SUMMARY
The involution of the bursa of Fabricius begins in the autumn and is fully achieved by the end of the winter in all studied species. The presence of this organ may be used as an age criterion in shorebirds collected during fall migrations. The degree of cranial ossification does not permit distinguishing young birds from adults, since large "windows" persist generally in adult was well as in juvenile shorebirds. Two different patterns of cranial ossification are found in shorebirds; one applies to most species while the other one is found in the American Woodcock, Common Snipe, Knot, and Short-billed Dowitcher. The genera of Charadriidae attain a higher degree of cranial ossification than the genera of Scolopacidae. The authors also discuss the adaptive value of the skull pneumaticity.
A study of age criteria in some species of North American shorebirds
brought us to consider two of the best known techniques of age deter-
mination in birds, the size of the bursa of Fabricius and the degrees and pat-
terns of skull pneumatization. The only attempt, known to us, to correlate
bursa of Fabricius and gonadal development with the ossification of the skull
is that of Davis (1947).
The bursa of Fabricius is a lympho-epithelial organ lying dorsally above the
cloaca. At least in some species it has an opening in the cloaca. It reaches its
maximum size at 4-6 months and then begins involution (Davis, 1947). By
cloacal examination of the bursal pouch, it is possible to distinguish juvenile
from adult individuals of some taxa of birds especially Anseriformes and
Galliformes (Gower, 1939; Hochbaum, 1942; Linduska, 1943; Kirkpatrick,
1944). Unfortunately, in shorebird species, the bursa of Fabricius has no
cloacal opening and thus cannot be used as an age criterion of living birds.
The pneumatization of the skull has been used as a criterion for estimating
the age of birds by C. L. Brehm as far back as 1822 (Niethammer, 1968),
but it was not generally used until the turn of the century (Serventy et al.,
1967). Miller (1946) describes the skull ossification process as follows:
"The skull of a passefine bird when it leaves the nest is made of a single layer of bone
in the area overlaying the brain; at least, the covering appears single when viewed mac-
roscopically. Later the brain case becomes doubledayered, the outer layer being separated
from the inner layer by an air space across which extend numerous small columns of
bone .... Externally the skull of an immature bird appears uniform and pinkish in live
or freshly killed specimens. The skull of the adult is whitish, due to the air space, and
also it is finely speckled as a result of the dense white bony columns between the layers."
Nero (1951) and Serventy et al. (1967), in their respective studies of Passer
domesticus and Taeniopygia castanotis, give examples of the pattern and rate
of cranial ossification, from the juvenile to the adult; through a series of
stadia ending with the complete pneumatization of the cranial roof in the adult
before it is one year of age. This general rule, applied to the Passerines, ad-
mits some exceptions as mentioned by White (1948), Chapin (1949), Grant
(1966), McNeil and Martinez (1967), and Payne (1969). Chapin (1949)
also reported that "swifts and small sandpipers retained a condition through-
out life that suggested immaturity. In some other larger birds the pneumatiza-
tion of the cranial vault seemed to proceed very rapidly." Other workers like
Chapin (1949), Verheyen (1953), Harrison (1958, 1964) were interested in
329
330 THE WILSON BULLETIN Septenber 1972
Vol. 84, No. 3
the evolutive and adaptive significance of the fully versus incompletely pneu-
matized skull in birds.
Although cognizant of the fact that adult shorebirds have incompletely
ossified cranial roofs, we undertook the present studies to ascertain whether
or not the rate of skull ossification can be used as an indication of age in
living and dead birds.
MATERIAL AND METHODS
Series of shorebirds representing 21 species were collected in the Kamouraska region,
Quebec, on the south shore of the St. Lawrence River in 1968 (spring, summer, and fall)
and 1969 (spring), and on Magdalen Islands, Quebec, in fall 1969. A few specimens
also were brought from Venezuela by the senior author in November 1968. These speci-
mens were all prepared as study skins to examine the age characteristics, but the skull
roofs were removed and kept separate for further examination of the unpneumatized
areas. These skull vaults were then held against a window allowing light to illuminate
the unpneumatized areas which were outhned.
