957; Code, Bass, McClary, Newman, and Davis, 1960; Curran, 1960; Hindle and Code, 1962). During the passage of ingested fresh water through the proventriculus and the duodenum, gastric and pancreatic secretions will be added and the electrolyte concentration of the fluid leaving the duodenum will be increased so that its osmotic pressure will approximate that of the surrounding extracellular fluid. The active uptake of Na+ from the intestinal fluid by the epithelial cells of the mucosa will cause water to flow passively from the lumen to the extracellular compartment (Cur-ran and Solomon, 1957; Cur-ran, 1960). Clearly, the activity of the Na+ uptake mechanism will determine the volume of water that can diffuse out of the gut lumen and into the tissues. Thus, under freshwater conditions, a volume approximately equal to that ingested plus the combined volumes of the gastric and pancreatic juices must be absorbed from the intestine to yield to the tissues a net volume equal to that ingested (Fig. 5). When the bird drinks seawater, however, the ingested fluid will be diluted by the passive movement of water from the tissues into the lumen of the gastrointestinal tract (Code et al., 1960; Hindle
Freshwater-adapted Sscrefionr ., ._ ,_ :I:::
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5. A schematic representation of the uptake of water from the gastrointestinal tract of a bird drinking fresh water (upper) and a bird drinking a similar volume of seawater (lower). FIG.
OSMOREGULATION
and Code, 1962). This will continue until the fluid has been diluted to the same concentration as the fluid in the surrounding tissues and the final volume entering the small intestine will be much greater than the volume ingested (Fig. 5). Thus, in order to gain a volume of water equal to that ingested, a bird drinking seawater must transfer out of its intestine and into its tissues a larger volume of fluid than a bird drinking fresh water. In other words, the rate of Na+ and water absorption by the intestinal mucosa must increase if the bird is to adapt successfully to the marine environment. The combined effect of water moving into the gut to dilute the hypertonic drinking water, and Na+ being reabsorbed into the extracellular space from the contents of the small intestine, is to increase the plasma osmolality. This change in plasma osmolality is believed to stimulate an osmoreceptor in the central nervous system. From the central receptor impulses are presumed to pass along two motor pathways. The first is a visceral motor pathway associated with the facial branch of the VIIth cranial nerve. Direct electrical stimulation of this nerve or the parenteral administration of cholinergic and parasympathomimetic drugs stimulate the secretion of nasal gland fluid in the unloaded bird. On the other hand, cholinergic blocking agents, sympathomimetic drugs, general anesthesia, denervation of the gland, and decerebration inhibit nasal gland function in birds that have been loaded previously with hypertonic saline (Fange et al., 1958; Schmidt-Nielsen, 1960; Ash, Pearce, and Silver, 1969; Hanwell, Linzell, and Peaker, 1971). The effects of parasympathetic stimulation appear to be partly vasomotor, and some investigators have postulated that an increase in blood flow to the gland would make more Na+ available to the Na+-K+dependent ATPase system and thus enhance the active transport of Na+ (FPnge,
IN
MARINE
BIRDS
253
Krog, and Reite, 1963; Bonting et al., 1964; Hanwell et al., 1971). Nerve endings, however, terminate on the principal cells within the nasal glands (Fawcett, 1962), and cholinergic agents increase the oxygen consumption, the activity of the phosphatidic acid cycle, and the Na+transporting abilities in the nasal gland tissue (Hokin and Hokin, 1959, 1960; Borut and Schmidt-Nielsen, 1963; Van Rossum, 1966). Although a cholinergic mechanism is essential for nasal gland function, this normal secretory response of the gland in the duck also depends on a second motor pathway associated with the adenohypophysialadrenocortical axis (Wright, Phillips, and Huang, 1966; Holmes, Lockwood, and Bradley, 1972). Removal of the adenohypophysis reduces the secretion of nasal gland fluid, and treatment of adenohypophysectomized ducks with ACTH restores the extrarenal excretory response to normal (Holmes, Lockwood and Bradley, 1972). Unilateral adrenalectomy in the duck also attenuates the extrarenal response to hypertonic saline, and the response is abolished almost completely when the bird is totally adrenalectomized. Corticosteroid replacement therapy in the totally adrenalectomized bird restores nasal gland secretion to normal, and nasal gland secretion in the intact duck is augmented significantly when either cortisol, cortexone, corticosterone, or ACTH is administered along with the hypertonic saline load (Holmes, Phillips, and Butler, 1961; Phillips, Holmes, and Butler, 1961; Bellamy and Phillips, 1966; Peaker, Peaker, Phillips, and Wright, 1971). The events leading to the secretion of nasal gland fluid in the marine bird are summarized in Fig. 6. At least three physiological events involved in the control mechanisms leading to normal nasal gland function are sensitive to some pathogens and pollutants present in the environment. These are (1)
254
W.
N.
HOLMES
.o Corticorterone
Ormottc laod
FIG. 6. A summary in marine birds.
Nor01 gland 7 No+ & K+excrebn
K+excrehon
of the possible
pathways
involved
the intestinal uptake of Na+ and water, (2) the biosynthesis of corticosteroids in the adrenal, and (3) the cholinergic control of nasal gland secretion (Fig. 6). The magnitude of the increment of mucosal transfer necessary for successful adaptation to the marine environment must be proportional to the amount of Na+ ingested in drinking water. Any interference with the development or maintenance of this adaptive change will limit the ability of the organism to survive. We have examined recently the effects of small volumes of ingested crude oil on the intestinal transfer rates of freshwater- and seawatermaintained ducklings (Cracker, Cronshaw,
in the initiation
and regulation
of nasal gland
secretion
and Holmes, 1974). Although the administration of crude oil had no effect on the basal rate of mucosal transfer in ducklings maintained on freshwater, the adaptive response in birds given seawater was inhibited (Fig. 7). This effect was apparent 24 hr after the oil was administered, and experimental evidence showed that the effect of a single dose persisted for at least 4 days (Fig. 7). Furthermore, the increment in mucosal transfer rate developed during a previous 3-day exposure to hypertonic drinking water was abolished 24 hr after a single dose of crude oil had been given (Fig. 7). The degree of inhibition varied with crude oils from different locations and
25 r
Experimenl
I
Experiment
2
Experiment
3
FIG. 7. The effect of a single oral dose (0.2 ml) of Santa Barbara crude oil on the mean rates of mucosal transfer in the small intestine of ducklings maintained on either fresh water or seawater. In Expts 1 and 2 the transfer rates were measured 24 hr and 4 days, respectively, after the oil was given, and in Expt 3 the birds were allowed to adapt to seawater for 3 days, the oil was given at the beginning of the fourth day of adaptation, and the mucosal transfer rates were determined 24 hr later (from Cracker, Cronshaw, and Holmes, 1974).
