Hereditas 94: 225-233 (1981)

Chromosomes in birds (Aves): evolutionary implications of

macro-and microchromosome numbers and lengths
HAKAN TEGELSTROM and HANS RYTTMAN

Department of General Genetics, University of Uppsala, Sweden

TEGELSTROM. H. and RYITMAN. H. 1981. Chromosomes in birds (Aves): evolutionary implications of

macro- and microchromosome numbers and lengths. - Hereditas 94: 225-233. Lund. Sweden. ISSN
0018-0641. Received November 6. 1980
The karyotypes of 234 bud species from published reports were analysed with respect to diploid number
ofchromosomes, number of macm and microchromosomes, length of microchromosomes compnrcd to
macrochromosomes, and centromeric position.
There seems to be a conservation of a standard bird karyotype with 16 macro- and 64 microchromo-
somes, @vhg the diploid chromosome number 80. However, in all orders investigated. there is a
tendency towards reduction of the number of microchromosomes and increase in the number of
macrochromosomes. We propose that the smallest macrochromosomes(nos. 7-10) have been created by
Robertsonian translocations of larger microchromosomes and that translocation of microchromosomes
to macrochromosomes shifts the centromeric position from telocentric to submetacentric or metacent-
ric .
Hikan Tegelstrom, Department of General Genetics, University of Uppsala, S-750 07 Uppsala, Sweden

The DNA content in birds and reptiles is smaller
than in mammals and the range of variation is
much less than in fishes and amphibians. The
range of DNA content per haploid cell is 1.7-2.3
pg in birds (BACHMAN et al. 1972) and 1.5-3.5 pg in
reptiles (HINEGARDNER 1976).
The chromosomes of birds and reptiles are
characterized by great variation in size and it is
common to speak about macro- and microchro-
mosomes although there is not always a sharp
borderline between the two groups.
To date, we have found reports presenting the
karyotypes of 302 different species of birds out of
a total of 8 700. Thus, 3.5 % of all bird species
have been karyotyped as compared to about 30 %
in mammals.
Unfortunately, not all of the reports can be used
in karyological comparisons, as the microchromo-
somes are often omitted. In this study, we have
compared the number of macro- and microchro-
mosomes of 234 species, omitting old reports
where the results are questionable. We have
avoided reports concerning the order Falconi-
fomes (around 30 species karyotyped) where the
karyotypes are not comparable to those in the
other orders.
The intriguing question about microchromo-
somes is why such a high proportion of small
chromosomes have persisted in birds and reptiles.
The existence of many small chromosomes seems
to be a specialized system for information storing,
and the hypothesis that chromosomal evolution
would tend to favour aggregations into fewer and
larger chromosomes has been put forward (SHOFF-
NER 1974).
It is difficult to make definite counts of the
number of microchromosomes, for two reasons.
Firstly, it is difficult to separate macro- from mic-
rochromosomes as there are no generally accepted
rules for this classification. Secondly, the smallest
microchromosomes are difficult to count in a light
microscope as (1) they can escape from the meta-
phase plates when the cell suspension is dropped
on the slide, (2) they can be hidden near the mac-
rochromosomes, (3) they can lie indistinguishable
near each other, and (4) small spots of dye and
stained dust can be misjudged as microchromo-
somes.
Methods
Reports on karyotypes of different species of birds
were collected. The diploid number of chromo-
somes (2n), number of macrochromosomes and
the number of microchromosomes were registered
(234 species). Where pictures were presented
showing the microchromosomes, these were
226 H rEGELSTROM ET AL. Hereditas 94 (1981)

