Introduction of the Interactive Atlas of Zebrafish Vascular Anatomy

VESSEL NOMENCLATURE

Prior to our undertaking this work, there were no comprehensive standard references for comparing the vascular anatomy of developing teleost fish to that of other vertebrates. Previous detailed descriptive studies of teleost vascular development were performed almost exclusively using Salmonids (zebrafish are Cyprinids), and were generally limited to particular subportions of the vasculature and/or particular embryonic stages (see Introduction). We also examined a large number of previous reports on the embryonic development of other teleosts (most not cited in this study). However, the fragmentary description of the vascular anatomy in most of these reports, and the fact that names for vessels were often adopted without sufficient consideration having been given to their comparative anatomy, limited their usefulness. In order to conform as much as possible to the nomenclature accepted for vertebrates in general, we have therefore relied extensively on standard, landmark references for the vascular anatomy of other developing vertebrates. These references include those for amphibians (Aoyama, 1956; Grodzinski, 1924; Hartmann, 1922; Hartmann, 1923; Hartmann, 1924; Miki, 1968; Takaoka, 1956; Ura, 1956), reptiles (Furuyama, 1960; Hashimoto, 1960; Kawanishi, 1956; Miura, 1960; Spanner, 1929; Suzuki and Kasai, 1990), birds (Coffin and Poole, 1988; Evans, 1909b; Hiruma and Hirakow, 1995; Inui, 1960; Popoff, 1894), mammals (including humans) (Abe, 1960; Aizawa et al., 1999; Evans, 1912; MacClure and Butler, 1925; Padget, 1948; Padget, 1957; Sabin, 1917; Tada, 1956) and vertebrates in general (Evans, 1909a; Hochstetter, 1906; Rückert and Mollier, 1906; Ura, 1949). We also examined comparative studies of the adult vasculature of fish (Allis, 1912; Aridome, 1959; Bertin, 1958; Harder, 1975; Hochstetter, 1888; Ishida, 1959; von Zwehl, 1961) and vertebrates in general (Gillilan, 1982; Goodrich, 1958; Hafferl, 1967; van Gelderen, 1967) to compare these to the disposition of blood vessels in zebrafish larvae. To the extent that there are limitations to our ability to make definitive assignments of vessel nomenclature, our names may be reconsidered if future studies warrant this (see "Limitations and caveats," below). The designated names and abbreviations of all vessels named in the diagrams in this website are listed here.

LIMITATIONS AND CAVEATS

Although this is the probably the most detailed and comprehensive characterization of the vasculature ever compiled for a developing vertebrate, we must note a few limitations and caveats of our work. First, angiography only visualizes vessels that have formed an open lumen continuous with the rest of the circulation. Angioblast progenitors may be (and often are) in place at substantially earlier stages than this. This should be kept in mind when comparing the expression patterns of vascular-specific molecular markers to the descriptions provided in this paper. In situ hybridization with early vascular-specific markers allows visualization of a developing vessel before it is usually detectable by angiography. Furthermore, it is possible that some "vessels" seen by these molecular methods may never make an appearance by angiography, if they are unused transitory and/or vestigial structures.

Second, we do not provide a detailed description of the precise anatomical positions of different vessels relative to other internal structures and organs. Unlike methods such as serial histological sectioning, our angiography method does not permit direct visualization of non-vascular tissues. We have, however, been able to roughly determine the course of vessels relative to adjacent tissues by preliminary correlation of our data with other, histological data, and are reasonably confident in the identification of major vessels. A more precise determination would require much more extensive characterization of histological specimens and cross-correlation of these specimens with our angiographic data. This sort of analysis will be carried out in the future, however, in collaboration with ongoing efforts in other laboratories to develop a complete histological atlas of the developing zebrafish.

Third, the vascular patterns shown in the angiograms and drawings were derived from particular specimens, and the fine details of these patterns do vary from animal to animal. In the course of our study many different animals were examined at each time point, and the images and drawings are representative of the typical patterns found in most animals. Nevertheless, there is significant variability in exactly when particular vessels (both large and small) come "on-line," both in absolute time and relative to other blood vessels and other tissues. There is also significant variability in the appearance, morphology, and specific connections of smaller caliber vessels, particularly in the head. However, the patterns of interconnections between larger caliber vessels are quite reproducible, and it is these patterns, and how they change over time, that are the major focus of our work. We provide descriptions and names for larger caliber vessels, but not for smaller vessels. It should be noted that in the anatomical descriptions of other vertebrate species most smaller caliber vessels are also either not described, or not given individual names. Therefore, these smaller vessels are in any case less useful for cross-species comparisons.