OSMOREGULATION
IN MARINE
was not associated exclusively with the same distillation fraction of each oil; for example, in one the inhibitory effect was found in the low molecular weight fraction and in another it was associated with the highest molecular weight distillation fraction (Cracker, Cronshaw, and Holmes, 1975). The steroidogenic mechanisms of the adrenocortical tissue may also be sensitive to the presence of pollutants in the diet. A derivative of o,p’ DDT( 1 , 1,l -trichloro-2,2bis [ chlorophenyl] ethane) is o,p’ DDD (l,l-dichloro-2,2-bis[chlorophenyl]ethane), and when this compound is fed to mammals the secretion of physiologically active corticosteroids is blocked and necrosis of the zona fasciculata occurs (see Dorfman, 1972). The effect of o,p’DDD on adrenal function in birds has not been tested. But, when metopirone (2-methyl1,2-bis [ 3-pyridyl] -I-propanone), a compound which inhibits the 1 lp hydroxylase activity in the adrenocortical tissue, is given to the hypertonic saline-loaded duck, the secretion of nasal gland fluid ceases (Fig. 8). Since nasal gland secretion is restored following the administration of corticosterone, it is presumed that the inhibition of endogenous corticosterone synthesis by metopirone was responsible for the cessation of nasal gland function
Time
8. The effect of Metopirone with hypertonic saline. During the corticosterone were administered. topirone, nasal gland secretion was FIG.
BIRDS
255
(Fig. 8). It is possible, therefore, that the ingestion of o,p’DDD by marine birds might also block corticosteroid biosynthesis and as a result impair normal nasal gland function in the same way. Some species of ducks, gulls, grebes, and shorebirds spend portions of their life cycle on the Great Plains of North America. These birds, which are known to drink the highly alkaline and hypertonic water occurring in many prairie sloughs and lakes, have been shown to have functional nasal glands. For many years, periodic outbreaks of a disease causing high mortality among these species have been recorded. Early workers attributed the deaths to “alkaline poisoning” but later the disease was recognized as avian botulism (Wetmore, 1915; Gunnison and Coleman, 1932; Kalmbach and Gunderson, 1934). Birds may die of “botulism” either from a massive dose of toxin ingested while eating insect larval cases or from ingesting hypertonic drinking water along with what would be a sublethal dose of toxin in birds drinking fresh water. From these field and experimental observations Coach (1964) assessed correctly the link between “alkaline poisoning,” nasal gland function, and the inhibitory effects of the neurotoxin produced by Clostridium botulinurn. Thus, birds fed either hypertonic saline or “pot-
(min)
and corticosterone on the pattern of nasal gland secretion by ducks loaded indicated intervals, intravenous infusions of 10% NaCI, Metopirone, and When corticosterone was given to birds inhibited previously with Merestored (adapted from Cheeseman. Cheeseman, and Phillips, unpublished).
256
W. N. HOLMES
REFERENCES
N.CI
NOCI
9. The LD,, (expressed in mouse lethal dose units) of orally administered Clostridium botulinurn Type C toxin for Mallard and Pintail ducks given in combination with oral loads of either freshwater or hypertonic NaCl solutions (adapted from Coach, 1964). FIG.
hole” drinking water succumbed to much lower doses of neurotoxin than birds maintained on fresh water (Fig. 9). Furthermore, as the dose of administered neurotoxin was increased, the duration and rate of nasal gland secretion diminished and the volume of cloaca1 fluid discharged increased (cf. Coach, 1964 and Fig. 1). Since the neurotoxin produced by Clostridium botulinurn Type C inhibits the release of acetylcholine (Stover, Fingerman, and Forester, 1953), it was concluded that, in the intoxicated birds fed hypertonic saline, the visceral motor impulses to the nasal glands were blocked and therefore the nasal glands could not function (Coach, 1964). The fact that fresh water given to a saltwater-adapted bird in the early symptomatic stages of botulism is equally as effective as antitoxin lends credence to this conjecture (Coach, 1964). These examples must represent only a few of the instances where environmental contaminants interfere with physiological control mechanisms. In view of the need to understand fully the effects of environmental pollutants, a fundamental knowledge of their interactions with the physiological control mechanisms in affected organisms is imperative. ACKNOWLEDGMENT I acknowledge gratefully the preparation Ilene Hames of Figs. 1 and 2.
by Mrs.