measured with sliding callipers (88 species). The In many cases, it was necessary to lower the esti-
results are presented as microchromosome length mated number of macrochromosomes, there being
in percent of total genome length (including Z and a tendency to overestimate the number of macro-
W). When determining which chromosomes were chromosomes. There is also an obvious discrep-
macro- and which were microchromosomes, the ancy between authors about the definition of the
following criteria were used: two types of chromosomes. The criteria we have
used are tentative, but they have proved to be
1. The distinction between the two types of chro-
practical. Another way to define microchromo-
mosomes used by the author of a report was
somes is by an upper limit of length. OHNOet al.
used, if it did not contravene criteria number 2 ,
3 and 4.
(1Wproposed
) the limit to be 0.7pm. However,
this suggestion could not be used, as most authors
2 . There should be a discontinuity in length be-
do not provide a scale on their illustrations.
tween two groups of chromosomes where the
We classified the macrochromosomes of 74 ran-
group with small chromosomes are defined by
domly chosen species, according to centromeric
criteria 3 and 4.
position (Table 1). Only pictures were used where
3. Microchromosomes are small chromosomes
a judgement of the centromeric position was pos-
that are impossible to distinguish from each
sible or where the authors had classified the chro-
other.
mosomes according to centromeric position. The
4. I n microchromosomes, there should be no
chromosomes were designated as metacentric,
possibility of defining the centromeric position
submetacentric, subtelocentric or telocentric. The
when they are routinely stained with orcein or
species were classified into two groups with more
Giemsa.

Table I . Compilation of the species used for comparison of centromeric position

Order Family Species Reference

Struthioniformes Struthionidae Struthio camelus TAKACI and SASAKI 1972

Sphenisciformes Spheniscidae Spheniscus humboldti TAKACI and SASAKI 1974
Gaviiformes Gaviidae Gavia stellata HAMMAR 1970
Podicipediformes Podicipedidae Podiceps cristatus TAKAGI and SASAKI 1974
Ciconiiformes Ardeidae Ardea cinereo HAMMAR 1970
Ardeola grayii RAY-CHAUDHURI
1976
Threskiornithidae Threskiornis melanoee-
phalus TAKAGI and SASAKI 1974
Phoenicopteridae Phoenicoprerus ruber TAKAGI and SASAKl 1974
Anseriformes Anhimidae Chauna chavaria TAKAGI and SASAKl 1974
Anatidae Anser anser ITOH et d. 1%9
Anser cygnoides H A M M A R1966
Cygnus olor HAMMAR 1970
Branta canadensis HAMMAR 1970
Tadorna tadorna HAMMAR 1970
Anas platyrhynchos SHOFFNER 1974
Somateria mollissima HAMMAR1970
Aythya ferina HAMMAR1970
Aythya fuligula HAMMAR1966
Bucephala clangula HAMMAR 1970
Mergus merganser HAMMAR 1970
Galliformes Phasianidae Coturnix coturnix BENIRSCHKE and H S U 1971
Gallus domesticus BENIRSCHKE and H S U 1971
Phasianus colchicus BENIRSCHKE and H S U 1971
Pavo crisratus RAY-CHAUDHURIet al. 1%9
Numididae Numida meleagris BENIRSCHKE and H S U 1971
Gruiformes Rallidae Gallinula chloropus HAMMAR 1970
Fulica atra HAMMAR 1970
Porphyrio poliocephalus ITOH et d. 1969
Charadriiformes Haernatopodidae Haematopus ostralegus HAMMAR 1970
Charadriidae Vanellus vanellus HAMMAR 1970
Charadrius hiaticula HAMMAR 1970
Scolopacidae Numenius arquata HAMMAR1970
Tringa totanus HAMMAR I970
Gallinago gallinago HAMMAR 1970
Hereditas 94 (1981) CHROMOSOMES I N BIRDS 227

