The present paper is the result of an attempt to collect together and give an account of the literature of the formation of the corpus luteum, during the last ten years, that is, since the publication of Sobotta’s first paper on the corpus luteum of the mouse.

Of the three original hypotheses put forward to explain the mode of formation of the corpus luteum, and the origin of the lutein cells, that of Paterson, who regarded the structure as derived from the blood coagulum left in the cavity of the Graafian follicle after its discharge, gained few or no adherents among subsequent investigators. The other two theories, those of von Baer and Bischoff, on the other hand, have each received a considerable amount of support. Von Baer supposed the corpus luteum to be a connective-tissue structure, in the formation of which the membrana granulosa or follicular epithelium had no share; while Bischoff concluded that the lutein cells were formed by the hypertrophy of the epithelial cells of the undischarged follicle. Among the principal supporters of von Baer’s view appear the names of Leuckart, His, Kolliker, Slavjansky, Gegenbaur, Beuckiser, Schottlander, and Minot. Those who have adopted the alternative theory of Bischoff include Pflüger, Waldeyer, Call and Exner, Beigel, and Schulin.

The first really systematic effort to deal with the question was made by Sobotta, whose earliest paper on the subject was published in the ‘Anatomischer Anzeiger’ in 1895. In the following year the complete paper was issued. These papers describe an investigation on the development of the corpus luteum in the mouse, in which a large series of stages was examined, each of them being collected according to a definite plan, the animals being killed at known intervals after the occurrence of coition, in reference to which the period of ovulation had been previously determined. Sobotta’s investigation resulted in confirming Bischoff’s view that the lutein cells are the much hypertrophied epithelial cells of the undischarged follicle, the connective-tissue element which forms an anastomosis among the lutein cells being derived from the inner layer of the theca. The theca externa is described as taking no share in the ingrowth, while the theca interna is stated to become entirely used up in the formation of the interepithelial network. The hypertrophy of the epithelial cells is described as being of the nature of a simple enlargement, unaccompanied by cell division. The cavity of the follicle is said to become eventually filled up by a central plug of connective tissue.

The conclusions reached by Sobotta regarding the formation of the corpus luteum were subsequently corroborated by him in an investigation on the corpus luteum of the rabbit, the stages of development being also obtained by killing the animals at stated intervals after coition.

In 1898 Stratz published descriptions of stages in the formation of the corpus luteum of Tarsius, Tupaia, and Sorex; and these agree in all essential particulars with the accounts given by Sobotta.

The development of the rabbit’s corpus luteum was also studied by Honoré, who adopted the same method as that employed by Sobotta. According to Honoré the interepithelial proliferation of connective tissue is derived in part from the theca externa, and not exclusively from the inner theca, as supposed by Sobotta ; while the theca interna is stated to be not entirely exhausted by the ingrowth, some part remaining to form a layer within the outer theca, after the full formation of the corpus luteum.

Kreis’s observations on the young human corpus luteum likewise support the hypothesis put forward by Bischoff.

Belloy, who investigated the formation of the corpus luteum in the rat and guinea-pig, while regarding the lutein cells as being derived from the follicular epithelium, describes an active proliferation of these cells soon after the follicle’s rupture. No figures are given by Belloy, and it seems possible that he has confused the ingrowing cells of connective tissue from the theca interna with the membrana granulosa cells. Bouin, who also investigated the corpus luteum of the ra.t and guinea-pig, reached conclusions similar to those of Belloy.

Heape, without entering into a discussion on the origin of the lutein cells, lays some stress on the absence of division among these cells in the ovaries of certain monkeys, pointing out that the enlargement is the result of a simple hypertrophy.

Rabi, writing especially on the human corpus luteum, concludes that the lutein cells have a double origin, arising both from the membrana granulosa and from the theca interna.

A number of investigators, on the other hand, since the publication of Sobotta’s work, have adopted the theory originally put forward by von Baer, that the lutein cells arise from the connective-tissue wall, the follicular epithelium being either completely discharged along with the ovum and the greater part of the liquor folliculi, or else being partially discharged and partially degenerating in situ. Among those holding this view are His, Kólliker, and Paladino, who have lately reiterated their former opinions.

Von Baer’s theory has also received considerable support in recent years from Nagel, who has described the corpus luteum in the human subject as an entirely connective-tissue structure. In this he has been followed by Clark, who worked on the formation of the corpus luteum in the sow and in the human female, and claimed that the result of his investigation had put the matter almost beyond question. Clark’s account has been confirmed by Doering, who also worked upon the sow’s corpus luteum. Others who have adopted the view that the lntein cells have a connective-tissue origin are Bühler, Wendeler, and Stöckel, who have examined and described developing human corpora lutea.