Ash, R. W., Pearce, J. W., and Silver, A. (1969). An investigation of the nerve supply to the salt gland of the duck, Quart. .I. Exp. Physiol. 54, 28 l-295. Ballantyne, B., and Wood, W. G. (1968). ATP-ase and Na+ transport: histochemical and biochemical observations on the avian salt gland. J. Physiol. (London) 196, 125P. Bellamy, D., and Phillips, J. G. (1966). Effect of the administration of sodium chloride solutions on the concentration of radioactivity in the nasal glands of ducks (Anas platyrhynchos) injected with 3H-corticosterone. J. Endocrinol. 36, 97-98. Bonting, S. L., Caravaggio, L. L., Canady, M. R., and Hawkins, N. M. (1964). Studies on sodiumpotassium-activatedadenosinetriphosphatase.XI. The salt gland of the herring gull. Arch. Biochem. Biophys. 106,49-56. Borut, A., and Schmidt-Nielsen, K. (1963). Respiration of avian salt-secreting glands in tissue slice experiments. Amer. J. Physiol. 204, 573-581. Bradley, E. L., and Holmes, W. N. (1972). The role of the nasal glands in the survival of ducks (Anas platyrhynchos) exposed to hypertonic saline drinking water. Con. J. Zoo/. 50, 61 l-617. Bradley, E. L., Holmes, W. N., and Wright, A. (197 1). The effects of neurohypophysectomy on the pattern of renal excretion in the duck Anas platyrhynchos. J. Endocrinol. 51, 57-65. Chance, B., Lee, C. P., Oshino, R., and Van Rossum, G. D. V. (1964). Properties of mitochondria isolated from herring gull salt gland. Amer. J. Physiol. 206, 461-468. Code, C. F., Bass, P., McClary, G. B., Jr., Newnum, R. L., and Orvis, A. L. (1960). Absorption of water, sodium and potassium in small intestine of dogs. Amer. J. Physiol. 199, 281-288. Coach, F. G. (1964). A preliminary study of the survival value of a functional salt gland in prairie anatidae. Auk 81, 380-393. Cracker, A. D., and Holmes, W. N. (197 1). Intestinal absorption in ducklings (Anus platyrhynchos) maintained on freshwater and hypertonic saline. Comp. Biochcm. Physiol. 4OA, 203-211. Cracker, A. D., Cronshaw, J., and Holmes, W. N. (1974). The effect of a crude oil on intestinal absorption in ducklings (Anus platyrhynchos). Environ. Pollution 7, 165- 178. Cracker, A. D., Cronshaw, J., and Holmes, W. N. ( 1975). The effect of several crude oils and some distillation fractions on intestinal absorption in ducklings (Anas platyrhynchos). Environmental Physiology (Copenhagen). In press. Curran, P. F. (1960). Na, Cl and water transport by rat ileum in vitro. J. Gen. Physiol. 43, 1137-l 148. Curran, P. F., and Solomon, A. K. (1957). Ion and
OSMOREGULATION
water fluxes in the ileum of rats. J. Gen.
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Dorfman, R. 1. (1972). Biochemistry of the adrenocortical hormones. In “The Adrenocortical Hormones, Their Origin, Chemistry, Physiology, and Pharmacology; Handbuch der Experimentellen Pharmakologie,” (H. W. Deane, ed.), Vol. 14, part 1, Chapter 3, pp. 41 l-5 13. Springer-Verlag, Berlin. Ellis, R. A., Goertemiller, C. C., DeLellis, R. A., and Kablotsky, Y. H. (1963). The effect of a saltwater regimen on the salt glands of domestic ducklings. Develop. Biol. 8, 286-308. Ensor, D. M., Thomas, D. H., and Phillips, J. G. (1970). The possible role of the thyroid in extrarenal secretion following a hypertonic saline load in the duck (Anus platyrhynchos). J. Endocrinol.
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FPnge, R., Krog, J., and Reite, 0. (1963). Blood flow in the avian salt gland studied by polarographic oxygen electrodes. Actu Physiol. Stand. 58, 40-47. FPnge, R., Schmidt-Nielsen, K., and Robinson, M. (1958). Control of secretion from the avian salt gland. Amer. J. Physiol. 195, 321-326. Fawcett, D. W. (1962). Physiologically significant specializations of the cell surface. Circulation 26, 1105-I 132. Fletcher, G. L., Stainer, I. M., and Holmes, W. N. (1967), Sequential changes in the adenosinetriphosphatase activity and the electrolyte excretory capacity of the nasal glands of the duck (Anus plutyrhynchos) during the period of adaptation to hypertonic saline. J. Exp. Biol. 47, 375-392. Gunnison, J. B., and Coleman, G. E. (1932). Clostridium botulinurn, type C, associated with western duck disease. J. Infect. Dis. 51, 542-551. Hanwell, A., Linzell, J. L., and Peaker, M. (1971). Cardiovascular responses to salt-loading in conscious domestic geese. J. Physiol. (London) 213, 389-398. Heinroth, O., and Heinroth, M. (1927). “Die Vogel Mitteleuropas,” Bd. III, p. 223. H. Vermuhler, Berlin-Lichterfelds. Hindle, W., and Code, C. F. (1962). Some differences between duodenal and ileal sorption. Amer. J. Physiol. 203, 2 15-220. Hokin, L. E., and Hokin, M. R. (1959). Evidence for phosphatidic acid as the sodium carrier. Nature (London) 184, 1068. Hokin, L. E., and Hokin, M. R. (1960). Studies on the carrier function of phosphatidic acid in
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BIRDS
sodium transport. 1. The turnover of phosphatidic acid and phosphoinositide in the avian salt gland on stimulation of secretion. J. Cen. Physiol. 44, 61-85. Hokin, M. R. (1963). Studies on a Na++K+-dependent, ouabain-sensitive adenosine triphosphatase in the avian salt gland. Biochim. Biophys. Acta 77, 108-120. Holmes, W. N., and Adams, B. M. (1963). Effects of adrenocortical and neurohypophysial hormones on the renal excretory pattern of the waterloaded duck (Anas platyrhynchos). Endocrinology 73, 5- 10. Holmes, W. N., Fletcher, G. L., and Stewart, D. J. (1968). The patterns of renal electrolyte excretion in the duck (Anus platyrhynchos) maintained on freshwater and on hypertonic saline. J. Exp. Biol.
Ernst, S. A., Goertemiller, C. C., and Ellis, R. A. (1967). The effect of salt regimens on the development of (Na+ + K+)-dependent ATP-ase activiity during growth of salt glands of ducklings. Biochim.
IN
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Holmes, W. N., Lockwood, L. N., and Bradley, E. L. (1972). Adenohypophysial control of extrarenal excretion in the duck (Anus platyrhynchos). Gen. Comp.
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Holmes, W. N., Phillips, J. G., and Butler. D. G. (1961). The effect of adrenocortical steroids on the renal and extra-renal responses of the domestic duck (Anus platyrhynchos) after hypertonic saline loading. Endocrinology 69, 483495. Holmes, W. N., and Stewart, D. J. (1968). Changes in the nucleic acid and protein composition of the nasal glands from the duck (Anas plutyrhynchos) during the period of adaptation to hypertonic saline. J. Exp. Biol. 48, 509-520. Kalmbach, E. R., and Gunderson, M. F. (1934). Western duck sickness: a form of botulism. U. S. Dept. Agr. Tech. Bull. 411, 82 pp. Peaker, M., Peaker, S. J., Phillips, J. G., and Wright, A. (197 1). The effects of corticotrophin, glucose and potassium chloride on secretion by the nasal salt gland of the duck (Anus plutyrhynchos). J. Endocrinol.