Order Family Species Reference

Burhinidae Burhinus oedicnemus BULATOVA et d. 1971
Laridae Larus argentatus RYTTMAN et d. 1979
Lorus canus RYTTMAN et d. 1979
Larus fuscus HAMMAR1970
Larus ridibundus HAMMAR1966
Sterna albifrons HAMMAR 1966
Sterna hirundo PICClNNl and STELLA 1970
Columbiformcs Ptcroclididae Prerocles exustus RAY-CHAUDHURI 1976
Columbidae Columba livia STOCK et d. 1974
Columba palumbus HAMMAR1966
Geopelia cuneata DE LUCCA and CHAMMA 1977
Psittaciformes Psittacidae Melopsittacus undufatus ROTHFELS et d. 1%3
Loriculus vernalis RAY-CHAUDHURI et al. 1969
Psittacula alexandri RAY-CHAUDHURI et d.1969
Cuculiformes Cuculidae Eudynamys scolopacea RAY-CHAUDHURI 1%7
Strigiformes Strigidae otus scops ITOH Ct d. 1969
Bubo virginianus BIEDERMAN et d. 1980
Athene brama RAY-CHAUDHURI et al. 1%9
Strix aluco HAMMAR 1970
Caprimulgiformes Caprimulgidae Caprimulgus aegyptius BULATOVA et d. 1971
Coraciiformes Coraciidae Caracias benghalensis MISRA and SRIVASTAVA I975
Passeriformes Motacillidae Anthus trivialis HAMMAR and HERLIN 1975
Campephagidae Caracina melanoptera RAY-CHAUDHURI et d. 1%9
Muscicapidae Saxicola torquata BULATOVA and PANOV 1973
Oenanthe deserti BULATOVA and PANOV 1973
Monticola saxatilis BULATOVA and PANOV 1974
Turdus merula HAMMAR 1970
Turdus leucomelas DE LUCCA 1974
Turdoides striatus RAY-CHAUDHURI et d. 1%9
Paridae Parus major HAMMAR 1970
Parus palustris HAMMAR 1970
Ccrthiidae Certhia familiaris HAMMAR 1970
Emberizidae Emberiza citrinella HAMMAR and HERLIN 1975
Fringillidae Fringilla coelebs PICClNNl and STELLA 1970
Carduelis chloris HAMMAR and HERLIN 1975
Ploceidae Passer domesticus BULATOVA et d. 1972
Passer hispaniolensis BULATOVA et d. 1972
Passer montanus HAMMAR 1970
Sturnidae Sturnus contra RAY-CHAUDHURI et d. 1969
Corvidae Pica pica HAMMAR 1966

or less than 60 microchromosomes. The choice of groups give too small a number of species in each
60 as dividing number of microchromosomes is group.
based on Fig. 1 c, where birds with less than 60 are
considered to have a low number, and birds with
62 or more are considered to have a high number
of microchromosomes. Birds with 60 microchro- Results
mosomes have not been included in the correla- The diploid number of chromosomes and the
tion calculations. number of macro- and microchromosomes in the
Our numbering of the autosomal macrochromo- 234 species are presented in Table 2. The table is
somes is not intended to imply any homology be- arranged according to the taxonomy of PETERS
tween the chromosomes. They are just numbered (1931-1978). In the orders of old evolutionary ori-
according to size, following the authors’ presenta- gin, the number of species investigated is low. In 8
tion. orders, the number of species is high enough to
The different bird species have been taxonomi- allow statistical treatment.
cally classified according to GRUSON (1976). The The diploid numbers of chromosomes in birds
lowest taxonomic rank possible to use in grouping (except Falconiformes) range from 40 (Burhinus
the data proved to be the order. Lower taxonomic oedicnemus) to 126 (Upupa epops) with a great
228 H. T E G E L S T R ~ MET AL Hereditas 94 (1981)

tendency for an increase or decrease in the num-

ber of microchromosomes or macrochromosomes

60
'O 1 I
during the long-term evolution.
The most impressive fact expressed by the figu-

so
40 1 res in Table 2 is the conservation of number of
chromosomes. A standard karyotype for birds
seems to be one with a diploid number of 80 with 8

1
30 macrochromosomes and 32 microchromosomes.
This karyotype is also expressed in the mean val-
ues of the orders Tinamiformes, Anseriformes,
/ I Galliformes, Strigiformes and Passeriformes.
I 80 !!
82 84
! !
88 ~0
These represent 66 % of the species investigated
The amount of DNA in the microchromosomes,
Diploid number here expressed as the relative length, ranges from
22 to 63 %, with a mean around 39 %.
We have tested the correlation between the
number of macro- and microchromosomes from
the orders with 6 species or more (see Table 2).