Fourth, we only examine the first 7 days of development, up to early larval stages. There is no published description of the anatomical details of the vascular system at later stages or in adult zebrafish. Preliminary examination of the adult zebrafish vasculature suggests that most major vessels are approaching their final configurations by 7 dpf, at least in terms of basic wiring. Furthermore, the patterns we observed and the names we assign for vessels in 7 dpf larvae correspond very well to the patterns of vessels in adults of other teleost species (Allis, 1912; Aridome, 1959; Bertin, 1958; Gillilan, 1982; Goodrich, 1958; Harder, 1975; Hochstetter, 1888; von Zwehl, 1961). Nevertheless, in the absence of detailed descriptions for zebrafish stages later than 7 dpf, the possibility remains that subsequent unforeseen changes will necessitate altering the specific names we have adopted here. This could be addressed in future studies, in which we will employ additional non-angiographic methods and examine vessels in later larvae, juveniles, and adults.

Despite the reservations noted above, we believe our designations will be found to correspond to the eventual final adult disposition of the vasculature. The anatomical patterns we have uncovered relate quite well, in general, to those observed in other teleosts and even non-piscene vertebrates. Furthermore, the major plan of the vasculature seems well-established by 2.5 dpf, with a strong similarity to the adult teleost circulatory plan. Undoubtedly numerous additional changes occur after 2.5 dpf, but many of these are likely to be relatively predictable elaborations and modifications of extant primary pathways. Nevertheless, if the results of future studies warrant it we will correct our anatomical names to insure that our classification of the developing zebrafish vascular anatomy remains strictly comparable to that of other vertebrates.