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Phillips, J. G., Holmes, W. N., and Butler, D. G. (I 961). The effect of total and subtotal adrenalectomy on the renal and extra-renal response of the domestic duck (Anus plutyrhynchos). Endocrinology
69, 958-969.
Van Rossum, G. D. V. (1966). Movements of Na+ and K+ in slices of herring-gull salt gland. Biochim.
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Schildmacher, H. (1932). Uber des Einfluss des Salzwassers auf die Entwicklung der Nasendrtisen. J. Ornithol.
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Schmidt-Nielsen, K. (1960). The salt secreting gland of marine birds. Circulation 21, 955-967. Schmidt-Nielsen, K., Jorgensen, C. B., and Osaki, H. (1958). Extrarenal salt excretion in birds. Amer. J. Physiol. 193, 101-107. Scothorne, R. J. (I 959). On the response of the duck
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and the pigeon to intravenous hypertonic saline solutions. Quurt. J. Exp. Physiol. 44, 200-206. Stainer, I. M., Ensor, D. M., Phillips, J. G., and Holmes, W. N. (1970). Changes in glycolytic enzyme activity in the duck (Anus plotyrhynchos) nasal gland during the period of adaptation to salt water. Comp. Biochem. Physiol. 37, 257-263. Stover, J. H., Fingerman, M., and Forester, R. H. (1953). Botulinum toxin and the motor end plate. Proc. Sot. Exp. Biol. Med. 84, 146- 147.
HOLMES
Wetmore, A. (19 15). The duck sickness in Utah. U.S. Dept. Agr. Tech. Bull. 672, 26 pp. Wright, A., Phillips, J. G., and Huang, D. P. (I 966). The effect of adenohypophysectomy on the extrarenal and renal excretion of the saline-loaded duck (Anus platyrhynchos). J. Endocrinol. 36, 249-256.
AND
COMPARATIVE
Hormones
ENDOCRINOLOGY
25,
249-258 (1975)
and Osmoregulation
in Marine
Birds1,2
W. N. HOLMES Department of Biological Sciences, University of California, Santa Barbara, California 93106 Accepted October 15, 1974 The neural and hormonal mechanisms responsible for the control of electrolyte excretion by the nasal glands of marine birds are outlined. At least three stages in the sequence of events leading to excretion, and therefore successful adaption to the marine environment, are sensitive to the presence of environmental pollutants and pathogens. The initiation and continuation of nasal gland function depends on the development of increased rates of Na+ and water transfer across the small intestinal mucosa. This adaptive response is sensitive to the presence of crude oil and crude oil distillation fractions and ingestion of these substances may prevent the development of increased rates of intestinal transfer. Degradation products of DDT may also inhibit the normal pattern of adrenal steroid biosynthesis and thus lead to impaired nasal gland function. Ingestion of the neurotoxin produced by Clostridium botulinum inhibits the release of acetylcholine and therefore blocks the essential visceral motor impulses to the nasal gland function. Thus, when intoxicated birds are fed either hypertonic saline or “pothole” drinking water derived from many prairie sloughs and lakes, they show higher rates of mortality than do similarly intoxicated birds given fresh drinking water.
In the freshwater-maintained duck, hyperosmotic urine is produced rarely, even under conditions of extreme antidiuresis (Holmes and Adams, 1963; Holmes, Fletcher, and Stewart, 1968; Bradley, Holmes, and Wright, 1971). Upon exposure to a diet containing hypertonic saline drinking water, however, the pattern of renal excretion changes and a urine which is slightly hyperosmotic with respect to plasma is produced (Holmes et a/., 1968). The mean osmotic pressure of this urine is approximately 0.4 Osm/liter, but the available osmotic space is such that the limiting isorrheic concentration of Na+ is always less than that necessary 1 This work was supported by research grants from the U.S. National Science Foundation (Grant No. GB 20806), Committee on Research, University of California and the American Petroleum Institute, Washington, DC. * A report based on this paper was given at the Seventh Symposium on Comparative Endocrinology, Tsavo National Park, Kenya in July 1974.
to excrete all of the ingested Na+ via the kidneys (Holmes et al., 1968). Thus, the osmotic imbalance which may occur in a hypothetical bird attempting to excrete via the kidneys all of the osmotic activity in 1 liter of ingested seawater is depicted in Fig. 1. Clearly, a supplementary or extrarenal excretory mechanism is necessary to ensure homeostasis in a marine bird or a freshwater bird adapting to a diet where the drinking water is hyperosmotic. The extrarenal excretory organs in birds are developed from paired nasal glands situated in the orbit. In terrestrial and freshwater species, these glands may be nonfunctional, but, in coastal and pelagic birds, aquatic birds living in regions where lake water is alkaline and hyperosmotic, and in some species of terrestrial birds living in arid environments, the glands are functional excretory organs and their degree of development is commensurate with the osmotic load the species must excrete extrarenally. Although early investigators ob249
Copyright @ 1975 by Academic Press, Inc. AU rights of repmduction in my form reserved.
250
W.
Total Net
excretion: loss:
1.5 liter
1.0
Orm
N.
in 2 5 liter
welter
1.0
Orm
FIG. 1. A representation of the osmotic imbalance which would occur in a marine bird attempting to excrete the electrolyte contained in ingested seawater via the renal pathway alone.
