NASAL

SALT SECRETIONIN

FALCONIFORMTOM J. CADE and LEWIS

BIRDS

GREENWALD

Falconers have long known that various raptors, especially accipiters and eagles,
exude a clear fluid from their nares while eating. We were reminded of this fact
while handling a melanistic Gabar Goshawk (1Micronisus g&r),
which we trappedin the Kalahari Desert in August 1964. As the hawk ate his prey, the small dropletsof fluid that collected on our gloves had a strong salty taste. This discovery led us
to look for nasal secretions in 16 species and 10 genera of Accipitridae and in eightspecies and three genera of Falconidae. We have studied behavioral and physiological aspects of nasal secretion in these raptors with reference to Schmidt-Nielsen’s(1964) hypothesis regarding the general necessity for birds to utilize an extrarenalmechanism of salt excretion, as an adjunct to efficient water reabsorption from thecloaca in concentrating uric acid, and also in connection with the overall water
economy of carnivorous birds.
MATERIALSAND

METHODSWe obtained birds and information from various sources. Our initial observations were made on an adult male Gabar Goshawk, an adult female Red-necked
Falcon (F&o chiqueru), and a pair of adult Pigmy Falcons (Polihierax semitorquatus), which we trapped in the Kalahari Gemsbok National Park in the Republicof South Africa and subsequently transported to our laboratory at Syracuse University. In addition, we obtained the following hawks from a bird dealer in New
York: an immature Savannah Hawk (Heterospizias meridionalis) and a juvenile
Yellow-headed Caracara (M&ago chimuchima), both from South America, and an
immature Saker (F&o chewug) and an adult Laggar (Fake jugger) from India.
Heinz Meng kindly permitted us to obtain some samples from a trained Peregrine(F&operegrinus), Goshawk (Accipiter gent&),
and Red-tailed Hawk (Buteo
jamaicensis). We also made spme observations and measurements on a female
American Kestrel (Falco sparverius), an immature Red-tailed Hawk, and an immature Sharp-shinned Hawk (Accipiter stviatus), all from the vicinity of Syracuse,
New York. Walter R. Spofford and Morlan W. Nelson made some observations for
us on their captive Golden Eagles (Aquila chvysaltos), and Archie White and George
Goode, taxidermists of the Transvaal Museum, and 0. P. M. Prozesky, ornithologist
there, noted secretions for us in a number of captive South African eagles and hawks.
We have. also been able to observe secretions at close hand in caged specimens of
the Lappet-faced Vulture (Torgos trecheliotus) , Cape Vulture (Gyps copotheres) ,and White-backed Vulture (Gyps africanus) at the Pretoria Zoo, and recently wehave had a tame Bateleur (Terathopius ecaudatus) under close observation. Thus,
our material has been drawn from four continents and represents a fairly wide
taxonomic sampling of species within the Falconiformes.
When a hawk expelled nasal secretions, the fluid could be collected for analysis
in various ways. The simplest method was to place a sheet of aluminum foil in frontof -the. bird at the level of its feet and wait for it to sneeze or sling the fluid thatcollected in its nares onto the foil. The droplets were immediately collected withsmall, volumetric pipettes ranging from 1 to 25 pl in capacity. With docile birds a
10 or 25 ~1 pipette could be inserted into one of the hawk’s nares to collect thesecretion before it was voided (fig. 1).
THE CONDOR,68:338-350,

1966.

13381

NASALSALT

SECRETION

IN FALCONIFORM

BIRDS

339

Figure 1. Method of taking samples of nasal secretion directly from the nares of a Bateleur.
Note shape of nare and the secretion that has drooled onto beak. In the normal head-up posture,
the secretion drains directly down to the tomium and drips off the hooked tip of the beak.

