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Study of the ossification centers and skeletal development of pelvic limb in quail after hatching.

Introduction

Skeletal development in birds has always been a subject under attention. The first studies that were about bone histogenesis were done by Brachet [4] but it was done thoroughly in before and after hatching time [9, 31].

Leg skeleton in birds, because pentadactyl limb, compared to wing skeleton, has been considerably under less attention and probably because of that the information about natural development of the skeleton is rare.

The mentionable exception is Johnson's study about leg formation in chicken that the primary stages of skeletal development are described thoroughly but the stages after that are ignored [13].

Most investigations about embryonic development of leg in birds are about chickens, except for some on zebra parakeet, ostrich, duck, and larus [5, 29, 32].

Many studies are done on chicken with special aspects of leg skeletal development, like knee joint development [24, 25] or development of a certain bone, for example tibiotarsus or tarsometatarsus [9, 28], with only a now-and-then mentioning of other parts of the skeletal system.

Many different investigations are done about the ossification centers in embryonic period that are about all mesenchymal, cartilaginous and ossification stages [14, 27].

Also the natural growth of leg skeleton in quail embryo from the primary mesenchymal changes to last stages of embryonic period are investigated thoroughly [20].

Most of the studies are about the embryonic period and the best studies about hatching and after hatching are mostly done on gallus domesticus [18].

There is no citable study until now about the ossification centers in quail (coturnix c. japonica) after hatching and this investigation studies the ossification centers in quail after hatching for the first time.

Materials and Methods

This study is done on quail after hatching. Fourteen quail (coturnix c. japonica) were kept from day one under the same conditions and were reared under the standard conditions related to food, temperature, humidity and light.

The main techniques employed are processing the radiographic stereotype with normal radiography film. The radiography machine was Dean 44 X-Ray machine, KV 40-110 and mas 0.1-200 (depending on the size of the specimens) and focal-film distance 100 cm. For radiography the lateral and ventrodorsal position were used. Preparing the radiographs was on the specified times which means radiography was done twice on the first week (first and seventh days) and then once at the end of second, third, fourth, fifth, sixth, seventh, eighth, and ninth week and after the ninth week until the full maturity stage and completion of skeletogenesis radiography of specimens was done every two weeks.

In this study all the birds were sampled from hatching until 91 days.

Results:

Ossification time of pelvic girdle:

Ilium, ischium, pubis:

These bones were cartilaginous until the end of the second week and after day 21 it was observed as a bone in all specimens (Figure 1). The ossification starting time of pelvic girdle bones are shown in table 1.

Ossification time of pelvic limb bones:

Head of femur:

It was not observed in any of the specimens until day 49. It was observed in day 56 in 65% and in day 63 in more than 90% and after day 70 in all specimens.

Trochanter of femur:

It was not observed in any of the specimens until day 14. It was observed in day 21 in 70% and in day 28 in more than 90% and after day 35 in all specimens.

Femur:

On the first day after hatching this bone was not observed in any specimen because it was cartilaginous and was observed in all specimens after day seven.

Patella:

It was not observed in any of the specimens until day 28. It was observed in day 35 in 85% and in day 42 in all specimens (Figure 2).

Condyle of femur:

It was not observed in any of the specimens until day 14. It was observed in day 21 in 70% and in day 28 in more than 90% and after day 35 in all specimens.

Fibula:

It was not observed in any of the specimens until day 14. It was observed in day 21 in 80% and in day 28 in all specimens (Figure 3).

Tibiotarsal bone:

On the first day after hatching this bone was not observed in any specimen because it was cartilaginous and was observed in all specimens after day seven.

Condyle of tibiatarsal bone:

It was not observed in any of the specimens until day 7. It was observed in day 14 in 70% and in day 21 in more than 90% and after day 28 in all specimens.

Hypotarsal crest of tarsometatarsal bone:

It was not observed in any of the specimens until day 56. It was observed in day 63 in 75% and in day 70 in 90% and after day 77 in all specimens.

Trochlea of tarsometatarsal bone, Digit I, Digit II, Digit III, Digit IV, Metatarsal I:

On the first day after hatching this bone was not observed in any specimen because it was cartilaginous and was observed in all specimens after day seven. Ossification times of leg skeleton bones are shown in table 2.

Discussion

In this study we try to compare leg skeletal development in quail after hatching with the pre-hatching time and more specifically with gallus domesticus after hatching because the information about the natural development of leg skeleton in chick is vast.