served that the size of the nasal gland declined when marine birds were fed fresh water (Heinroth and Heinroth, 1927; Schildmacher, 1932), their physiological significance was not realized until 1958. At that time Schmidt-Neilsen and his coworkers described the excretory function of the nasal glands in the cormorant (Phafacrocorax auritus), and later their observations were confirmed in other species of marine birds including the duck (Flnge, Schmidt-Neilsen, and Robinson, 1958; Schmidt-Neilsen, Jorgensen, and Osaki, 1958; Scothorne, 1959; Schmidt-Neilsen, 1960). When functioning, the glands secrete a hyperosmotic fluid containing Na+, K+, and Cl- at concentrations higher than those found in seawater, and their ability to excrete a large fraction of the electrolytes ingested complements the limited, although essential, excretory capacity of the kidneys. Thus, the combined activities of the renal and extrarenal pathways will not only enable a bird to excrete all the electrolytes in 1 liter of ingested seawater, but will also yield sufficient free water to balance the respiratory and fecal water losses (Fig. 2). The essential role of the extrarenal pathway in birds fed hyperosmotic drinking water is emphasized when the
HOLMES
nasal glands are removed surgically (Ballantyne and Wood, 1968; Bradley and Holmes, 1972). Such birds seldom survive more than 4 days, and during the first 3 days after exposure to hypertonic drinking water they become severely dehydrated, lose body weight, and show a continuous increase in the concentration of total osmotically active material in plasma. Since the glandless birds can only osmoregulate via the kidneys, the volume of urine necessary to excrete the ingested electrolytes exceeds the volume of water drunk. Therefore, the birds become progressively dehydrated as outlined previously in Fig. 1. Even though functional nasal glands may be present in a species, they will normally remain inactive as long as adequate quantities of fresh water are available. Soon after hypertonic drinking water is ingested for the first time, however, the glands begin to secrete fluid and prolonged exposure to this diet causes them to enlarge, differentiate structurally, and become more efficient as excretory organs. Changes in the protein, DNA, and RNA content of these developing nasal glands indicate that both hypertrophy and hyperplasia of the tubular secretory cells contribute to their growth (Ellis, Goertemiller, Total Net
excretion: win:
0
1.0
Orm
in 0.85
liter
15 liter water
litw
containing
:: . .
. LL
Y N.rol
Urine 0.25
liter
containing
1.0 Orm
0 1 Own
0.6
her
gland coMc2ininQ
flwd
0.9 Own
2. A representation of the osmotic balance which is achieved when a marine bird utilizes both the renal and the extrarenal pathways to excrete the electrolytes in ingested seawater. FIG.
OSMOREGULATION
DeLellis, and Kablotsky, 1963; Holmes and Stewart, 1968). Early in the adaptive process, the secretory cells of the developing nasal gland also show increases in the activities of some mitochondrial and cytoplasmic enzyme systems, and increases in the activity of an Na+-K+-dependent adenosine triphosphatase (ATPase) system in the membranes is correlated closely with the ability of the glands to secrete Na+, K+, and Cl- (Ellis et al., 1963: Hokin, 1963; Bonting, Caravaggio, Canady, and Hawkins, 1964; Chance, Lee, Oshino, and Van Rossum, 1964; Ernst, Goertemiller, and Ellis, 1967; Fletcher, Stainer, and Holmes, 1967; Ballantyne and Wood, 1968, 1970; Stainer, Ensor, Phillips, and Holmes, 1970). Indeed, the gland seems to be functionally dependent upon the activity of this ATPase system for, when G-strophanthin is injected into the nasal gland of the Herring gull, the positive potential which exists between the excretory fluid and the blood is abolished and the secretion of Na+ ceases (Van Rossum, 1966). When fully adapted birds are returned to a fresh water diet, the nasal glands once more assume the characteristics of those in birds maintained continuously on fresh water and, if these birds are given hypertonic drinking water for a second time, high levels of enzyme activity in the tissue and high rates of electrolyte excretion by the gland are reestablished rapidly (Fletcher et al., 1967; Holmes and Stewart, 1968). Although osmotic loads administered parenterally will elicit a secretion of nasal gland fluid, stimulation occurs normally through the reabsorption of hypertonic fluid from the gastrointestinal tract. The small intestine is the principal site of this reabsorption, and any decrease in its absorptive properties will affect adversely the initiation of nasal gland function and the ultimate adaptation of the organism to a marine environment. For example, the intestinal uptake mechanisms of the duck
IN MARINE
251
BIRDS
become impaired following thyroidectomy and, when a single oral load of hypertonic saline is given to these birds, the onset of nasal gland secretion is delayed and the secretory response of the glands is diminished (Ensor, Thomas, and Phillips, 1970). Further, chronic exposure to a hypertonic saline diet causes the mucosal transfer rates of Na+ and water to increase (Fig. 3). These increases occur first in the anterior segments of the small intestine but later the more posterior segments show similar increases and after 2 days the mucosal transfer rates throughout the whole of the small intestine are 60-100% higher than those found in the corresponding segments from ducklings maintained continuously on fresh water (Fig. 3). These characteristic increases in mucosal transfer rates, however, do not occur if the ducklings are treated with spironolactone before transfer to the hypertonic drinking water and the nasal glands in these birds do not seem- to become fully functional (Fig. 4; Cracker and Holmes, 1971). Therefore, not only are normal absorptive properties in the intestinal mucosa dependent on the action of the thyroid, but also the development of the adaptive response Frerhwoter --*
0
I
2
Seawater
3
4
5
Freshwater
6
7
8
9
10
.
I1
12
T,me (doyrl
FIG. 3. The percentage increase in water transfer across the small intestinal mucosa of ducklings during the period of adaptation to hypertonic saline and freshwater regimens. The rate of mucosal transfer is uniform along the length of the small intestine of freshwater-maintained birds, but during adaptation of the bird to hypertonic saline the increment in mucosal transfer is greater in the anterior than in the posterior segments of the small intestine (from Cracker and Holmes, 1971).
252
W.
N.
4. The effect of spironolactone on the transfer of water across the small intestinal mucosa of ducklings maintained for 24 hr on hypertonic saline equivalent to 60% seawater. The values represent mean transfer rates for the whole of the small intestine (from Cracker and Holmes, 1971). FIG.
in this tissue may depend on the direct action of an adrenocortical steroid. Since seawater-adapted ducklings ingest each day the same volume of water as freshwater-maintained birds, the adaptive significance of an increased mucosal transfer rate is not immediately apparent. The following hypothesis, based mainly on mammalian studies, is an attempt to explain this paradox in terms of the sequence of events occurring in the gastrointestinal tract following the ingestion of drinking
HOLMES
water (Cm-ran and Solomon, 1957; Code, Bass, McClary, Newman, and Davis, 1960; Curran, 1960; Hindle and Code, 1962). During the passage of ingested fresh water through the proventriculus and the duodenum, gastric and pancreatic secretions will be added and the electrolyte concentration of the fluid leaving the duodenum will be increased so that its osmotic pressure will approximate that of the surrounding extracellular fluid. The active uptake of Na+ from the intestinal fluid by the epithelial cells of the mucosa will cause water to flow passively from the lumen to the extracellular compartment (Cur-ran and Solomon, 1957; Cur-ran, 1960). Clearly, the activity of the Na+ uptake mechanism will determine the volume of water that can diffuse out of the gut lumen and into the tissues. Thus, under freshwater conditions, a volume approximately equal to that ingested plus the combined volumes of the gastric and pancreatic juices must be absorbed from the intestine to yield to the tissues a net volume equal to that ingested (Fig. 5). When the bird drinks seawater, however, the ingested fluid will be diluted by the passive movement of water from the tissues into the lumen of the gastrointestinal tract (Code et al., 1960; Hindle
Freshwater-adapted Sscrefionr ., ._ ,_ :I:::
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::::::::::::::::::::::::::: .~.._~.L...,... :::::.