340

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J. CADE

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GREENWALD

Urine samples were collected on aluminum foil sheets placed beneath the birds.
If the urine had a distinct, clear, and liquid portion, this fluid was collected in apipette in the same way the nasal secretions were taken. More often, whole urine
was sucked into a small capillary tube, one end was flame sealed, and the tube wits
centrifuged. The clear, liquid supernatant was used for ion analysis.
Blood was obtained from a wing vein and drawn into a heparinized capillary
tube. The tube was centrifuged, and the plasma supernatant was blown into a
depression slide and taken up in a volumetric pipette.
After any of the samples had been measured in a volumetric pipette, the contents
were blown out into 2 ml of distilled water. These diluted samples were then analyzed for Na+, K+, and Cat+ on a Coleman flame photometer, and for Cl- on an
Aminco electric chloride titrator. Phosphate determinations were made using themethod of Fiske and Subbarow ( 1925).
Nasal glands were dissected from the Gabar Goshawk, the Sharp-shinned Hawk,
the Red-tailed Hawk, the Savannah Hawk, the American Kestrel, one of the Pigmy
Falcons, the Yellow-headed Caracara, and from a Lappet-faced Vulture collected inSouth West Africa and a Black Kite (J4iZva.s migrans) collected in the western
Transvaal. These glands were fixed in formalin.
RESULTSANDDISCUSSIONThe Gabar Goshawk. Micronisus gabw. This bird, which weighed 175 to 180 g,nearly always exuded a salty tasting secretion from its nares while eating and forsome time after finishing a meal. Most often the fluid, which collected in the orificesof the external nares, was eliminated by vigorous head-shaking and was frequently
associated with ruffling of the plumage, but sometimes this hawk also sneezed thefluid out in fine droplets. We never saw any nasal secretions except during the brief
period of feeding each day, but the encrustations of salt crystals around its nares
led us to believe that the bird must have secreted for some time after the meal was
over. When fed a laboratory mouse, the bird secreted 10 to 15 ~1 of fluid, about halfof which was voided while eating the mouse, the other half within five minutes after
finishing. Fluid could be seen forming in the bird’s nares within nine minutes after
it started eating. When this hawk was fed raw meat from a chicken wing, he usually
did not secrete any nasal fluid at all; on a few occasions somewhat less than 2 ~1
were obtained. An intact sparrow carcass stimulated as much secretion as a mouse.
Adding 0.1 g of NaCl to a mouse produced no marked change in the secretory
pattern of this hawk. Salted chicken was not tried.
We collected 23 nasal samples from this accipiter. The high, low, and meanvalues for the ionic concentrations in these samples are shown in table 1. The lowest
concentrations of Na+ and Cl-, the predominant ions in the secretion, were well
above the blood concentrations. The first secretion voided by the bird was usuallyof much higher concentration than subsequent samples; this occurred because thefirst secretion dissolved and mixed with crystals of salt that had accumulated in the
nares from the previous day. As an example, one initial sample had a Na+ concentration of 2316 mmole/liter and Cl- concentration of 2441 mmole/liter. Crystals ofsalt were visible in the nares before the drop of fluid formed. The next secretion
was less than half the concentration of the first, 1039 mmole/liter for Na+ and 770
mmole/liter for Cl-.
Because of the formation of salt crystals from evaporation in the nares, it is
impossible to make an unequivocal statement about the osmotic concentration ofNASALSALT

SECRETION

IN FALCONIFORM

341

BIRDS

TABLE 1SUMMARY OF IONIC CONCENTRATIONSIN BLOOD, URINE, AND NASAL SECRETION OF FALCONWORM
BIRDS, AS MILLIMOLES PER LITER

Na+

K+

NZWIl

Urine

BlOCd
Species
Ca++ Cl-

Na+

K+

ca++

Cl-

Nat

K+

Ca++ Cl-

-

127

190
73
24

100
48
12

17
6
2

67
48
32

1

9

9

5

5

2316
1023
440
23

128
45
16
18

56 2441
21 983
3 416
6
20

-

-

-

-

130
1

128
1

-

31
1

620
380
2

200
100
2

-

502
339
2

206

76

-

21

380

20

-

226

135
88
40
2

150
123
96
2

32
19
6
2

47
43
39
2

890
433
255

30
16
6

10
3
1

949
455
263

7

5

5

7

100

144

-

138

45
10

-

9

77
18
9-

40
5
9

520
259
176
10

15
9
6
10

-

505
256
185
10

234

268

-

155

920

170

-

851

120

232

-

14

-

-

-

-

340
103
13
12

92
41
9
10

6
4
1
9

237
89
23
12

-

-

-

-

150
94
56
6

300
115
46
5

10
7
2
5

71
34
13
7

Micronisus gabar
High
Mean
Low
Number_--160 ---1

Accipiter gentilis
High
Low
Number
Buteo jamuicensis
Number = 1_---

Heterospizias meridionalis
High
Mean
Low
Number---170
----

8

3123

1

1

1

1

Terathopius ecaudatus
High
Mean
Low
Number----Falco cherrug
Number = 1
Falco peregrinus
Number = 1
Falco sparverius
High
Mean
Low
Number

190
187
184
2

16
14
12
2

-

157
5 152
147
1
2

Polihierax semitorquatus
High
Mean
Low
Number

----

-

-

-

-

630
-

40
-

42
_

397
-

1

1

1

1

the actual secretion without
cannulation of the gland. We feel, however, that theminimum values, about 450 to 500 mmole/liter for both Na+ and Cl-, approximate
closely the true concentrating ability of the nasal gland in this species.
There were never any definite proportions between the concentrations of thevarious ions; cations were always in excess. Since the amount of phosphate in the