Although the changes happen at different times for the mesenchymal density of bone marrow, primary cartilage, and ossification in large elements, it is clearly observed that the development of the skeleton in quail and chick are very similar and this can mean that quail and chick are classified under the galliformes class [30].

Mesenchymal density and first stages of cartilage development in femur, tibia, and fibula diaphysis in day one is completely observable.

In chicken, the femur, as the strongest element in primary leg skeleton in chondrogenesis period is explained, although its development rate is lower than development rate of tibia.

Nonetheless, in quail the tibia is not only the strongest element but its development rate is also higher even in cartilaginous stage.

In addition, fibula in chick has more chondrogenesis speed compared to tibia [10], yet, in quail the development rate of fibula is lower than tibia.

In past studies, it is mentioned that fibula is considerably thinner than tibia in cross section.

And by the increase in ossification process the distal end gets thinner than the proximal end. It seems impossible that fibula can always have higher rate of development compared to tibia in chick [25].

It seems that patella ossifies a little earlier in quail than chicken and after day 35, whereas in chicken the ossification is observed after day 63 in it [18] but like quail, chicken patella is not also ossified after hatching, and until the time it is in late incubation period only a weak cartilage is observed in it [25].

The metatarsus development in quail is like of chick in many ways, except for the metatarsus I turn to posterior position that happens later in quail.

Fujioko says that the center of ossification in digits I, II, and III seems to be in a proximal-distal sequence, but the sequence of ossification in phalanges in digit IV is 1, 4, 5, 2, and 3 [12].

The same sequence of ossification is seen in quail although the ossification in digit IV is 1, 5, 2, 3, and 4 in quail.

The existence of two rows of ossification centers in tarsus joint region in birds (hock joint) is completely obvious which is fused with tibia from proximal extremity and to big metatarsus from distal extremity (Figure 4).

Previous researchers have put forth this theory about bones in tarsus region, too. [22]. At last we can say that in tarsus area the bones adjacent to long bones are fused and are usually called tibiotarsus and tarsometatarsus. When we relate these expressions to them no justification about the secondary ossification centers in tarsus area mentioned in previous studies is acceptable [7, 11].

This study confirms the general idea about the existence of two centers at proximal row and one center in distal row in tarsus and is equal with Hogg's study on gallus domesticus [18] but contradicts with Franceschini that declared the existence of three centers [11].

It seems that the proximal center of tibia is the only secondary and real center of ossification in long bones that probably exists in all birds (Figure 5). This center was ossified in all specimens on day 56 and just in one specimen on day 70 after hatching (Figure 6). If this center causes the increase in the size of bone that is a growth plate (Epiphyseal plate) and maybe it is a traction epiphysis.

Some researchers claim that the secondary centers only exist in mammals, lizards and in the avian tibia and chartilage canal in mammals are usually related to the subsequent developments of the secondary centers as in lizards [17].

cartilage canals are in epiphysis area of bird bone and are described by Haines. The first have more secondary centers and may destroy during the bone pneumatisation and invasion of air bags inside the bone. Pneumatisation in long bones increases hence there is an unusual relation between species of birds. Although the existence if a center in proximal extremity of tibia is completely obvious, little attention is paid to it.

Parsons believed that they belong to the group of traction epiphyses and he has applied the term to them. He suggested that these represented preexisting sesamoid bones [26].

Some researchers have disagreed with this expression and have called them the inter tendon centers and by ossification progress, the cartilage epiphysis area is placed inside tendon and they also believed that these should be differentiated with the sesamoids [18, 19].

In some studies Parson's theory is supported since it was proved that in some birds there may not be a patella and it may be fused with tibia bone. Although in this study the existence of patella is completely obvious.

According to previous findings the tibia is separate so it is more similar to a sesamoid bone.

Probably the proximal center of tibia shows the preformed joint of sesamoid to tibia and in addition is a tool to reinforce the joint of quadriceps femoris muscle, too.

Some of these forms, like the longer length of crus bones from proximal elements and specificity of tarsus region, in which the proximal elements are intensely bond to crus (tibia and fibula), can be an adaption to running and locomotion with two legs.

In birds, in a separate line of pseudosuchian, because of the running habit a similar essential mechanism has made a structure called tibiotarsus (fusing of proximal tarsal row to distal extremity of tibia) that this tibiotarsus is one of the specific characteristics of the bird class skeleton.

Conclusion:

By comparison of leg development in quail (coturnix c. japonica) and chicken, it is obvious that the skeleton elements in both birds are very similar in one sequence although the development in the chicken is longer than in the quail.