The cloaca of each bird was excised and measurements (mm) were taken of the length
(A) and height (B) of the fresh bursa of Fabricius; both measurements were used in
the approximation of the size of the organ (AB). All birds which had a bursa of Fabricius
were considered as immature. However, some birds which had a damaged cloaca were
considered as immature if they bore juvenile feathers, especially among the wing coverts.
In addition to the above mentioned specimens, we used measurements of the bursa taken
by Miss Franoise Cadieux during another study.
RESULTS AND DISCUSSION
Bursa o] Fabricius.--The bursa of Fabricius was absent in yearling speci-
mens taken in May and June. Thus the bursa is eliminated within the first
year of growth. Moreover, two specimens from Venezuela in November, a
Least Sandpiper (Erolia minutilla) and a Lesser Yellowlegs (Totanus fiavipes),
had almost fully regressed bursae, though their basic I plumage (first winter)
still retained characteristic juvenal feathers. This suggests that, at least in
some individuals, the involution of the bursa of Fabricius is completed in less
than six months.
The measurements of the average size of the bursa (-'), as shown in Table
1, indicate that the size of this structure diminishes from July to November.
The best examples are the Semipalmated Plover (Charadrius semipalmatus),
the Ruddy Turnstone (4renaria interpres), the Greater Yellowlegs (Totanus
melanoleucus), Lesser Yellowlegs, and the Short-billed Dowitcher (Limno-
dromus griseus). The same general trend appears in most of the twelve re-
maining species, but less clearly because of too small sample sizes.
Cranial Ossi]ication Patterns.--All adult as well as immature skulls were
characterized by the presence of unpneumatized "windows," the size of which
shows great individual variations. Two different patterns of cranial pneumati-
McNeil AGE CRITERIA IN SHOREBIRDS 331
and Burton
332 THE WILSON BULLETIN Scptcnlber 1972
Vol. 84, No. 3
Fig. l. Different stages of the type I of cranial pnemnatization pattern in North Aner-
ican shorebirds. The clear areas represent the absencc of pnemnatization.
zation are found among the species of shorebirds belonging to the two families
that were investigated (Charadriidae and Scolopacidae). The type I (Fig.
1) occurs in the majority of the species of both families (Table 2). It was
divided into ten stages of degrees which do not clearly appear to be related
to age but may be progressive. Four species had a different pattern that we
are designating as type I! (Fig. 2), in which we distinguished six consecutive
stages. These species were the Common Snipe (Capella gallinago), Knot
(Calidris canutus), Short-billed Dowitcher, and American Woodcock (Philo-
hela minor).
Cranial pneumaticity cannot be used as an indication of the age of shore-
birds. In fact, no clear correlation exists between the age of the birds and
the extent to which their skulls are ossified (Tables 2 and 3); some immature
(first year) birds have a skull roof as pneumatized as that of some adults.
McNeil AGE CRITERIA IN SHOREBIRDS 333
and Burton
Fc. 2. Different stages of the type II of cranial pneumatization pattern in North Amer-
ican shorebirds. The clear areas represent the absence of pneumatization.
However, the different stages found in each type of cranial ossification are
probably time progressive. Categories 7 and 8 in Table 2 are found almost
exclusively in the adult age class, which suggests that there may be some age
significance.
The extent of skull ossification attained in the shorebird species following
the type I of cranial pneumatization (Table 2) varies between the genera and
species. It seems obvious that the genera of Charadriidae attain a higher
degree of cranial ossification than the genera of Scolopacidae. The stages or
categories numbered 6, 7 and 8 are found almost exclusively in Charadrius,
Pluvialis, Squatarola, and Arenaria, while the stages numbered 1 and 2 are
found almost exclusively in the genera of Scolopacidae, especially in Erolia,
Ereunetes, Limosa, and Crocethia. The two Totanus species seem to be inter-
mediate between the two groups. It would be hazardous to draw conclusions
about Numenius, Actitis, and Tringa because of the small sample sizes.