342

TOM

J. CADE

AND

LEWIS

GREENWALD

secretion was below our limit of analysis, some other anion, such as sulfate or bicarbonate, must have been present.
The fact that this goshawk responded by secreting when given an intact mouseor bird carcass to eat but not when fed plain chicken muscle can be explained bydifferences in the composition of water and electrolytes in the two kinds of food.
On the average, raw chicken wing meat has more preformed water in it than the
average for various mouse tissues (3.38 mg HzO/mg dry wt of chicken versus 2.83
mg &O/mg dry wt of whole mouse), but the differences in ionic composition areeven more important. The total body store of Na+ is about 60 mmole/kg or roughly
90 mmole/liter of total body water; for K+ the comparable figures are 42 mmole/kg
and 63 mmole/liter; but for muscle the Na+ concentration is only about 10 mmole/liter of water, whereas the K+ concentration averages 160 mmole/liter (from Pitts,
1963). The excretion of Na+ is much less of a problem on a diet of pure muscle,
but the reverse is true for K+.
On the other hand, the nasal secretion begins to form within a few minutes after
food has been swallowed, while the bulk of it is still in the crop and before any
appreciable amounts of ions, water, or other materials could have passed from thegut into the general circulation. The idea of a direct sensory stimulation (fromtactile or chemical receptors in the mouth or via ocular routes) is suggested and isconsistent with Schmidt-Nielsen’s (1960) finding that the nasal gland of the Herring
Gull (Larus urgenta&) is controlled by parasympathetic fibers associated with thefacial nerve. Such innervation indicates control by a higher central nervous organization, into which various sensory inputs could be directed. Our observations indicate that in this species, as in other falconiforms (see below), the nasal secretion isnormally stimulated to flow by sensory inputs originating directly from the gustatory process, as well as by blood-borne chemical stimuli acting on osmoreceptors in
the central nervous system. McFarland (1965) has recently shown that both photic
and auditory stimuli can produce an increase in the rate of flow of the nasal secretion in minimally salt-loaded “sea-gulls.”
In general, the concentrations of Na+ and Cl- in the urine of the Gabar Goshawk
were less than those of its blood, while the urine concentration of K+ (48 mmole/liter)
was much higher than one would expect for plasma (around 5 mmole/liter). It also
appears that phosphate is a major anion in this bird’s urine, as we obtained a valueof 158 mmole/liter. There was no obvious or consistent relationship among thevarious ions, but the blood concentrations of Na+ and Cl- were in the range to be
expected for birds.
The Savannah Hawk. Heterospizias meridiomzlis. This bird submitted to having
a small pipette inserted into its nares, either for the purpose of washing them freeof salt crystals or to withdraw the nasal secretion as it accumulated at the orifice.
This was the closest we could come to a direct cannulation. Also, because this hawk,
which weighed about 1 kg, swallowed laboratory mice whole, it was possible to saltload the bird by putting NaCl into the body cavity of an eviscerated mouse. We alsosalt-loaded the bird by means of a tube directed into its crop, into which we introduced salt solutions.
Like the Gabar Goshawk, the Savannah Hawk eliminated its nasal secretions as
they collected in large drops at the orifices of its nares by slinging its head fromside to side as it ate. We never saw it sneeze out the fluid. Sometimes the drops
drooled down the sides of its beak and dripped off. Fluid was observed in the nares

NASAL SALT SECRETION IN FALCONIFORM BIRDS

343

within 30 seconds after the bird began to eat, but the bird never showed a response
just at the sight of food.
Secretions were collected during and immediately after feeding the hawk somemice. The ionic concentrations in the secretions were less than those from the Gabar
Goshawk but greater than the concentrations in the Savannah Hawk’s blood (table1). In all of these determinations, the secretion was obtained by inserting a 10 ~1
pipette into one of the hawk’s nares in order to minimize the effect.of evaporation.
The concentration of phosphate ion was again below the limit of the technique ofanalysis (0.05 mmole/liter).
The average equivalents of anions and cations balanced each other almost perfectly, but this was usually not the case for any given
sample. The urine samples were similar to those of the Gabar Goshawk in that they
were hypotonic to blood for Na+ and Cl- but hypertonic for K+.
Because of the relatively high rates of secretion, which were estimated at about
100 ~1 per minute during the time of eating, we regard it as unlikely that the samples
represent secretions contaminated by dissolved salt crystals lodged in the nares. In
all cases, the first secretion from the Savannah Hawk was omitted, and only secretions that formed after the feeding of the first mouse were analyzed. Copious
secretion stopped in a few minutes after the last mouse was eaten, but intermittent
secretion may have occurred subsequently, as the bird often had an encrustation ofsalt in its nares the following day.
To see whether or not the nasal secretion could be stimulated by an osmotic
stress, we fed the hawk 0.5 g of NaCl placed in the body cavity of a mouse. The
bird’s nares were previously washed free of salt crystals by flushing with distilledwater. After a drying period the hawk was given the salted mouse. Within 30
seconds after the mouse had been swallowed, a nasal secretion formed in the nares
and was collected for analysis. This sample had the highest ionic concentrations
obtained for this bird, 1010 mmole/liter for Na+ and 1040 for Cl-. Moreover, about
five minutes after eating the mouse, the hawk passed an extremely liquid urine oflarge volume. This was the only hyperosmotic urine sample collected from the bird,
346 mmole/liter for Na+ and 173 for Cl-. After 12 hours of rest without food, thehawk had a heavy encrustation of salt crystals on the cere around both nares. Similar
encrustations occurred after injecting 5 ml of 100 mmole/liter NaCl into the bird’s
crop with a tube, even though in this case the solution was hypotonic to the hawk’s
blood.
The Bateleur. Tmathopius ecaudatus. We were attracted to this species when
we saw a tame, immature individual begin to secrete at the mere sight of food in
the trainer’s hand, again indicating the importance of nonosmotic stimuli in the
production of this secretion among falconiform birds. Moreover, the secretion was
copious and salty tasting. We were subsequently able to observe this bird in detailand to obtain both urine and nasal samples (table 1) . The volume of secretion produced by this bird was quite high by comparison with the other birds we handled:assuming about 20 drops per ml, the fluid secreted during feeding usually amounted
to about 2 or 3 ml. We also saw the Bateleur secreting at other times of the day,especially when lying on the ground sunning and panting. The concentration of ionsin the secretion was, however, rather low, the lowest values being not much above
expected concentrations of Na+ and Cl- in blood.
The nares of the Bateleur are dorso-ventrally elongated and taper to a point atthe ventral end (see fig. 1). This shape appears to be a structural arrangement that