REFERENCES

Abe, H. (1960). Pri la disvolvigo de la angiosistemo de la reno ce hamsteroj- Unu konsidero pri la devno de azygosvejno kaj postkavavejno (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 677-699.
Aizawa, Y., Isogai, S., Izumiyama, M., and Horiguchi, M. (1999). Morphogenesis of the primary arterial trunks of the forelimb in the rat embryos: the trunks originate from the lateral surface of the dorsal aorta independently of the intersegmental arteries. Anat Embryol 200, 573-584.
Allis, E. P. (1912). The pseudobranchial and carotid arteries in esox, salmo and gadus, together with a description of the arteries in the adult amia. Anat. Anz. Bd. 41, 113-142.
Aoyama, M. (1956). Disvolvigo de sangvazoj de la mez- kaj finintesto ce hynobius naevius (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 573-598.
Aridome, M. (1959). A vascular system of the gibel brain. (in Japanese, English summary). Fukuoka Igaku Zasshi 50, 3541-3452.
Bertin, L. (1958). Appareil circulatoire. In "Traité de Zoologi", Vol. 13-2, pp. 1399-1458.
Coffin, J. D., and Poole, T. J. (1988). Embryonic vascular development: immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryos. Development 102, 735-748.
Evans, H. M. (1909a). On the development of the aortae, cardinal and umbilical vein, and the other blood vessels of vertebrate embryos from capillaries. Anat. Record 3, 498-519.
Evans, H. M. (1909b). On the earliest blood vessels in the anterior limb buds of the birds and their relation to the primary subclavian artery. Anat. Rec. 2.
Evans, H. M. (1912). The development of the vascular system. In "Manual of human embryology" (F. Keibel and F. P. Mall, Eds.), Vol. 2.
Furuyama, Z. (1960). Disvolvigo de la angiosistemo de la korpomuro ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 302-330.
Gillilan, L. A. (1982). Blood supply of vertebrate brains. In "Comparative correlative neuroanatomy of the vertebrate telencephalon.", pp. 266-309. Crosby, E. C. Macmillan.
Goodrich, E. S. (1958). "Studies on the structure and development of vertebrates." Dover Publications, New York.
Grodzinski, Z. (1924). Über die Entwicklung der Gefässe des Dotterdarmes bei Urodelen. Bull. Acad. Polon., B. Sci. T. 1.
Hafferl, A. (1967). Das Arteriensystem. In "Bolk’s Handb (Handbuch der vergleichenden Anatomie der Wirbeltiere)", Vol. Bd 6, pp. 563-684. Urban & Schwarzenberg, Berlin.
Harder, W. (1975). The circulatory system. In "Anatomy of Fishes.", pp. 226-264. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart.
Hartmann, A. (1922). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes. Z. Anat. Entwgsch. Bd. 63, 96-117.
Hartmann, A. (1923). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes (II Teil ). Z. Anat. Entwgsch. Bd. 67, 404-456.
Hartmann, A. (1924). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes (III Teil). Z. Anat. Entwgsch. Bd. 70, 260-307.
Hashimoto, N. (1960). Disvolvigo de la angiosistemo de la spinalmedolo ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 331-369.
Hiruma, T., and Hirakow, R. (1995). Formation of the pharyngeal arch arteries in the chick embryos. Observations of corrosion casts by scanning electron microscope. Anat Embryol. 191, 415-423.
Hochstetter, F. (1888). Beiträge zur vergleichenden Anatomie und Entwicklungsgeschichte des Venensystems der Amphibien und Fische. Morph. Jahrb. 13, 119-172.
Hochstetter, F. (1906). Die Entwickelung des Blutgefäßsystems. In "Oskar Hertwig Entwickelungslehre der Wirbeltiere.", Vol. Bd 3, Teil 2, pp. 21-166.
Inui, G. (1960). Pri la disvolvigo de la angiosistemo de la reno ce kokidoj (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 644-676.
Ishida, M. (1959). On the angioarchitecture in the gibel’s brain. (in Japanese, English summary). Fukuoka Igaku Zasshi 50, 4176-4196.
Kawanishi, H. (1956). Disvolvigo de sangvazoj de ovoflavsako ce testudoj, Caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 517-550.
MacClure, C. F. W., and Butler, E. G. (1925). The development of the vena cava inferior in man. Am. J. Anat. 35, 331-383.
Miki, S. (1968). Über die genetische Beziehung der Milz zu den Gefässen des Magens besonders zu seinen sekundären Venen beim Riesensalamander (Megalobatrachus japonicus) (in Japanese, German summary). Kaibogaku Zasshi 38, 140-155.
Miura, S. (1960). Pri la disvolvigo de la angiosistemo de la reno ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 525-557.
Padget, D. H. (1948). The development of the cranial arteries in the human embryo. In "Contributions to Embryology", Vol. 212, pp. 207-261.
Padget, D. H. (1957). The development of the cranial venous system in man, From the viewpoint of comparative anatomy. In "Contributions to Embryology", Vol. 247, pp. 81-140.
Popoff, D. (1894). "Dottersack-gafässe des Huhnes." Kreidl’s Verlag, Wiesbaden.
Rückert, J., and Mollier, S. (1906). Die erste Entstehung der Gefässe und des Blutes bei Wirbeltieren. In "Oskar Hertwigs Entwickelungslehre der Wirbeltiere", Vol. Bnd 1, Teil 2, pp. 1019-1297.
Sabin, F. R. (1917). Origin and development of the primitive vessels of the chick and of the pig. Contrib. Embryol. 6, 61-124.
Spanner, R. (1929). Über die wurzelgebiete der nieren-, nebenmieren und leberpfortader bei reptilien. Morph. Jahrb. 63, 314-358.
Suzuki, T., and Kasai, T. (1990). Development of the subclavian artery in the loggerhead turtle (Caretta caretta) studied by the injection method. Kaibougaku Zasshi 65, 361-373.
Tada, Y. (1956). Disvolvigo de sangvazoj sur la ovoflavsako kaj ankau de la mesintesto ce hamsteroj (Cricetus anuratus) (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 388-417.
Takaoka, K. (1956). Disvolvigo de sangvazoj de pronefro kaj opistonefro hynobius naevius (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 349-376.
Ura, R. (1949). The development of the blood vascular systems. (in Japanese). Nisshin Igaku 33, 130-143.
Ura, R. (1956). Kontribuo al ontogenio de vazsistemo de antauj mmbroj, precipe ce hynobius naevius- Unu provo solvi membroproblemon (in Esperanto). Okajimas Folia. Anat. Jpn. 28, 257-285.
van Gelderen, C. (1967). Venensystem, mit einem Anfang über den Dotter- und Plazentarkreislauf. In "Bolk’s Handb (Handbuch der vergleichenden Anatomie der Wirbeltiere)", Vol. Bd 6, pp. 685-744.
von Zwehl, V. (1961). Uber die Blutgefässversorgung des Gehiruns bei eigen Teleostein. Zool. Zool. Jahrb. Abt. Anat. 79, 371-438.