None of these investigators, however, appear to have given an account of the growing corpus luteum in all stages of development, while in the case of several of the accounts, it is not clear that the structures described were not in reality atretic follicles, that is to say, follicles which had undergone degenerative changes without discharging their ova. On the other hand, the words used in a description by Clark point to the conclusion that this author was dealing with the degenerate epithelial cells of an atretic follicle. It seems not improbable that the young human “corpus luteum “which Doering describes was also an undischarged atretic follicle; while Kôlliker’s opinion that the corpus luteum is a connectivetissue structure appears to be founded on the assumption that the changes undergone by discharged follicles and retrogressive undischarged or atretic follicles are identical in character. His, and also Bühler, with reference especially to Sobotta’s work on the mouse, have remarked that it can scarcely be an accidental circumstance that the accounts given of the development of the corpus luteum in the larger animals and in man are radically different from those described for the smaller species. That the discrepancy between the accounts of various investigators depends upon the size of the animals employed does not seem, on the face of it, a very probable suggestion. It is to be noted further that in the investigations of all these writers who have upheld the connective-tissue theory the ages of the developing corpora lutea were unknown, the material in no case being obtained by Sobotta’s method of killing the animals at definite intervals after coition.

In 1901 the present writer published a preliminary account of an experimental inquiry upon the formation of the corpus luteum in the sheep. In this inquiry the sheep were killed at stated periods either after coition or after the animals had been observed to undergo œstrus. The relation which was found to exist between the condition of development of the corpus luteum and the length of the interval that was allowed to elapse between œstrus and the killing of the animal, was in itself a strong presumption that ovulation in the sheep occurs normally during œstrus. Thus the approximate age of the young corpus luteum or discharged follicle could in every case be determined. The result of this investigation was to confirm in all essential particulars Bischoff’s theory, which had been accepted by Sobotta. The sheep, however, was found to present some differences from the mouse in regard to the mode of formation of the corpus luteum, the connective tissue ingrowth being derived partly from the theca externa, and not merely from the theca interna, and the follicular epithelium continuing to undergo division after the rupture of the follicle, but with greatly decreased frequency. The former of these two observations is in agreement with Honoré’s statement in regard to the interepithelial connective tissue in the rabbit. The theca interna was said to become entirely used up in the formation of the connective-tissue ingrowth, this statement agreeing with Sobotta’s description, but differing from that of Honoré. Two years later the complete account of the development of the corpus luteum in the sheep was published.

The description given in these papers is thus completely opposed to His’s suggestion that the mode of formation of the corpus luteum in the larger mammals is different from what it is in small animals like the mouse and rabbit, unless, as Sobotta remarks, it was intended to include only the elephant and the whale in the former category.

Meanwhile, in 1901, the same year in which the preliminary account referred to above was issued, van der Stricht published descriptions of the developing corpus luteum of bats belonging to the genera Vesperugo, Vespertilio, and Placotus. This author’s researches also resulted in confirming Bischoff’s hypothesis, but he differs from others who hold this view in stating that a certain relatively small number of lutein cells arise from interstitial cells existing in the inner theca of the connective-tissue sheath. Van der Stricht differs from Sobotta, while agreeing with the present writer in finding mitotic division among the follicular epithelial cells after the follicle’s rupture. A figure is given in one of van der Stricht’s papers of a section of a human ovary in which such division is also shown to exist. It would thus appear that the lutein cells, at any rate, in certain mammals, do not arise entirely by simple hypertrophy of the follicular epithelial cells, but by hypertrophy accompanied by a greater or less amount of cell division. The very early appearance of fatty particles in these cells in the bat’s discharged follicle is a point of considerable interest to which van der Stricht calls attention.

At the meeting of the “Anatomische Gesellschaft “at Bonn, Kopsch exhibited sections of corpora lutea from the sow, representing three-, six-, and ten-day stages of development. These preparations in a general way supported the follicular epithelia] theory.1

Sobotta’s account of the formation of the corpus luteum in the rabbit has been recently further confirmed by Cohn, who also obtained a series of stages by killing the rabbits at stated periods after copulation. Thus the development of the rabbit’s corpus luteum has formed the subject of experimental investigations by three separate observers—Sobotta, Honoré, and Cohn,—who have all arrived at the conclusion that the lutein cells are hypertrophied follicular epithelial cells.