TOM

344

J. CADE

AND

LEWIS

GREENWALDTABLE 2
OCCURRENCE OF NASAL SECRETIONIN FALCONIFORM BIRDS
Secretion

present

Observers

Accipitridae
Torgos tracheliotus
Gyps coprotheres
Gyps ajricanus
Aquila chrysal;tos
Aquila verreauxi
Aquik rapax
Aquila wahlbergi
PolemaEtus bellicosus
Terathopius ecaudatus
Buteo jamaicensis
Buteo rujojuscus
Accipiter gentilis
Accipiter striutus
Yicronisus gabar
A4elilrax musicus
Heterospizias meridionalis

yes
yes

yes
yes
yes
yes
yes
Yes

yes
yes
yes

yes
Yes

yes
yes
yes

Cade
Cade
Cade
Spofford and Nelson
Goode, Cade, and Greenwald
Goode, Cade, and Greenwald
Cade and Greenwald
Goode, Prozesky, and White
Goode, Cade, and Greenwald
Cade, Greenwald, and Meng
Goode, Prozesky, and White
Geenwald and Meng
Cade
Cade and Greenwald
Goode and Prozesky
Cade and Greenwald

Falconidae
Milvago chimachima
Falco cherrug
Falco jugger
Falco biurmicus
Falco peregrinus
Falco chiquera
Falco sparverius
Polihierax semitorquatus

no
yes
no
yes
yes
yes
no
yes

Cade and Greenwald
Cade and Greenwald
Cade and Greenwald
Goode
Greenwald and Meng
Cade
Cade and Greenwald
Cade and Greenwald

permits the secretion to accumulate in the lower part of the nares and to drain out
without obstructing the air passages.
Average values for urine concentrations of Na+ and Cl- in the Bateleur are
hypotonic to expected values for blood, whereas the concentration of K+ is muchhigher. It is interesting, however, that the maximum values for all three ions differ
from the minimum values by a full order of magnitude. The ionic composition of
hawk urine changes markedly through the day, apparently in relation to the time offeeding and to uric acid production; but only after samples for the entire day havebeen analyzed will it be possible to work out the details.
Other species of Accipitridae. For both the American Goshawk (Accipiter gentdis) and the Red-tailed Hawk (Btieo jamaicensis), the urine concentrations of Na+
and Cl-, but not of K+, were lower than the expected values for blood, whereas thenasal secretions of both species were hypertonic for Na+ and Cl-. All the observed
species of Accipitridae showed definite signs of nasal secretion while eating (table2). The aegypine vultures, like the Bateleur, produce an especially copious secretionthat is salty tasting. They also secrete when panting and have dorso-ventrally
elongated nares. These accipitrid species typically eliminate the secretion from theirNASALSALT