In this study the existence of epiphyseal plate at the proximal extremity of tibia was doubtful that maybe causes the increase in the size of the diaphysis in all specimens or it was the secondary center of ossification that cause the traction epiphysis.

Maybe the best time to say that all the pelvic limb elements are totally formed and ossified is the 70th day after hatching (Figure 7).

The final form of the body is very similar in both birds.

Thus, according to the observations of the development of pelvic limb, it seems that quail (coturnix c. japonica) is also categorized under the galliformes class like chicken.

References

[1.] Barnerr, C.H., O.J. Lewis, 1958. The evolution of some traction epiphyses in birds and mammals. Journal of Anatomy, 92(4): 593-601.

[2.] Baumel, J.J., 1980. Osteologia ln Nomina Anatomica Avium (ed. J. J. Baumel, A. S. King, A. M. Lucas, J. Breazile & H. E. Evans). New York and London Academic Press.

[3.] Bellaairs, A.D'A., C.R. Jenkin, 1960. The skeleton of birds. In Biology and Comparative Physiology of Birds, vol. 1 (ed. A. J. Marshall). New York and London Academic Press, pp: 241-300.

[4.] Brachet, A., 1893. Etudes sur la resorption du cartilage et le developpement des os longs chez lesoiseaux. Internationale Monatsschrift ffr Anatomie and Physiologie, 10: 391-417.

[5.] Broom, R., 1906. On the early development of the appendicular skeleton of the ostrich, with remarks on the origin of birds. Trans. S. Afr. phil. Soc, 16: 355-368.

[6.] Chamberlain, F.W., 1943. Atlas of Avian Anatomy. Michigan State College.

[7.] Church, L.E., L.C. Johnson, 1964. Growth of long bones in the chicken. Rates of growth in length and diameter of the humerus, tibia and metatarsus. American Journal of Anatomy, 114(3): 521-538.

[8.] Dawson, A.B., 1926. A note on staining of the skeleton of cleaned specimens in alizarin red S. Stain Technol, 1: 123-124.

[9.] Fell, H.B., 1925. The histogenesis of cartilage and bone in the long bones of the embryonic fowl. Journal of Morphology and Physiology, 40(3): 417-459.

[10.] Fell, H.B., R.G. Canti, 1934. Experiments on the development in vitro of the avian knee joint. Proc. R. Soc, B, 116: 316-349.

[11.] Franceschi, M.P, 1967. On the appearance and evolution of secondary ossification centersin the tibia of Gallus gallus (Linn.). Acta anatomica, 68: 169-188.

[12.] Fujioka, T., 1955. Time and order of appearance of ossification centers in the chicken skeleton. Acta anatomica nipponica, 30: 140-150.

[13.] Johnson, A., 1883. On the development of the pelvic girdle and skeleton of the hind limb in the chick. Q. JI microsc, Sci., 23: 399-411.

[14.] Hamilton, H.L., 1952. Lillie's Development of the Chick, 3rd ed. New York: Henry Holt & Co.HERRICK, E. H. & HERRICK, E. M. (1956). Rib abnormalities in fowls. Poultry Science, 35: 191-194.

[15.] Hines, R.W., 1942. The evolution of epiphyses and of endochondral bone. Biological Reviews of the Cambridge Philisophical Society, 17: 267290.

[16.] Hines, R.W., 1940. Note on the independence of sesamoid and epiphyseal centers of ossification. Journal of Anatomy, 75: 101-105.

[17.] Hines, R.W., 1938. Primitive form of epiphysis in long bones of tetrapods. Journal of Anatomy, 72: 323-343.

[18.] Hogg, D.a., 1980. A re-investigation of the centers of ossification in the avian skeleton at and after hatching. Journal of Anatomy, 130(4): 725-743.

[19.] Hogg, D.A., 1978. The articulations of the neurocranium in the postnatal skeleton of the domestic fowl (Gallua gallus domesticus). Journal of Anatomy, 127: 53-63.

[20.] Lansdown, A.B.G., 1970. A study of the normal development of the leg skeleton in the quail (Coturnix coturnix japonica). Journal of Anatomy, 106(1): 147-160.

[21.] Montagna, W., 1945. Areinvestigation of the development of the wing of the fowl. Journal of Morphology, 76: 87-113.

[22.] MORSE, E.S., 1874. On the tarsus and capus of birds. Ann. Lyc. nat. Hist, N.Y., 10: 141-158.

[23.] Nagaviri, S.S., P.N. Dubey, 1975. Epiphysis at the lower end of chick tibia. Journal of Anatomical Society of India, 24: 35.