334 THE WILSON BULLETIN
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McNeil AGE CRITERIA IN SHOREBIRDS 335
and Burton
336 THE WILSON BULLETIN Scptcmbcr 1972
Vol. 84, No. 3
all
cNei AGE CRITERIA IN SHOREBIRDS 337
and Burton
A few workers have attempted to find the evolutionary and/or adaptive
significance of the fully versus incompletely pneumatized skull vault in birds.
Chapin (1949) mentioned that "the skull-roof of most woodpeckers is com-
posed of single layer of bone, thicker and stiffer than that seen in the young
of Passeres." He "considered this as a direct adaptation to their hammering
and the use of the beak as a chisel." As far as Verheyen (1953) is concerned:
"les os dermiques pneumatiques prsentent... l'avantage de mieux resister aux vibrations
et de mieux amortir les secousses que les lames paisses qui manquent de souplesse. Aussi
la plupart des espces arboricoles (donc celles qui, au conrs de leurs Evolutions aCriennes,
penvent se cogher la tgte contre divers obstacles) possdent-elles un crane pneunatique
tandis que celles qui vivent sur l'eau on qui vitent les terrains boiss out un dermatocr&ne
incompltement pneumatis."
On the other hand, according to Harrison (1958), the skull pneumaticity of
birds is related to their mode of life, depending upon whether they are swim-
ming or diving birds, hammering species, swift or slow fliers. Harrison (1964)
believed that birds "showing diminished pneumatisation can be loosely classi-
fied as "swift fliers" and include such species as the gallinaceous birds (Galli-
formes) which accelerate rapidly, sandgrouse (Pteroclididae), most of the
limicoline birds (Charadrii), and the swifts Apus apus and A. a]]inis. An
exception among the Charadrii is the slow-flying Jack Snipe Lymnocryptes
minimus, which develops complete pneumatization." The present results indi-
cate that the Killdeer, American Woodcock, Common Snipe, Knot, and Short-
billed Dowitcher are the shorebird species that show less unpneumatized
skulls: some specimens of these species had almost fully ossified skulls, almost
as pneumatized as that of the Jack Snipe. One fact is against Harrison's theory
of swift versus slow fliers. The Common Snipe, while performing its aerial
nuptial evolutions, dives to the ground from at least a hundred yards and then
suddenly, before swooping down upon the ground, turns back abruptly and
starts again the same aerobatics. The Killdeer, American Woodcock, Common
Snipe, Knot and, even the Jack Snipe (Bent, 1927, 1929), also perform aerial
evolutions at the time of breeding, although they are less spectacular. This
means that these species are subjected to a heavy acceleration followed by an
equal deceleration, and according to Harrison's theory, a much less fully ossi-
fied skull would be advantageous.
On the other hand, we would be tempted to make a comparison between
the incompletely ossified skull of shorebirds and the ones of the woodpeckers.
According to Harrison (1964), "the partial absence of skull pneumatization
in woodpeckers suggests that this type of skull may be relatively heavier and
therefore a more effective hammer." Shorebirds, excluding plovers and turn-
stones, feed by probing and making series of holes in sand and/or mud, so
it may be that a heavier type of skull could possibly be of some advantage.
ACKNOWLEDGMENTS
The study was undertaken as part of the M.Sc. research program of the junior author,
and was supported by a National Research Council of Canada research grant to the senior
author and a scholarship to the junior author. We are indebted to Miss Franoise Cadieux
who provided some useful data and to W. Earl Godfrey who read the manuscript.
LITERATURE CITED
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142.
BENT, A.C. 1929. Life histories of North American shorebirds. U.S. Natl. Mus., Bull.
146.
CaaeN, J.P. 1949. Pneumatization of the skull in birds. Ibis, 91:691.
Dams, D.E. 1947. Size of bursa of Fabricius compared with ossification of skull and
naturity of gonads. J. Wildl. Mgmt., 11:244-251.