SECRETION

IN FALCONIFORM

BIRDS

345

nares by head-shaking. The Gabar Goshawk is the only one we have observed tosneeze out the fluid.
The Falconidae. A male and female Pigmy Falcon (Poliheirax semitorquatus),each weighing between 50 and 55 g, were observed for several months; both birds
occasionally sneezed out minute and uncollectable droplets of secretion while feeding.
The total amount voided during a meal was probably always less than 5 ~1. A sample
of one secretion was finally obtained. It was hyperosmotic to blood for Na+, Cl-,and other ions, whereas Na+ and Cl- in the urine were hypotonic to the expectedblood values, while the concentration of K+ was much higher. One hundred milligrams of NaCl added to 10 g of chicken meat produced a somewhat more copious
secretion from the female, but she nevertheless died from the treatment.
A female American Kestrel (Fake sparverius) produced rather concentrated
urine, by comparison with the other species,and the ionic concentrations of her bloodplasma were unusually high also (table 1) . This increased blood concentration may
have significance in explaining the fact that this kestrel was never observed tosecrete nasal fluid.
Our observations on the Pigmy Falcons, Meng’s Peregrine Falcon, the Saker,
and the Red-necked Falcon indicate that those species of Falconidae that secrete a
nasal fluid typically eliminate the material by sneezing rather than by head-shaking,as in the Accipitridae. Furthermore, the amount of secretion voided ‘during a mealis considerably less for falcons than for accipitrids of comparable size. Some species
apparently do not secrete at all (table 2). Our data also indicate the possibility
that the urine of members of the Falconidae is more concentrated in electrolytes
than the urine of the Accipitridae. While this point requires further investigation,
we suggest that the Falconidae may have largely obviated the need for an extrarenal mechanism of salt excretion by enhancing the ability of their kidneys to concentrate. If the high blood values of the kestrel are typical of falcons, then thiswould be another physiological attribute of this family that would reduce the needfor an extrarenal excretion of salt.
Anatomical considerations. Presumably the secretions that we have observed
come from the nasal glands, although we have no direct evidence that this is so.
Except for the aegypine vultures, the nasal glands of the Falconiformes are muchsmaller than the functional salt-secreting glands of marine birds (Technau, 1936).
Moreover, the shape and position of these glands in the orbital region vary considerably among the groups of falconiform birds. We found that the general shape andposition of the glands from the Pigmy Falcon, American Kestrel, Greater Kestrel(Fake rupicoloides), and Yellow-headed Caracara correspond closely to those given
for the Gyrfalcon (Falco rusticolus) by Technau ( 1936: 571). The glands of thesefalcons are rather ovoid in shape, only slightly flattened, and lie with approximately
the anterior half in the orbital sinus and the posterior half in the orbit itself (positionIIa, preorbital-interorbital, of Technau’s classification, p. 594). Technau gives theweight of the preserved Gyrfalcon gland as 25 mg (approximately 2 mg of glandper 100 g body weight), whereas the wet weight of the Pigmy Falcon gland was 5
mg (approximately 10 mg per 100 g body weight). Although the American Kestrel,Greater Kestrel, and Yellow-headed Caracara are considerably larger in body size,
their glands are not much larger than that of the Pigmy Falcon. It may be a significant association that neither the American Kestrel nor the caracara was observed
to secrete, but caution should be exercised in generalizing from observations basedon single individuals of a species. We have some evidence that the influences of346

TOM J. CADE AND LEWIS GREENWALD

captivity on a wild hawk may inhibit secretion. The hand-reared Bateleur referred
to previously always secreted copiously when fed, but a wild-caught and untamed
individual of the same age did not secrete at all for the first two weeks after capture.
Even after a month of captivity, although calm enough to feed freely from the hand,
this bird secreted only a few drops of fluid during a meal. All of the birds listed intable 2 as not secreting were wild-caught individuals that were always nervous whenhandled. All of those that secreted copiously were quite tame.
The shape of the glands from the Gabar Goshawk and the Sharp-shinned Hawk
correspond closely to the description given by Technau for the glands of Accipitertisus and A. gent&.
These accipiterine glands are thin, elongate strips of tissue,
but whereas Technau (p. 595) gives the position for the two species he observed asIId, exorbital, the position of ours corresponds more closely to position IIb, interorbital. They lie entirely in the orbit, appressed against the ventral surface of thefrontal bone and near the bony septum between the two orbits. Technau gives theweight of the Goshawk’s gland as 20 mg, about the same relative size as the Gyrfalcon’s, and of the European Sparrowhawk as 6 mg. A freshly preserved gland fromMicroniszcs gabar weighed about 7 mg (approximately 4 mg of gland per 100 g bodyweight).
The gland of the Black Kite is also elongate but thicker than the accipiterine
glands. It lies with part of its body against the bony rim of the orbit and partagainst the connective tissue sheath that stretches between the dorsal edge of theorbit and the frontal shield, in a position approximating IIc, interorbital-exorbital.
The glands of the Red-tailed Hawk and the Savannah Hawk also lie in positionIIb, interorbital, but in each of these species there is a distinct depression in theventral surface of the frontal bone, in which the glands are lodged. Moreover, theglands are thicker and oval in shape rather than thin and elongated. Examinationof a mummified head of a Bateleur found dead in the Kalahari revealed a similar
shape and location, also with a depression in the frontal bone.
An 8.5kilogram Lappet-faced Vulture collected in the Namib Desert had anasal gland weighing approximately 400 mg-an elongate kidney-shaped organ 25 x
8 x 5 mm, lying in position Ha. The gland of this vulture is larger than any listed
by Technau for members of the Pelecaniformes and is close to the size of theHerring Gull’s (Larus urgent&us) supraorbital gland.
This cursory examination of morphology indicates that a detailed study of nasal
glands in the Falconiformes might yield some useful taxonomic information. The
fact that the gland of the Savannah Hawk is like that of the Red-tailed Hawk andnot like the glands of the accipiters is another suggestive reason for removing Heterospizias from the Accipitrinae, where it is usually placed, and including it with the
Buteoninae instead.
GENERAL DISCUSSION
In early studies on the function of nasal salt glands in pelecaniform and charadriiform birds, it became evident that these glands serve as organs of osmotic regulation, secreting hyperosmotic solutions of NaCl in response to salt-loading (SchmidtNielsen et at., 1958; Fange et al., 1958). It was later shown that these glands areunder central nervous, cholinergic control and respond to any increase in blood
osmolarity by secreting salt solutions that are hyperosmotic to the blood (SchmidtNielsen, 1960). The general conclusion from this fascinating work seemed to be thatfunctional nasal glands represent a specialized adaptation for marine existence.