40 -
ll
30 - indicates an evolutionary connection between the
20 - sizes.
10 - If the regression lines are drawn, we can get a
c 0 2 0 25 30 35
Fig. 1a-r. The distribution of chromosomal numbers in
234 bird species. a Diploid numbers of chromosomes. b
Haploid numbers of macrochromosomes. c Haploid
numbers of microchromosomes.
number of species centering around 80. 61 % of
the species have a diploid number of 78-82 (Fig.
la). The haploid numbers of macrochromosomes
in birds (except Falconiformes) range from 5 to 14,
centering around 9 . 7 0 % of the species investigat-
ed have 7-9 macrochromosomes.
The numbers of microchromosomes range from
16 to 114 with a median value of 64. 73 % of the
species investigated have a microchromosome
number between 60 and 68 (Fig. lc). There is no
There is a negative correlation between the two
types of chromosomes within an order. When the
number of macrochromosomes increases, the
number of microchromosomes decreases. This
numbers of chromosomes of the two different
rough estimate of the decrease in the number of
microchromosomes when the macrochromosomes
increase by one. The mean of this estimate is 1.3.
In the order Charadriiformes, we found a decrease
amounting to 2.6 microchromosomes. A possible
explanation for the type of chromosomal change
involved in this negative correlation is found in
Table 3. Telocentric macrochromosomes are
much more common (40.2 %) in bird species with
many microchromosomes than in birds with few
microchromosomes (20.2 %). The opposite is true
for metacentric macrochromosomes (24.5 % and
40
36.5 % respectively). We propose that Robert-
sonian translocations of microchromosomes giv-
ing rise to small macrochromosomes are re-
sponsible for these chromosomal changes.
In birds with a high number of microchromo-
somes, the smallest macrochromosomes are pref-
erentially telocentric (79.6 %), but in birds with a
low number of microchromosomes, the smallest
macrochromosomes are metacentric (50.0 %) or
submetacentric (15.5 %).There is also a significant
difference among the first 6 macrochromosomes
as they are more frequently telocentric in birds
with a high microchromosome number.
This is further illustrated in Table 4 and Fig. 2
where the centromeric position has been deter-
mined in the different macrochromosomes. There
Table 2. The chromosomes in 234 species of birds belonging to 21 orders
3
Order Number of AU chromosomes, Macrochromosomcs. Microchromosomcs, Microchromosome Correlation ~ecreascofmicro- 3
species diploid number haploid number haploid number length between num- chromosomes when
berofmcro- macrochromosomes 5
h
Mean Range Mean Range Mean Range In 96 of Number and micro- incrcase by one,
genome ofspe- chromosomes mean L
B
cies

Struthioniformes 1 80 - 9 - 31 - 32 1
Rheiformes 2 76 12-82 6 - 32 30-35 47 1
cas&ormes 2 64/82 64-82 816 6-8 25/34 25-34 36 2
Tinamiformes 2 80 78-80 7 6-8 32 32-33 - -
Spknisciformes 1 78 - 8 - 31 - 36 I
Gaviiformcs 1 88 - 8 - 36 - 48 1
Podicipcdiformcs 1 78 - 9 - 30 - 30 1
Pelecdormes 2 68 670 8 6-1 1 26 22-30 22 1
Ciconiifonnes 13 70.724.9 62-80 11.022.5 614 24.424.6 20-34 31 3 -0.91 -1.6
Anseriformes 19 80.122.4 72-84 7.221.2 6-10 33.121.4 28-35 44.125.6 12 -0.69 -1.0
Galliformes I5 79.524.2 66-84 7.820.9 6-9 31.922.5 24-35 34.025.7 10 -0.58 -1.6
Gruifomcs 13 80 72-92 7 6-9 33 2740 41.8 3 -
Charadriiormcs 16 71.8212.2 40-98 9.522.1 7-13 28.925.9 8-42 35.1+11.1 12 -0.72 -2.6
Columbiformes I3 76.522.3 72-80 8.020.9 6-10 30.221.3 2634 33.225.6 6 -0.49 -0.7
Psittaciformes 6 67.725.3 58-72 7.420.9 6-12 27.421.7 22-30 33.9 3 -0.60 -1.2
Musophagiformes 2 76 72-78 6/13 6-13 23133 23-33 43.9 2 -
str@folmcs 9 79.822.3 7642 7.821.7 5-10 32.122.3 2ax 53.1 2 -0.87 -1.2
Caprimuigiformes I 70 - 12 - 23 - - - -
Coraciiformes 3 high 78-126 5.5 3-9 44 32-57 over50 2
Picifomes 3 85 84-92 9.2 7-12 33.3 28-37 - -
Passcriformes 109 79.023.9 68-90 8.221.3 6-12 31.522.1 26-37 39.526.1 25 -0.47 -0.7
Total 234 78.023.9 40-126 8.321.8 3-14 30.8+4.2 a57 38.928.8 88 -1.3320.62

h)
h)
W
230 H. TEGELSTROM ET A L . Hereditas 94 (1981)