~ ..~_~.~_~_~.~.~_~.~.-.......... .. .. .. .. . ... .. . .. .. .. ,...,... .::... ,....._.....,.,...................
Seawoter-adopted
H Hypsr-xmolic E3 Ire-omc.tic q Hype-ormotic
1 with rsrpac~ lo sx~rocellulor 1
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# Active bmrporl 0 Porlive 0
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5. A schematic representation of the uptake of water from the gastrointestinal tract of a bird drinking fresh water (upper) and a bird drinking a similar volume of seawater (lower). FIG.
OSMOREGULATION
and Code, 1962). This will continue until the fluid has been diluted to the same concentration as the fluid in the surrounding tissues and the final volume entering the small intestine will be much greater than the volume ingested (Fig. 5). Thus, in order to gain a volume of water equal to that ingested, a bird drinking seawater must transfer out of its intestine and into its tissues a larger volume of fluid than a bird drinking fresh water. In other words, the rate of Na+ and water absorption by the intestinal mucosa must increase if the bird is to adapt successfully to the marine environment. The combined effect of water moving into the gut to dilute the hypertonic drinking water, and Na+ being reabsorbed into the extracellular space from the contents of the small intestine, is to increase the plasma osmolality. This change in plasma osmolality is believed to stimulate an osmoreceptor in the central nervous system. From the central receptor impulses are presumed to pass along two motor pathways. The first is a visceral motor pathway associated with the facial branch of the VIIth cranial nerve. Direct electrical stimulation of this nerve or the parenteral administration of cholinergic and parasympathomimetic drugs stimulate the secretion of nasal gland fluid in the unloaded bird. On the other hand, cholinergic blocking agents, sympathomimetic drugs, general anesthesia, denervation of the gland, and decerebration inhibit nasal gland function in birds that have been loaded previously with hypertonic saline (Fange et al., 1958; Schmidt-Nielsen, 1960; Ash, Pearce, and Silver, 1969; Hanwell, Linzell, and Peaker, 1971). The effects of parasympathetic stimulation appear to be partly vasomotor, and some investigators have postulated that an increase in blood flow to the gland would make more Na+ available to the Na+-K+dependent ATPase system and thus enhance the active transport of Na+ (FPnge,
IN
MARINE
BIRDS
253
Krog, and Reite, 1963; Bonting et al., 1964; Hanwell et al., 1971). Nerve endings, however, terminate on the principal cells within the nasal glands (Fawcett, 1962), and cholinergic agents increase the oxygen consumption, the activity of the phosphatidic acid cycle, and the Na+transporting abilities in the nasal gland tissue (Hokin and Hokin, 1959, 1960; Borut and Schmidt-Nielsen, 1963; Van Rossum, 1966). Although a cholinergic mechanism is essential for nasal gland function, this normal secretory response of the gland in the duck also depends on a second motor pathway associated with the adenohypophysialadrenocortical axis (Wright, Phillips, and Huang, 1966; Holmes, Lockwood, and Bradley, 1972). Removal of the adenohypophysis reduces the secretion of nasal gland fluid, and treatment of adenohypophysectomized ducks with ACTH restores the extrarenal excretory response to normal (Holmes, Lockwood and Bradley, 1972). Unilateral adrenalectomy in the duck also attenuates the extrarenal response to hypertonic saline, and the response is abolished almost completely when the bird is totally adrenalectomized. Corticosteroid replacement therapy in the totally adrenalectomized bird restores nasal gland secretion to normal, and nasal gland secretion in the intact duck is augmented significantly when either cortisol, cortexone, corticosterone, or ACTH is administered along with the hypertonic saline load (Holmes, Phillips, and Butler, 1961; Phillips, Holmes, and Butler, 1961; Bellamy and Phillips, 1966; Peaker, Peaker, Phillips, and Wright, 1971). The events leading to the secretion of nasal gland fluid in the marine bird are summarized in Fig. 6. At least three physiological events involved in the control mechanisms leading to normal nasal gland function are sensitive to some pathogens and pollutants present in the environment. These are (1)
254
W.
N.
HOLMES
.o Corticorterone
Ormottc laod
FIG. 6. A summary in marine birds.
Nor01 gland 7 No+ & K+excrebn
K+excrehon
of the possible
pathways
involved
the intestinal uptake of Na+ and water, (2) the biosynthesis of corticosteroids in the adrenal, and (3) the cholinergic control of nasal gland secretion (Fig. 6). The magnitude of the increment of mucosal transfer necessary for successful adaptation to the marine environment must be proportional to the amount of Na+ ingested in drinking water. Any interference with the development or maintenance of this adaptive change will limit the ability of the organism to survive. We have examined recently the effects of small volumes of ingested crude oil on the intestinal transfer rates of freshwater- and seawatermaintained ducklings (Cracker, Cronshaw,
in the initiation
and regulation
of nasal gland
secretion
and Holmes, 1974). Although the administration of crude oil had no effect on the basal rate of mucosal transfer in ducklings maintained on freshwater, the adaptive response in birds given seawater was inhibited (Fig. 7). This effect was apparent 24 hr after the oil was administered, and experimental evidence showed that the effect of a single dose persisted for at least 4 days (Fig. 7). Furthermore, the increment in mucosal transfer rate developed during a previous 3-day exposure to hypertonic drinking water was abolished 24 hr after a single dose of crude oil had been given (Fig. 7). The degree of inhibition varied with crude oils from different locations and
25 r
Experimenl
I
Experiment
2
Experiment
3
FIG. 7. The effect of a single oral dose (0.2 ml) of Santa Barbara crude oil on the mean rates of mucosal transfer in the small intestine of ducklings maintained on either fresh water or seawater. In Expts 1 and 2 the transfer rates were measured 24 hr and 4 days, respectively, after the oil was given, and in Expt 3 the birds were allowed to adapt to seawater for 3 days, the oil was given at the beginning of the fourth day of adaptation, and the mucosal transfer rates were determined 24 hr later (from Cracker, Cronshaw, and Holmes, 1974).