NASALSALT

SECRETION

IN FALCONIFORM

BIRDS

347

Nasal salt secretions have now been described in 10 avian orders and in a few
species of reptiles (Schmidt-Nielsen, 1960; Schmidt-Nielsen et al., 1963 ; Coach,
1964; Norris and Dawson, 1964; and our study). Although the nasal glands ofmarine birds are most conspicuously developed (Technau, 1936) and are capableof high rates of flow (Schmidt-Nielsen, 1960)) there is no a priori reason why thesmaller nasal glands of many terrestrial birds should not also be functional; that is,capable of secreting a salty fluid hyperosmotic to the blood. Schmidt-Nielsen et al.
(1963) have recently reported that this is indeed the case for two terrestrial birdsof desert habitat, the Ostrich (Struthio camelus) and a North African partridge(Ammoperdix heyi) ; but they presented no data on either the concentrations of theions or on the rates of flow of the solutions secreted by these birds. We are now
able to provide some corrobo8rativedata on 21 terrestrial speciesin the order Falconiformes. It may be that the relative size of the nasal gland is associated primarily
with rates of flow and not at all, or only to a small extent, with concentrating ability.
As a result of his recent experience with terrestrial birds and lizards, SchmidtNielsen (1964) has broadened his concept of the extrarenal mechanism for reducing
plasma osmotic pressure to include the interesting idea that such a mechanism may
have been a prerequisite for birds to take full advantage of the water economy
inherent in uric acid excretion. His argument is approximately as follows: Uric
acid cannot be concentrated to the maximum degree in the kidney tubules without
clogging them and the ureters; hence, the uric acid arrives in the cloaca with a large
amount of water. This water is probably removed from the uric acid by an active
transport of sodium with a passive following of water, in accordance with the prevailing notion that active transport of water is energetically improbable and not yet
convincingly demonstrated in any biological system. Such a mechanism leaves thebird or reptile with the problem of excreting the salt that is moved across the cloaca
into the blood. Schmidt-Nielsen’s scheme further suggests that it is necessary for
the water and salt voided from the cloaca to form at most an isotonic solution withrespect to blood, since a greater concentration of salt would hold back water andmilitate against the water-conserving properties of uric acid. There are some difficulties with this hypothesis, not the least of which is the fact that it remains to beshown unequivocally that there is a concentration or precipitation of uric acid in
the cloaca, but the scheme seems reasonable and worth pursuing.
Implicit in Schmidt-Nielsen’s thinking is the idea that as a result of the movement of sodium and water across the cloaca the blood becomes concentrated withrespect to sodium. It is not immediately clear from Schmidt-Nielsen’s presentation
why this should be so; it is because birds lose large amounts of ion-free waterby evaporation from their respiratory systems (see Bartholomew and Cade, 1963).
Thus, if a bird’s urine is usually hypotonic or isotonic to its blood and it acquires
appreciable quantities of electrolytes from ingested food or water, then-quite apartfrom any mechanism involving the movement of sodium from the cloaca to concentrate uric acid-the organism must have an extrarenal route for excreting salt inorder to remain in water and salt balance; or it must drink a sufficient amount ofion-free water to compensate for the evaporative loss.
Carnivorous birds provide an instructive case in point. Our data indicate thatfalconiform birds typically pass a cloaca1 fluid with hypotonic concentrations of Na+
and Cl-. Although sometimes drinking free water, these birds are quite capable ofmaintaining water balance with only the preformed water taken in their fleshy food
(Bartholomew and Cade, 1963). Since raptors eat freshly killed prey with water