Table 3. The per cent distribution of centromeric positions in macrochromosomes of 74 species of birds. Note especially the difference
in meta- and telocentric chromosomes between birds with high and low numbers of microchromosomes

Birds with more than 60 microchromosomes Birds with less than 60 microchromosomes

All First 6 Remaining All First 6 Remaining

Centromeric macro macro macro macro macro macro
position (n = 306) (n = 257) (n = 49) (n = 263) (n = 179) (n = 84)

Metacentric 24.5 27.2 10.2 36.5 30.2 50.0

Submetacentric 20.9 24.2 4.1 22.8 26.3 15.5
Subtelocentric 14.4 15.9 6.1 20.5 24.0 13.1
Telocentric 40.2 32.7 79.6 20.2 19.5 21.4

appears to be a difference in the centromeric posi-
tion of chromosomes 7 to 10 when the high and
low microchromosome groups are compared. The
low group has metacentric small macrochromo-
somes in contrast t o the telocentric ones in birds
with more than 60 microchromosomes.
Discussion
The investigated karyotyped species in different
orders reflect the total number of species in each
order. Almost 50 % of species investigated in this
study belong to the order Passeriformes. There is
also a good representation of species karyotyped
in “primitive” orders.
There are taxonomic problems that have not
been solved. These problems may be reflected in
our results, some orders being more heteroge-
neous than others. However, most taxonomic
problems being concerned with taxonomic levels
below the order, they do not influence the main
conclusions drawn from our material.
There is a great deal of uncertainty in using
pictures from published papers. Firstly, there is
the difficulty of counting the number of micro-
chromosomes, as pointed out by most authors.
We believe that many published karyotypes are
biased to the “normal karyotype” for the species.
It seems justified to define the number of micro-
chromosomes as a mean value with a standard
deviation, but this is never done. A standpoint
today is that we d o not know if there is a natural
variation in microchromosome numbers between
and/or in individuals.
Secondly, as mentioned in Methods, there are
also difficulties in defining the line of demarcation
between macro- and microchromosomes, there
being no general agreement about the criteria. We
have proposed some criteria for definition of the
microchromosomes in the Methods and they have
proved to be practical. We have estimated the
error of our measurements of total length of the

Table 4. The distribution of centromeric position in different macrochromosomes of 74 species of birds. Note the change of telocentric
chromosomes

Birds with more than 60 microchromosomes Birds with less than 60 microchromosomes

Meta- Submeta- Subtelo- Telo- Meta- Submeta- Subtelo- Telo-

centric centric centric centric centric centric centric centric
Chromosome % % % % n % % % % n

I 57.13 29.5 3.6 9.1 44 60.0 30.0 6.6 3.3 30

2 50.0 25.0 15.9 9.1 44 40.0 33.0 16.7 10.0 30
3 9.1 11.4 29.5 50 44 10.0 16.7 43.3 30.0 30
4 15.9 38.6 18.2 27.3 44 40.0 23.3 23.3 13.3 30
5 13.6 21.3 6.8 52.3 44 20.0 20.0 33.3 26.7 30
6 7.9 13.2 34.2 44.1 38 13.3 24.1 21.6 34.5 29
7 12.0 4.0 8.0 76.0 25 21.6 17.2 20.1 34.5 29
8 5.9 5.9 5.9 82.4 17 61.9 19.0 4.8 14.3 21
9 0 0 0 100 7 70.6 11.8 5.8 11.8 17
10 - - - - - 44.4 22.2 22.2 11.1 9
Hereditas 94 (1981) CHROMOSOMES IN BIRDS 23 1

“A
100

90

80

70

60

50

40

30

20

10

1 2 (3) 4 5 6 7 8 9 10 Mocrochromosomc

Fig. 2. Frequency, in percent, of centromeric position in different macrochromosomes of 74 species of birds,

illustrated diagrammatically for telocentrics and metacentrics. The figures are from Table 3.
Full lines = telocentric chromosomes; broken lines = metacentric chromosomes; filled dots = birds with more than 60 microchromosomes: open dots =
birds with less than 60 microchromosomes.
Chromosome no. 3 is omitted from the diagram.