OSMOREGULATION
IN MARINE
was not associated exclusively with the same distillation fraction of each oil; for example, in one the inhibitory effect was found in the low molecular weight fraction and in another it was associated with the highest molecular weight distillation fraction (Cracker, Cronshaw, and Holmes, 1975). The steroidogenic mechanisms of the adrenocortical tissue may also be sensitive to the presence of pollutants in the diet. A derivative of o,p’ DDT( 1 , 1,l -trichloro-2,2bis [ chlorophenyl] ethane) is o,p’ DDD (l,l-dichloro-2,2-bis[chlorophenyl]ethane), and when this compound is fed to mammals the secretion of physiologically active corticosteroids is blocked and necrosis of the zona fasciculata occurs (see Dorfman, 1972). The effect of o,p’DDD on adrenal function in birds has not been tested. But, when metopirone (2-methyl1,2-bis [ 3-pyridyl] -I-propanone), a compound which inhibits the 1 lp hydroxylase activity in the adrenocortical tissue, is given to the hypertonic saline-loaded duck, the secretion of nasal gland fluid ceases (Fig. 8). Since nasal gland secretion is restored following the administration of corticosterone, it is presumed that the inhibition of endogenous corticosterone synthesis by metopirone was responsible for the cessation of nasal gland function
Time
8. The effect of Metopirone with hypertonic saline. During the corticosterone were administered. topirone, nasal gland secretion was FIG.
BIRDS
255
(Fig. 8). It is possible, therefore, that the ingestion of o,p’DDD by marine birds might also block corticosteroid biosynthesis and as a result impair normal nasal gland function in the same way. Some species of ducks, gulls, grebes, and shorebirds spend portions of their life cycle on the Great Plains of North America. These birds, which are known to drink the highly alkaline and hypertonic water occurring in many prairie sloughs and lakes, have been shown to have functional nasal glands. For many years, periodic outbreaks of a disease causing high mortality among these species have been recorded. Early workers attributed the deaths to “alkaline poisoning” but later the disease was recognized as avian botulism (Wetmore, 1915; Gunnison and Coleman, 1932; Kalmbach and Gunderson, 1934). Birds may die of “botulism” either from a massive dose of toxin ingested while eating insect larval cases or from ingesting hypertonic drinking water along with what would be a sublethal dose of toxin in birds drinking fresh water. From these field and experimental observations Coach (1964) assessed correctly the link between “alkaline poisoning,” nasal gland function, and the inhibitory effects of the neurotoxin produced by Clostridium botulinurn. Thus, birds fed either hypertonic saline or “pot-
(min)
and corticosterone on the pattern of nasal gland secretion by ducks loaded indicated intervals, intravenous infusions of 10% NaCI, Metopirone, and When corticosterone was given to birds inhibited previously with Merestored (adapted from Cheeseman. Cheeseman, and Phillips, unpublished).
256
W. N. HOLMES
REFERENCES
N.CI
NOCI
9. The LD,, (expressed in mouse lethal dose units) of orally administered Clostridium botulinurn Type C toxin for Mallard and Pintail ducks given in combination with oral loads of either freshwater or hypertonic NaCl solutions (adapted from Coach, 1964). FIG.
hole” drinking water succumbed to much lower doses of neurotoxin than birds maintained on fresh water (Fig. 9). Furthermore, as the dose of administered neurotoxin was increased, the duration and rate of nasal gland secretion diminished and the volume of cloaca1 fluid discharged increased (cf. Coach, 1964 and Fig. 1). Since the neurotoxin produced by Clostridium botulinurn Type C inhibits the release of acetylcholine (Stover, Fingerman, and Forester, 1953), it was concluded that, in the intoxicated birds fed hypertonic saline, the visceral motor impulses to the nasal glands were blocked and therefore the nasal glands could not function (Coach, 1964). The fact that fresh water given to a saltwater-adapted bird in the early symptomatic stages of botulism is equally as effective as antitoxin lends credence to this conjecture (Coach, 1964). These examples must represent only a few of the instances where environmental contaminants interfere with physiological control mechanisms. In view of the need to understand fully the effects of environmental pollutants, a fundamental knowledge of their interactions with the physiological control mechanisms in affected organisms is imperative. ACKNOWLEDGMENT I acknowledge gratefully the preparation Ilene Hames of Figs. 1 and 2.
by Mrs.
Ash, R. W., Pearce, J. W., and Silver, A. (1969). An investigation of the nerve supply to the salt gland of the duck, Quart. .I. Exp. Physiol. 54, 28 l-295. Ballantyne, B., and Wood, W. G. (1968). ATP-ase and Na+ transport: histochemical and biochemical observations on the avian salt gland. J. Physiol. (London) 196, 125P. Bellamy, D., and Phillips, J. G. (1966). Effect of the administration of sodium chloride solutions on the concentration of radioactivity in the nasal glands of ducks (Anas platyrhynchos) injected with 3H-corticosterone. J. Endocrinol. 36, 97-98. Bonting, S. L., Caravaggio, L. L., Canady, M. R., and Hawkins, N. M. (1964). Studies on sodiumpotassium-activatedadenosinetriphosphatase.XI. The salt gland of the herring gull. Arch. Biochem. Biophys. 106,49-56. Borut, A., and Schmidt-Nielsen, K. (1963). Respiration of avian salt-secreting glands in tissue slice experiments. Amer. J. Physiol. 204, 573-581. Bradley, E. L., and Holmes, W. N. (1972). The role of the nasal glands in the survival of ducks (Anas platyrhynchos) exposed to hypertonic saline drinking water. Con. J. Zoo/. 50, 61 l-617. Bradley, E. L., Holmes, W. N., and Wright, A. (197 1). The effects of neurohypophysectomy on the pattern of renal excretion in the duck Anas platyrhynchos. J. Endocrinol. 51, 57-65. Chance, B., Lee, C. P., Oshino, R., and Van Rossum, G. D. V. (1964). Properties of mitochondria isolated from herring gull salt gland. Amer. J. Physiol. 206, 461-468. Code, C. F., Bass, P., McClary, G. B., Jr., Newnum, R. L., and Orvis, A. L. (1960). Absorption of water, sodium and potassium in small intestine of dogs. Amer. J. Physiol. 199, 281-288. Coach, F. G. (1964). A preliminary study of the survival value of a functional salt gland in prairie anatidae. Auk 81, 380-393. Cracker, A. D., and Holmes, W. N. (197 1). Intestinal absorption in ducklings (Anus platyrhynchos) maintained on freshwater and hypertonic saline. Comp. Biochcm. Physiol. 4OA, 203-211. Cracker, A. D., Cronshaw, J., and Holmes, W. N. (1974). The effect of a crude oil on intestinal absorption in ducklings (Anus platyrhynchos). Environ. Pollution 7, 165- 178. Cracker, A. D., Cronshaw, J., and Holmes, W. N. ( 1975). The effect of several crude oils and some distillation fractions on intestinal absorption in ducklings (Anas platyrhynchos). Environmental Physiology (Copenhagen). In press. Curran, P. F. (1960). Na, Cl and water transport by rat ileum in vitro. J. Gen. Physiol. 43, 1137-l 148. Curran, P. F., and Solomon, A. K. (1957). Ion and
OSMOREGULATION
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41, 143-168.