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J. CADE

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GREENWALDTABLE 3
WATER AND SALT REGULATION IN A SMALL ACCIPITER
Item considered(1) Total body weight(2) Wet weight of daily food ration(3) Water content of food(4) Dry weight of food(5) Oxidative water from 10 g ofprotein(6) Total water from food(7) Evaporative loss of water
(8)
(9)
(10)
(11)
(12)
(13)
(14)
(15)
(16)

Computation or measurement

Value

Direct weighing
Direct weighing
665/3%, standard value1
Item (2) minus item (3)Item (4) x 0.449, based onuric acid end product1
Item (3) plus item (5)2.5% body wt/day, from generalized wt relative curve’
Item (6) minus item (7)60 mmole/kg wet wtS
Flame photometer

150 g

Water available for excretion
Total Na+ content of food
Average Na+ cont. in urine
Estimated total Na’ excreted bykidney/day
Item (8) x item (10)Excess Na’ to be excreted
extrarenally
Item (9) minus item (11)Volume of nasal secretion required
loo0 mmole/liter = 0.21 mmole/Xpl,
Estimated total K’ content of food 42 mmole/kg wet wt’
Flame photometer
Average K’ cont. in urine
Estimated total K+ excreted bykidneyItem (15) x item (8)1 Schmidt-Nielsen, 1964.

*Bartholomew and Cade, 1963.

30 g
20 g
10 g
5g
25 g
3.75 g21.25 g
1.8 mmole
75 mmole/liter1.59 mmole
0.21 mmole
X = 210 ~1
1.26 mmole
50 mmole/liter
1.06 mmole

3 Pitts, 1963.

and electrolyte compositions similar to their own, the salt and water obtained fromtheir food should be essentially isosmotic to their own body fluids. With evaporation as a significant factor in the total loss of water, but not of ions, these birds
must acquire a salt load from their food; and it seemsplausible that the nasal glands
play a role in eliminating the excess sodium chloride. Such a mechanism has evengreater significance for a raptor living in the desert, where rates of evaporation arehigh and where ion-free drinking water is of limited occurrence.
Let us consider a small accipiter weighing 150 g. Under moderate conditionsof temperature and humidity, for instance 20” to 25°C and 30 to 40 per cent relative
humidity, such a hawk can maintain body weight indefinitely on about 30 g of whole
mouse tissues per day without drinking. Certain quantitative implications of thisration for the regulation of water and salts are shown in table 3. The hawk ingests
approximately 1.8 mmoles of Na+ per day in its food. Although most of these ionscan be eliminated by a copious flow of hypotonic urine, about 0.21 mmoles remain
to be accounted for. Given an average Na+ concentration of 1000 mmole/liter forthe nasal secretion, these excess ions could be excreted in a volume of 210 ~1. Our
observations during the feeding of the Gabar Goshawk, for instance, did not suggest
a volume of secretion of this magnitude, but it is not unreasonable to suppose thathawks secrete at other times of the day also, as indicated by the accumulation ofsalt crystals in the nares.
Potassium is excreted mainly through the urine. The total intake in the food isabout 1.26 mmole, of which we can account for 1.06 mmole assuming an averageurine concentration of 50 n-mole/liter. Since individual samples of urine frequently
contain much higher concentrations and since there is the distinct possibility of aNASALSALT

SECRETION

IN FALCONIFORM

BIRDS

349

24-hour cycle of changes in these concentrations, we believe it is safe to assume thatthe kidney of hawks is able to handle the entire potassium load from the food,
although the nasal secretion does carry a small amount.
It is also interesting to consider the implications of a 30 g ration of butchered
meat (muscle). The water content amounts to about 78 per cent of the wet weight,
the Na+ concentration is very low, about 10 mmole/liter of water in the muscle, andthe K+ concentration is very high, about 160 mmole/liter (Pitts, 1963). The bird
has about 23 g of water available for excretion, giving a potential Na+ excretionfrom the urine alone of 1.15 mmoles per day, whereas the food ration contains only
about 0.234 mmoles. Obviously, sodium is no problem with this type of food. The
ingested potassium, on the other hand, amounts to about 3.74 mmoles. To excrete
this amount with the water available from the food, the average urine concentrationof K+ must be around 162 mmole/liter. Again, since we often obtained values forindividual urine samples well over 200 mmole/liter, we believe the falconiform
kidney is able to handle a potassium load of this magnitude. Occasional nasal secretions also contain rather high concentrations of .K+ and may sometimes contributesignificantly to the removal of this ion.
The most critical factor in all of this regulation is the rate of evaporation. In
falconiform birds, the upper limit to the amount of the total available water (preformed and oxidative) that can be lost by evaporation without producing a water
deficit seems to be determined by the volume and concentration of the nasal secretion for Na+ and by the concentrating ability of the kidney for K+. If the evaporation from our hypothetical hawk is increased to 10 per cent of its body weight per
day under conditions of high temperature and low humidity, a rate of evaporation
quite to be expected for a small bird living under desert conditions, then only 10 gof water are available for urine formation and nasal secretion on the mouse ration.
The average concentration of Na+ in the urine would allow only for the excretionof 0.75 mmoles out of the total 1.8 mmoles ingested, if all of this water were used
for urine. At a concentration of 1000 mmole/liter, it would take about 1 ml of nasal
secretion to excrete the remainder. The urine concentration of K+ would have .toaverage about 126 mmole/liter .
We do not know for sure that these concentrations and volumes can be realized
by an actual hawk of the size considered, but these simple calculations do illustrate
the obvious adaptive advantage, in terms of water conservation, of a functional saltsecreting gland for terrestrial, carnivorous birds that are not drinking. In fact, thisfunction may well have its greatest adaptive significance for nestling hawks, which,as Gordon (1934) pointed out long ago, are absolutely dependent upon the water intheir fleshy food and which are often exposed to rather intense heating by radiationin their open nests. A recent observation on a three- to four-day-old Bateleur chickin Kruger Park is indicative. When the bird was exposed to sunlight in its nest, itsoon began to pant, and in less than one minute thereafter a salty-tasting fluid
appeared in its nares.
SUMMARY