microchromosomes to be around 15 %. The great- VEGNI-TALLURI (1966). However, in some orders

er part of the error depends on differences in the
number of microchromosomes determined by dif-
ferent authors. In many cases, the same species
proved to have different numbers of macrochro-
mosomes, probably owing to the difficulties in
making an accurate count. However, we do not
think that these methodological objections un-
dermine the hypothesis that we wish to present
concerning the evolution of bird karyotypes.
In the present material, there is neither a
gradual reduction nor an increase of microchro-
mosome numbers or total length during the long
term evolution in birds (Table 2). Instead, there
seems to be a conservation of a “normal karyo-
type” with around 16 macro- and 64 microchro-
mosomes, giving the diploid chromosome number
of 80. This was also observed by RENZONI and
(Charadriiformes and Ciconiiformes) there is an
obvious tendency to reduction in the number of
microchromosomes. This tendency is clearly
expressed in these orders, but seems to exist in all
orders investigated, there being a negative corre-
lation between the numbers of macro- and micro-
chromosomes. From the regression lines we esti-
mate the microchromosome reduction per one
new macrochromosome to be 1.2-2.6 in different
orders. This rather surprisingly low number indi-
cates that the largest microchromosomes are those
that are involved in the chromosomal rearrange-
ments. If this explanation is correct, birds with
many macro- and few microchromosomes should
show a more distinct gap between the two types of
chromosome. This is generally the case.
In the evolution of animals, Robertsonian trans-
232 H. T E G E L S T R ~ MET AL.
locations have played a primary role in creating
new chromosomes. This investigation gives
support to the idea that the smallest macrochro-
mosomes (number 7-10) have been created by
Robertsonian translocations between larger mic-
rochromosomes (Table 3, 4 and Fig. 2) as judged
by their meta- and submetacentric morphology.
This process of microchromosomal transloca-
tion involves two steps: ( I ) The above outlined
process of microchromosomal fusion creating new
small metacentric macrochromosomes. (2) The
translocation of microchromosomes to macro-
chromosomes, not creating new macrochromo-
somes but shifting the centromeric position from
telocentric to submeta- or metacentric in the mac-
rochromosome.
The G- and C-banding patterns of bird chromo-
somes have revealed a surprising identity for the
three or four largest chromosomes. TAKAGI and
SASAKI(1974) showed that there were almost
identical G-banding patterns for the three largest
macrochromosomes in nine different orders, and
other papers have proved the same tendency to-
wards conservation (STOCKet al. 1974; RYITMAN
et al. 1979; RYITMAN and TEGELSTR~M 1981).
Cases of chromosomal fusions in birds have
been reported, supporting our hypothesis. ANSARI
and KAUL(1979) found a microchromosomal addi-
tion to the telocentric chromosome 3. STOCK et al.
(1974) investigated the G-banded karyotype of the
pigeon (Columba livia) and the dove (Streptopelia
risoria). The G-banding patterns of these birds
indicated that the species differences in karyo-
types result from the fusion of four pairs of micro-
chromosomes of the pigeon to form two pairs of
metacentric macrochromosomes in the dove.
There seem to be arguments supporting the idea
that, within a certain order, there is a process of
microchromosomal fusion to macrochromosomes,
especially giving rise to smaller macrochromo-
somes. As indicated above, this tendency to
chromosomal fusion might be connected with the
speciation process and, consequently, rapidly
evolving orders would show this tendency more
than others.
SLIZYNSKI (1964) proposed three hypotheses for
the existence of microchromosomes. He proposed
that, in the meiotic microchromosomes, the
chiasmata are scarce or absent. This probably re-
duces the amount of genetic variation present in a
species. The tendency towards reduction of the
number of microchromosomes in certain species
might reflect an increase in genetic variation
caused by microchromosomal fusion. However,
Hereditas 94 (1981)
we do not know much about the kind of genetic
material in the microchromosomes and it remains
to be proved that fusion of microchromosomes
and increased crossing over between microchro-
mosomal genes increase the amount of genetic
variation in such a way that it is of selective ad-
vantage.
The Falconiformes have been omitted from this
investigation owing to their rather unusual karyo-
types and much wider karyological variation than
in any other avian order. Especially the family
Accipitridae is characterized by an extremely low
number of microchromosomes, the absence of
really large macrochromosomes, the presence of a
high number of medium- to small-sized biarmed
macrochromosomes and a considerably lower
number of subtelocentrics (DE BOER1976).
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