Dorfman, R. 1. (1972). Biochemistry of the adrenocortical hormones. In “The Adrenocortical Hormones, Their Origin, Chemistry, Physiology, and Pharmacology; Handbuch der Experimentellen Pharmakologie,” (H. W. Deane, ed.), Vol. 14, part 1, Chapter 3, pp. 41 l-5 13. Springer-Verlag, Berlin. Ellis, R. A., Goertemiller, C. C., DeLellis, R. A., and Kablotsky, Y. H. (1963). The effect of a saltwater regimen on the salt glands of domestic ducklings. Develop. Biol. 8, 286-308. Ensor, D. M., Thomas, D. H., and Phillips, J. G. (1970). The possible role of the thyroid in extrarenal secretion following a hypertonic saline load in the duck (Anus platyrhynchos). J. Endocrinol.
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FPnge, R., Krog, J., and Reite, 0. (1963). Blood flow in the avian salt gland studied by polarographic oxygen electrodes. Actu Physiol. Stand. 58, 40-47. FPnge, R., Schmidt-Nielsen, K., and Robinson, M. (1958). Control of secretion from the avian salt gland. Amer. J. Physiol. 195, 321-326. Fawcett, D. W. (1962). Physiologically significant specializations of the cell surface. Circulation 26, 1105-I 132. Fletcher, G. L., Stainer, I. M., and Holmes, W. N. (1967), Sequential changes in the adenosinetriphosphatase activity and the electrolyte excretory capacity of the nasal glands of the duck (Anus plutyrhynchos) during the period of adaptation to hypertonic saline. J. Exp. Biol. 47, 375-392. Gunnison, J. B., and Coleman, G. E. (1932). Clostridium botulinurn, type C, associated with western duck disease. J. Infect. Dis. 51, 542-551. Hanwell, A., Linzell, J. L., and Peaker, M. (1971). Cardiovascular responses to salt-loading in conscious domestic geese. J. Physiol. (London) 213, 389-398. Heinroth, O., and Heinroth, M. (1927). “Die Vogel Mitteleuropas,” Bd. III, p. 223. H. Vermuhler, Berlin-Lichterfelds. Hindle, W., and Code, C. F. (1962). Some differences between duodenal and ileal sorption. Amer. J. Physiol. 203, 2 15-220. Hokin, L. E., and Hokin, M. R. (1959). Evidence for phosphatidic acid as the sodium carrier. Nature (London) 184, 1068. Hokin, L. E., and Hokin, M. R. (1960). Studies on the carrier function of phosphatidic acid in
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BIRDS
sodium transport. 1. The turnover of phosphatidic acid and phosphoinositide in the avian salt gland on stimulation of secretion. J. Cen. Physiol. 44, 61-85. Hokin, M. R. (1963). Studies on a Na++K+-dependent, ouabain-sensitive adenosine triphosphatase in the avian salt gland. Biochim. Biophys. Acta 77, 108-120. Holmes, W. N., and Adams, B. M. (1963). Effects of adrenocortical and neurohypophysial hormones on the renal excretory pattern of the waterloaded duck (Anas platyrhynchos). Endocrinology 73, 5- 10. Holmes, W. N., Fletcher, G. L., and Stewart, D. J. (1968). The patterns of renal electrolyte excretion in the duck (Anus platyrhynchos) maintained on freshwater and on hypertonic saline. J. Exp. Biol.
Ernst, S. A., Goertemiller, C. C., and Ellis, R. A. (1967). The effect of salt regimens on the development of (Na+ + K+)-dependent ATP-ase activiity during growth of salt glands of ducklings. Biochim.
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Holmes, W. N., Phillips, J. G., and Butler. D. G. (1961). The effect of adrenocortical steroids on the renal and extra-renal responses of the domestic duck (Anus platyrhynchos) after hypertonic saline loading. Endocrinology 69, 483495. Holmes, W. N., and Stewart, D. J. (1968). Changes in the nucleic acid and protein composition of the nasal glands from the duck (Anas plutyrhynchos) during the period of adaptation to hypertonic saline. J. Exp. Biol. 48, 509-520. Kalmbach, E. R., and Gunderson, M. F. (1934). Western duck sickness: a form of botulism. U. S. Dept. Agr. Tech. Bull. 411, 82 pp. Peaker, M., Peaker, S. J., Phillips, J. G., and Wright, A. (197 1). The effects of corticotrophin, glucose and potassium chloride on secretion by the nasal salt gland of the duck (Anus plutyrhynchos). J. Endocrinol.
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Van Rossum, G. D. V. (1966). Movements of Na+ and K+ in slices of herring-gull salt gland. Biochim.
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Schmidt-Nielsen, K. (1960). The salt secreting gland of marine birds. Circulation 21, 955-967. Schmidt-Nielsen, K., Jorgensen, C. B., and Osaki, H. (1958). Extrarenal salt excretion in birds. Amer. J. Physiol. 193, 101-107. Scothorne, R. J. (I 959). On the response of the duck
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