An important paper on the corpus luteum of the “Marsupial cat,” Dasyurus viverrinus, by Sandes shows that this structure is formed in a similar way in marsupials to what it is in the Eutheria. The theca interna folliculi is shown to be rudimentary in Dasyurus. Owing to this circumstance Sandes points out that it is easier to follow the subsequent changes undergone by this layer during the formation of the corpus luteum than in certain of the other mammals. Bühler had suggested that Sobotta might have confused the cells of the theca interna during an early stage of ingrowth with those belonging to the follicular epithelium, which they undoubtedly at one period resemble, saying that the latter author had not properly described the connective tissue sprouting into the cavity of the newly-discharged follicle. Sandes’s description is of value as showing that Bühler’s criticism loses all force when applied to Dasyurus, with which the membrana granulosa undergoes so considerable a hypertrophy prior to the thecal ingrowth as to sometimes almost fill the cavity of the follicle, and thus all possibility of a confusion between epithelial and connective-tissue cells is precluded.

Sandes describes also the fate of those follicles which do not rupture in Dasyurus. In the case of the smaller follicles both follicular epithelium and ovum frequently degenerate, but the former may persist as a single layer of cuboidal epithelium. Sometimes a metaplasia of epithelial cells into spindle- or star-shaped cells is said to take place, as in other animals. In this way the cavity of the follicle becomes filled up, oi’ it may be obliterated by the ingrowth of connective tissue. Other atretic follicles may for a time remain cystic, with a layer of cuboidal epithelial cells, which eventually disappear. Follicles which have become ripe, or almost ripe, however, are stated to pass through changes precisely similar to those undergone by corpora lutea, except that the ovum, instead of being extruded, degenerates in situ, becoming invaded by leucocytes and by connective tissue.

The corpus luteum in the marmot (Spermophilus citillus) has been shown by Völker to be formed in essentially the same way as that of the mouse, the rabbit, and the sheep. It resembles that of the sheep and (according to Honoré’s description) that of the rabbit, in the fact that the thecal ingrowth is not merely confined to strands of tissue arising from the inner layer. It also resembles the rabbit’s corpus luteum (according to Honoré) in that the theca interna need not become entirely spent in the formation of the interepithelial connective tissue. Volker finds also in unruptured atretic follicles lutein cells which are similar to those of discharged follicles.

Two authors who have recently written on the formation of the corpus luteum reject Bischoff’s theory, on what substantial grounds I find it difficult to understand. Of these, Jankowsky bases his opinions on the study of a miscellaneous collection of material obtained mostly from the sow, but without any attempt at systematic investigation. The few figures which this author gives do not seem to me in any way opposed to the follicular epithelial theory, while the figure of the developing corpus luteum from the guinea-pig appears rather to support the hypothesis that the hypertrophied cells arise from the membrana granulosa, and the anastomosis between those cells from the tissue of the theca. Jankowsky’s view is largely based on the appearance of “lutein cells “in the theca interna prior to the rupture of the follicle.

Williams, in a recent work on obstetrics, takes up the same position as Jankowsky, partly on the ground that “the membrana granulosa presents extensive degenerative changes, and is usually cast off in great part at the time of rupture,” and partly because the cells of the theca interna undergo marked changes during the follicle’s development, and eventually come to resemble lutein cells. The former statement, indeed, is very far from being proved, while the latter appears to me to be singularly inconclusive. Williams argues also that the degenerative changes which have been observed in the epithelium of atretic follicles afford evidence that similar changes occur in discharged follicles. “Observations based upon the study of several hundred human1 corpora lutea have convinced me that the connective tissue origin of the lutein cells is established beyond all reasonable doubt.” Williams, however, does not say that these specimens have been described in any published paper, and, in the absence of the evidence, I am unable to regard his opinion as in any way conclusive.

The changes undergone by the discharged follicle have also been studied in various lower vertebrates. Bühler, who investigated the ovaries of Cyclostomes and certain Teleosteans, was unable to find any hypertrophy of the follicular wall, and Cunningham arrived at a similar conclusion for the spent follicles of Teleosteans. The present writer has examined the discharged follicle of the common fowl without being able to detect any hypertrophy of the follicular epithelium. On the other hand, Mingazzini has discovered such hypertrophy in certain reptiles, structures resembling mammalian corpora lutea being found to occur; while Giacomini, who has investigated the subject in birds, amphibians, and, more particularly, in elasmobranch fishes, also gives an account of the formation of corpora lutea by the hypertrophy of the follicular epithelium. The latter author describes and figures the corpus luteum of Myliobatis as a glandular body in which the follicular epithelium is penetrated by an extensive ingrowth of connective tissue and blood-vessels. This account agrees substantially with what is found to take place in the mouse, the rabbit, and the sheep. A similar description is given by Wallace of the spent follicles in the fishes Zoarces aud Spinax. Zoarces, however, presents a comparatively slight resemblance to the mammals in regard to this point, there being merely a slight hypertrophy of the follicular epithelial cells. In Spinax, on the other hand, there is a considerable hypertrophic enlargement of these cells, together with a thecal ingrowth at various points in a radial manner, and an ingrowth of blood-vessels. Lucein has also described corpora lutea in the reptiles Anguis and Seps, with which there is a simple hypertrophy of the cells of the follicular epithelium, unaccompanied by mitotic division.