		VESSEL NOMENCLATURE Prior to our undertaking this work, there were no comprehensive standard references for comparing the vascular anatomy of developing teleost fish to that of other vertebrates. Previous detailed descriptive studies of teleost vascular development were performed almost exclusively using Salmonids (zebrafish are Cyprinids), and were generally limited to particular subportions of the vasculature and/or particular embryonic stages (see Introduction). We also examined a large number of previous reports on the embryonic development of other teleosts (most not cited in this study). However, the fragmentary description of the vascular anatomy in most of these reports, and the fact that names for vessels were often adopted without sufficient consideration having been given to their comparative anatomy, limited their usefulness. In order to conform as much as possible to the nomenclature accepted for vertebrates in general, we have therefore relied extensively on standard, landmark references for the vascular anatomy of other developing vertebrates. These references include those for amphibians (Aoyama, 1956; Grodzinski, 1924; Hartmann, 1922; Hartmann, 1923; Hartmann, 1924; Miki, 1968; Takaoka, 1956; Ura, 1956), reptiles (Furuyama, 1960; Hashimoto, 1960; Kawanishi, 1956; Miura, 1960; Spanner, 1929; Suzuki and Kasai, 1990), birds (Coffin and Poole, 1988; Evans, 1909b; Hiruma and Hirakow, 1995; Inui, 1960; Popoff, 1894), mammals (including humans) (Abe, 1960; Aizawa et al., 1999; Evans, 1912; MacClure and Butler, 1925; Padget, 1948; Padget, 1957; Sabin, 1917; Tada, 1956) and vertebrates in general (Evans, 1909a; Hochstetter, 1906; Rückert and Mollier, 1906; Ura, 1949). We also examined comparative studies of the adult vasculature of fish (Allis, 1912; Aridome, 1959; Bertin, 1958; Harder, 1975; Hochstetter, 1888; Ishida, 1959; von Zwehl, 1961) and vertebrates in general (Gillilan, 1982; Goodrich, 1958; Hafferl, 1967; van Gelderen, 1967) to compare these to the disposition of blood vessels in zebrafish larvae. To the extent that there are limitations to our ability to make definitive assignments of vessel nomenclature, our names may be reconsidered if future studies warrant this (see "Limitations and caveats," below). The designated names and abbreviations of all vessels named in the diagrams in this website are listed here. LIMITATIONS AND CAVEATS Although this is the probably the most detailed and comprehensive characterization of the vasculature ever compiled for a developing vertebrate, we must note a few limitations and caveats of our work. First, angiography only visualizes vessels that have formed an open lumen continuous with the rest of the circulation. Angioblast progenitors may be (and often are) in place at substantially earlier stages than this. This should be kept in mind when comparing the expression patterns of vascular-specific molecular markers to the descriptions provided in this paper. In situ hybridization with early vascular-specific markers allows visualization of a developing vessel before it is usually detectable by angiography. Furthermore, it is possible that some "vessels" seen by these molecular methods may never make an appearance by angiography, if they are unused transitory and/or vestigial structures. Second, we do not provide a detailed description of the precise anatomical positions of different vessels relative to other internal structures and organs. Unlike methods such as serial histological sectioning, our angiography method does not permit direct visualization of non-vascular tissues. We have, however, been able to roughly determine the course of vessels relative to adjacent tissues by preliminary correlation of our data with other, histological data, and are reasonably confident in the identification of major vessels. A more precise determination would require much more extensive characterization of histological specimens and cross-correlation of these specimens with our angiographic data. This sort of analysis will be carried out in the future, however, in collaboration with ongoing efforts in other laboratories to develop a complete histological atlas of the developing zebrafish. Third, the vascular patterns shown in the angiograms and drawings were derived from particular specimens, and the fine details of these patterns do vary from animal to animal. In the course of our study many different animals were examined at each time point, and the images and drawings are representative of the typical patterns found in most animals. Nevertheless, there is significant variability in exactly when particular vessels (both large and small) come "on-line," both in absolute time and relative to other blood vessels and other tissues. There is also significant variability in the appearance, morphology, and specific connections of smaller caliber vessels, particularly in the head. However, the patterns of interconnections between larger caliber vessels are quite reproducible, and it is these patterns, and how they change over time, that are the major focus of our work. We provide descriptions and names for larger caliber vessels, but not for smaller vessels. It should be noted that in the anatomical descriptions of other vertebrate species most smaller caliber vessels are also either not described, or not given individual names. Therefore, these smaller vessels are in any case less useful for cross-species comparisons. Fourth, we only examine the first 7 days of development, up to early larval stages. There is no published description of the anatomical details of the vascular system at later stages or in adult zebrafish. Preliminary examination of the adult zebrafish vasculature suggests that most major vessels are approaching their final configurations by 7 dpf, at least in terms of basic wiring. Furthermore, the patterns we observed and the names we assign for vessels in 7 dpf larvae correspond very well to the patterns of vessels in adults of other teleost species (Allis, 1912; Aridome, 1959; Bertin, 1958; Gillilan, 1982; Goodrich, 1958; Harder, 1975; Hochstetter, 1888; von Zwehl, 1961). Nevertheless, in the absence of detailed descriptions for zebrafish stages later than 7 dpf, the possibility remains that subsequent unforeseen changes will necessitate altering the specific names we have adopted here. This could be addressed in future studies, in which we will employ additional non-angiographic methods and examine vessels in later larvae, juveniles, and adults. Despite the reservations noted above, we believe our designations will be found to correspond to the eventual final adult disposition of the vasculature. The anatomical patterns we have uncovered relate quite well, in general, to those observed in other teleosts and even non-piscene vertebrates. Furthermore, the major plan of the vasculature seems well-established by 2.5 dpf, with a strong similarity to the adult teleost circulatory plan. Undoubtedly numerous additional changes occur after 2.5 dpf, but many of these are likely to be relatively predictable elaborations and modifications of extant primary pathways. Nevertheless, if the results of future studies warrant it we will correct our anatomical names to insure that our classification of the developing zebrafish vascular anatomy remains strictly comparable to that of other vertebrates. REFERENCES Abe, H. (1960). Pri la disvolvigo de la angiosistemo de la reno ce hamsteroj- Unu konsidero pri la devno de azygosvejno kaj postkavavejno (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 677-699. Aizawa, Y., Isogai, S., Izumiyama, M., and Horiguchi, M. (1999). Morphogenesis of the primary arterial trunks of the forelimb in the rat embryos: the trunks originate from the lateral surface of the dorsal aorta independently of the intersegmental arteries. Anat Embryol 200, 573-584. Allis, E. P. (1912). The pseudobranchial and carotid arteries in esox, salmo and gadus, together with a description of the arteries in the adult amia. Anat. Anz. Bd. 41, 113-142. Aoyama, M. (1956). Disvolvigo de sangvazoj de la mez- kaj finintesto ce hynobius naevius (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 573-598. Aridome, M. (1959). A vascular system of the gibel brain. (in Japanese, English summary). Fukuoka Igaku Zasshi 50, 3541-3452. Bertin, L. (1958). Appareil circulatoire. In "Traité de Zoologi", Vol. 13-2, pp. 1399-1458. Coffin, J. D., and Poole, T. J. (1988). Embryonic vascular development: immunohistochemical identification of the origin and subsequent morphogenesis of the major vessel primordia in quail embryos. Development 102, 735-748. Evans, H. M. (1909a). On the development of the aortae, cardinal and umbilical vein, and the other blood vessels of vertebrate embryos from capillaries. Anat. Record 3, 498-519. Evans, H. M. (1909b). On the earliest blood vessels in the anterior limb buds of the birds and their relation to the primary subclavian artery. Anat. Rec. 2. Evans, H. M. (1912). The development of the vascular system. In "Manual of human embryology" (F. Keibel and F. P. Mall, Eds.), Vol. 2. Furuyama, Z. (1960). Disvolvigo de la angiosistemo de la korpomuro ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 302-330. Gillilan, L. A. (1982). Blood supply of vertebrate brains. In "Comparative correlative neuroanatomy of the vertebrate telencephalon.", pp. 266-309. Crosby, E. C. Macmillan. Goodrich, E. S. (1958). "Studies on the structure and development of vertebrates." Dover Publications, New York. Grodzinski, Z. (1924). Über die Entwicklung der Gefässe des Dotterdarmes bei Urodelen. Bull. Acad. Polon., B. Sci. T. 1. Hafferl, A. (1967). Das Arteriensystem. In "Bolk’s Handb (Handbuch der vergleichenden Anatomie der Wirbeltiere)", Vol. Bd 6, pp. 563-684. Urban & Schwarzenberg, Berlin. Harder, W. (1975). The circulatory system. In "Anatomy of Fishes.", pp. 226-264. E. Schweizerbart’sche Verlagsbuchhandlung, Stuttgart. Hartmann, A. (1922). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes. Z. Anat. Entwgsch. Bd. 63, 96-117. Hartmann, A. (1923). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes (II Teil ). Z. Anat. Entwgsch. Bd. 67, 404-456. Hartmann, A. (1924). Die Entstehung der ersten Gefässbahnen bei Embryonen urodeler Amphibien (Salamandra atra und Axolotl) bis zur Rückbildung des Dotterkreislaufes (III Teil). Z. Anat. Entwgsch. Bd. 70, 260-307. Hashimoto, N. (1960). Disvolvigo de la angiosistemo de la spinalmedolo ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 331-369. Hiruma, T., and Hirakow, R. (1995). Formation of the pharyngeal arch arteries in the chick embryos. Observations of corrosion casts by scanning electron microscope. Anat Embryol. 191, 415-423. Hochstetter, F. (1888). Beiträge zur vergleichenden Anatomie und Entwicklungsgeschichte des Venensystems der Amphibien und Fische. Morph. Jahrb. 13, 119-172. Hochstetter, F. (1906). Die Entwickelung des Blutgefäßsystems. In "Oskar Hertwig Entwickelungslehre der Wirbeltiere.", Vol. Bd 3, Teil 2, pp. 21-166. Inui, G. (1960). Pri la disvolvigo de la angiosistemo de la reno ce kokidoj (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 644-676. Ishida, M. (1959). On the angioarchitecture in the gibel’s brain. (in Japanese, English summary). Fukuoka Igaku Zasshi 50, 4176-4196. Kawanishi, H. (1956). Disvolvigo de sangvazoj de ovoflavsako ce testudoj, Caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 517-550. MacClure, C. F. W., and Butler, E. G. (1925). The development of the vena cava inferior in man. Am. J. Anat. 35, 331-383. Miki, S. (1968). Über die genetische Beziehung der Milz zu den Gefässen des Magens besonders zu seinen sekundären Venen beim Riesensalamander (Megalobatrachus japonicus) (in Japanese, German summary). Kaibogaku Zasshi 38, 140-155. Miura, S. (1960). Pri la disvolvigo de la angiosistemo de la reno ce caretta olivacea (in Japanese, Esperanto summary). Kaibogaku Zasshi 35, 525-557. Padget, D. H. (1948). The development of the cranial arteries in the human embryo. In "Contributions to Embryology", Vol. 212, pp. 207-261. Padget, D. H. (1957). The development of the cranial venous system in man, From the viewpoint of comparative anatomy. In "Contributions to Embryology", Vol. 247, pp. 81-140. Popoff, D. (1894). "Dottersack-gafässe des Huhnes." Kreidl’s Verlag, Wiesbaden. Rückert, J., and Mollier, S. (1906). Die erste Entstehung der Gefässe und des Blutes bei Wirbeltieren. In "Oskar Hertwigs Entwickelungslehre der Wirbeltiere", Vol. Bnd 1, Teil 2, pp. 1019-1297. Sabin, F. R. (1917). Origin and development of the primitive vessels of the chick and of the pig. Contrib. Embryol. 6, 61-124. Spanner, R. (1929). Über die wurzelgebiete der nieren-, nebenmieren und leberpfortader bei reptilien. Morph. Jahrb. 63, 314-358. Suzuki, T., and Kasai, T. (1990). Development of the subclavian artery in the loggerhead turtle (Caretta caretta) studied by the injection method. Kaibougaku Zasshi 65, 361-373. Tada, Y. (1956). Disvolvigo de sangvazoj sur la ovoflavsako kaj ankau de la mesintesto ce hamsteroj (Cricetus anuratus) (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 388-417. Takaoka, K. (1956). Disvolvigo de sangvazoj de pronefro kaj opistonefro hynobius naevius (in Japanese, Esperanto summary). Kaibogaku Zasshi 31, 349-376. Ura, R. (1949). The development of the blood vascular systems. (in Japanese). Nisshin Igaku 33, 130-143. Ura, R. (1956). Kontribuo al ontogenio de vazsistemo de antauj mmbroj, precipe ce hynobius naevius- Unu provo solvi membroproblemon (in Esperanto). Okajimas Folia. Anat. Jpn. 28, 257-285. van Gelderen, C. (1967). Venensystem, mit einem Anfang über den Dotter- und Plazentarkreislauf. In "Bolk’s Handb (Handbuch der vergleichenden Anatomie der Wirbeltiere)", Vol. Bd 6, pp. 685-744. von Zwehl, V. (1961). Uber die Blutgefässversorgung des Gehiruns bei eigen Teleostein. Zool. Zool. Jahrb. Abt. Anat. 79, 371-438.