Many birds of prey exude a clear fluid from their nares while eating. In an
examination of 16 speciesof Accipitridae and 8 speciesof Falconidae, we found these
secretions to contain high concentrations of Na+ and Cl-, which were always hypertonic to known values for blood. Potassium ions were excreted mainly in the urine.
The gustatory process seems to provide some nonosmotic stimuli that promotesecretion.

350

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J. CADE

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GREENWALD

Presumably the secretion comes from the nasal glands, but we have no direct
proof that this is so. Except for the aegypine vultures, the nasal glands of falconiforms are much smaller than the functional salt-secreting glands of comparable-sizedmarine birds, but there is no a priori reason why a small gland should not be functional. Size of the gland may be associated only with the volume of secretion andnot with concentrating ability. The morphology of falconiform nasal glands shows
considerable differences among species groupings and might serve as a useful tool
for taxonomic considerations. The accipitrid species typically void the secretion byshaking their heads from side to side, and they secrete larger volumes than thefalcons, which sneeze out the fluid.
The main adaptive value of a functional salt gland for terrestrial, carnivorous
birds seems to be associated with the fact that they acquire a sodium load from theirfood that is not easily excreted by their typically hypotonic urine. Evaporation
results in a further concentration of the ingested electrolytes, but the salt gland
may function effectively enough in some species to permit them to remain in waterbalance solely on the preformed and oxidative water associated with their food, evenin the face of relatively high rates of evaporative loss. We have examined somequantitative aspects of this problem.
ACKNOWLEDGMENTS

This study was supported by a grant from the U.S. Public Health Service, ES
00008 (Environmental Health). We thank Philip B. Dunham for his wise advice
and for making his laboratory and equipment available for our use. Also, John
Stangel helped by doing the analyses for phosphate ion. Above all, we express our
deep appreciation to the National Parks Board of Trustees, Republic of South Africa,
for the many courtesies extended to us during our visit to the Kalahari.
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COOCH, F. G. 1964. A preliminary study of the survival value of a functional salt gland inprairie Anatidae. Auk, 81:38&393.
FHNGE, R., K. SCHMIDT-NIELSEN, and H. OSAKI. 1958. Salt gland of the Herring Gull. Biol.
Bull., 115:162.
FISKE, C. H., and Y. SUBBAROW. 1925. The calorimetric determination of phosphorous. J. Biol.
Chem., 66:375+00.
GORDON,S. 1934. The drinking habits of birds. Nature, 133:436-437.
MCFARLAND, L. Z. 1965. Influence of external stimuli on the secretory rate of the avian nasal
salt gland. Nature, 205:391-392.
NORRIS, K. S., and W. R. DAWSON. 1964. Observations on the water economy and electrolyte
excretion of Chuckwallas (Lacertilia, Sauvomalus). Copeia, 1964:638-646.
PITTS, R. F. 1963. Physiology of the kidney and body fluids. Year Book Medical Publishers
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SCHMIDT-NIELSEN, K. 1960. The salt-secreting gland of marine birds. Circulation, 21:955-967.
SCHMIDT-NIELSEN, K. 1964. Desert animals. Oxford University Press.
SCHMIDT-NIELSEN, K., A. BORUT, P. LEE, and E. CRAWFORD,JR. 1963. Nasal salt excretion andthe possible function of the cloaca in water conservation. Science, 142:1300-1301.
,SCHMIDT-NIELSEN, K., C. B. JORGENSEN,and H. OSAKI. 1958. Extrarenal salt excretion in birds.
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Department of Zoology, Syracuse University, Syracuse, New York, 22 September
1965.