GOWEa, I.O. 1939. The use of the bursa of Fabricius as an indication o.f age of game
birds. Trans. N. Amer. Wildl. Conf., 4:426-430.
GauNT, P.R. 1966. Retarded or arrested cranial development in a Mexican passerine,
Myiopagis viridicata (Vieillot). Amer. Midl. Nat., 75:142-149.
HaaRsoN, J.G. 1958. Skull pneumaticity in wildfowl in relation to their mode of life.
The Wildfowl Trust Ninth Annual Report (1956-1957):193-196.
HaRmsoN, J. G. 1964. Pneumatisation of bone. In Thomson, A. L. (Ed.), New dic-
tionary of birds. McGraw Hill, New York, pp 649q550.
HOCHIAIJM, H.A. 1942. Sex and age determination of waterfowl by cloacal examina-
tion. Trans. N. Amer. Wildl. Conf., 7:299-307.
IrdaIeATRCI, C.W. 1944. The bursa of Fabricius in Ring-necked Pheasants. J. Wildl.
Mgmt., 8:118-129.
LtNI)USICa, J.P. 1943. A gross study of the bursa of Fabricius and cock spurs as age
indicators in the Ring-necked Pheasant. Auk, 60:426-437.
MeNEra, R., ANI) A. MARTINEZ. 1967. Retarded or arrested cranial development in
Myiornis ecaudatus. Wilson Bull., 79:343-344.
MILLER, A. H. 1946. A method of determining the age of live passefine birds. Bird-
Banding, 17:33-35.
NERO, R. W. 1951. Pattern and rate of cranial "ossification" in the House Sparrow.
Wilson Bull., 63:84-88.
NIETnAER, G. 1968. Pnemnatization of the cranium as a criterion of age. Ibis, 110:
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cNa AGE CRITERIA IN SHOREBIRDS 339
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PAYNE, R. B. 1969. Unpneumatized skull condition in adult Scaly-fronted Weavers,
Sporopipes jrontalis. Auk, 86:570.
SERVENTY, D. L., C. A. NICttOLLS, AND D. S. FARNER. 1967. Pnemnatization of the
cranium of the Zebra Finch, Taeniopygia castanotis. Ibis, 109:570-578.
VERHEYEN, R. 1953. Contribution & l'tude de la structure pneumatique du crane chez
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DPARTEMENT DES SCIENCES BIOLOGIQUES, UNIVERSIT DE MONTREAL, C.P. 6128,
MONTREAL 101, QUEBEC, CANADA. 12 OCTOBER 1971.
REQUEST FOR INFORMATION: SANDERLING
For the past two years, the Long Point Bird Observatory has undertaken a study on
the relationship between fat deposition and fall migration in the Sanderling. In conjunc-
tion with this study, a large number of birds have been color-marked and sightings of
these marked birds away from Long Point have indicated that most of the birds fly
directly from the study area to the East Coast.
During 1972, the Observatory hopes to individually color-mark and color-code several
hundred Sanderling in order to further investigate this phenomenon.
Birds will be feather-dyed on the breast and abdomen with one of four colors: red,
yellow, green, or white (no color); according to the percentage of the bird's total body
weight attributable to fat.
The birds will be wing-tagged on each wing with semi-permanent wing tags of the
following colors: black, blue, brown, green, red, orange, yellow, and white. The wing-
tagging will individually identify each bird.
Birds banded on the right leg will be adults and those banded on the left leg will be
impnatures.
The Observatory would be pleased if anyone sighting these birds would report the
following information to us: Date of sighting; Location (including nearest city or town);
Color of feather-dye on the breast and abdomen; Color of the wing tag on the right wing;
Color of the wing tag on the left wing; Leg on which the bird is banded.
Co-operators will receive a short note explaining the project's application to the preser-
vation of the Long Point peninsula in a natural state and the date on which the bird
was last seen on Long Point. Reports of marked birds should be sent to: Long Point
Bird Observatory, Long Point, Ontario, CAiNIADA.