[24.] Nivnn, J.S.F., 1933. The development in vivo and in vitro of the avian patella. Wilhelm Roux Arch. Entw Mech. Org, 8: 480-501.

[25.] O'Rahilly, R., E. Gardener, 1956. The development of the knee joint of the chick and its correlation with embryonic staging. Journal of Morphology, 98: 49-88.

[26.] Parsons, F.G., 1904. Observations on traction epiphyses. Journal of Anatomy and Physiology, 38: 248-258.

[27.] Romanoff, A.L., 1960. The Avian Embryo. New York: Macmillan.

[28.] Schryver, H.F., 1967. A quantitative comparison of the growth of the embryonic chick tibiotarsus in vivo and in vitro. J. exp. Zool., 161: 81-88.

[29.] Sieglbaur, F., 1911. Zur Entwicklung. der Vogelextremitait. Z. wiss. Zool., 97: 262-313.

[30.] Wetmore, A., 1951. A revised classification of birds of the world. Smithson. misc. Collns, 117(4): 1-22.

[31.] Wolbach, S.B., D.M. Hegsted, 1952. Endochondral bone growth in the chick. American Medical Association Archives o Pathology, 54(1): 1-12.

[32.] Zehnter, L., 1890. Beitrage zur Entwicklung von Cypselus melba. Arch. Naturgesch, 56: 189-220.

(1) Behrooz Yahyaei, (1) Hassan Gilanpour, (2) Abbas Veshkini

(1) Department of Anatomical Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran.

(2) Department of Clinical Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran.

Corresponding Author

Behrooz Yahyaei, Department of Anatomical Sciences, Science and Research Branch, Islamic Azad University, Tehran, Iran.

Table 1: Time of pelvic girdle ossifying.

          Days after hatching

Bone      1   7   14   21   28   35   42

Ilium                  +    +    +    +
Ischium   -   -   -    +    +    +    +
Pubis     -   -   -    +    +    +    +

          Days after hatching

Bone      49   56   63   70   77   84   91

Ilium     +    +    +    +    +    +    +
Ischium   +    +    +    +    +    +    +
Pubis     +    +    +    +    +    +    +

Table 2: Time of leg skeleton ossifying.

Bone                               Days after hatching

                              1   7   14    21    28   35   42

Head of Femur
Trochanter of Femur                         -+    -+   +    +
Femur                         -   +   +     +     +    +    +
Patella                       -   -   -     -     -    +    +
Condyle of Femur                            - +   -+   +    +
Fibula                        -   -   - +   +     +    +    +
Tibiotarsal bone              -   +   +     +     +    +    +
Condyle of tibiatarsal bone   -   -   -+    -+    +    +    +
Hypotarsal crest of
  tarsometatarsal bone
Tarsometatarsal bone          -   +   +     +     +    +    +
Trochlea of tarsometatarsal   -   +   +     +     +    +    +
  bone
Digit I                       -   +   +     +     +    +    +
Digit II                      -   +   +     +     +    +    +
Digit III                     -   +   +     +     +    +    +
Digit IV                      -   +   +     +     +    +    +
Phalanges                     -   +   +     +     +    +    +
Metatarsal I                  -   +   +     +     +    +    +

Bone                                Days after hatching

                              49   56   63   70   77   84   91

Head of Femur                      -+   +    +    +    +    +
Trochanter of Femur           +    +    +    +    +    +    +
Femur                         +    +    +    +    +    +    +
Patella                       +    +    +    +    +    +    +
Condyle of Femur              +    +    +    +    +    +    +
Fibula                        +    +    +    +    +    +    +
Tibiotarsal bone              +    +    +    +    +    +    +
Condyle of tibiatarsal bone   +    +    +    +    +    +    +
Hypotarsal crest of                     -+   +    +    +    +
  tarsometatarsal bone
Tarsometatarsal bone          +    +    +    +    +    +    +
Trochlea of tarsometatarsal   +    +    +    +    +    +    +
  bone
Digit I                       +    +    +    +    +    +    +
Digit II                      +    +    +    +    +    +    +
Digit III                     +    +    +    +    +    +    +
Digit IV                      +    +    +    +    +    +    +
Phalanges                     +    +    +    +    +    +    +
Metatarsal I                  +    +    +    +    +    +    +
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Title Annotation:Original Article
Author:Yahyaei, Behrooz; Gilanpour, Hassan; Veshkini, Abbas
Publication:Advances in Environmental Biology
Article Type:Report
Date:Sep 1, 2013
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