It thus appears that the follicular epithelial theory of the origin of the corpus luteum of mammals has been found to be true also for various members of the other vertebrate groups.

The chief results obtained by the investigations of Sobotta, Strata, Honoré, van der Stricht, Colin, Bandes, Vôlker, and the present writer, all of whom agree in adopting this theory, may be summarised as follows :

The lutein cells of the fully-developed corpus luteum represent the epithelial cells of the undischarged Graafian follicle. ‘These cells, after rupture, undergo an enormous hypertrophy, which may be accompanied in the earlier stages by mitotic division, but usually only to a relatively slight extent (Ovis, Vesperugo, etc.). Meanwhile, the thickness of the wall of the developing corpus luteum is further increased by an ingrowth of connective tissue from the side of the follicle, forming eventually an anastomosis of cells, generally fusiform in shape, between the hypertrophying follicular epithelial cells. This connective tissue is derived either from the theca interna alone (Mus, Tarsius, Tupaia, Sorex, Dasyurus, Vesperugo, etc.), or it may arise from both theca interna and externa (Lepus, Ovis, Spermophilus). The formation of the anastomosis is accompanied by an ingrowth of blood-vessels, which gradually increase in number throughout the young corpus luteum. The theca interna may become entirely spent in this process (Mus, Tarsius, Tupaia, Sorex, Ovis, Dasyurus), or certain strands of this layer may remain outside the hypertrophied epithelial cells after the complete formation of the corpus luteum (Lepus, Spermophilns, Vesperugo, etc.). Certain cells in this layer are stated in some cases to become transformed into lutein cells (Vesperugo, etc.). The cavity of the discharged follicle becomes completely filled in eventually by the further growth inward of connective tissue accompanied by blood-vessels.

The corpus luteum may attain to very great dimensions, this structure, when fully formed, in the cow, having a diameter of from two to three centimetres, according to Schmidt.1 Its large size is all the more remarkable in view of its resulting to a large extent from the simple hypertrophy of certain of its constituent cells, namely, those which comprised the epithelium of the ripe follicle. The wonderful property which these cells possess of enlarging within a very short time of the follicle’s rupture, a rapidity which seems to be especially marked in the case of the sheep’s corpus luteum, is apparently without parallel in the histology of the Vertebrata. This unique characteristic becomes additionally interesting when considered in relation to Pflüger’s hypothesis, since supported by Schafer and others, that the cells of the follicular epithelium have a totally different origin from those belonging to the thecal tissue, being in fact derived from the same group of cells as that from which the ova arise.

Heape, in a recently published paper, describes the formation of the corpus luteum in the rabbit as follows:—”The corpus luteum is formed by the ingrowth of cells surrounding the follicle together with the follicular epithelium ; the ingrowth being at one time apparently a forcible rush before which the loosened epithelium is driven. The ingrowth takes place in the first instance in the region of the base of the follicle.”

Miss Lane-Claypon, in a paper lately communicated to the Physiological Society, “On the Post-Natal Formation of Primordial Ova,” states that the ovarian interstitial cells, and the follicular epithelial cells, like the primordial ova, are all “derived from the original ingrowths of the germinal epithetlium,” and not “from the mesoblast, which gives rise to the connective tissue and blood-vessels.” If the epithelial and interstitial cells are potentially and by origin identical, this fact helps to elucidate Van der Stricht’s discovery that in the bat’s ovary both of these elements may take part in the formation of the lutein cells. It is possible also that it provides an explanation of some of the discrepancies between statements by various authors regarding the mode of development of the corpus luteum in different animals. Miss Lane-Claypon says that in the rabbit “the interstitial cells form by far the largest part of the adult ovary,” while in the sheep, judging by my own observations, they are relatively scarce. F. H. A. M.

September 28th, 1905.

Bellot
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Recherches sur l’origine des corps jaune de l’ovaire chez le rat et le cochon d’Inde
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‘C. R. de l’Assoc. des Anatomistes,’ première session, Paris
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1899
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Bovin
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Atrésie des follicules de la Graaf et la formation de faux corps jaunes
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‘Bibl. Anat.,’
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Bühler
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Entwickelungsstadien menschlicher Corpora lutea
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‘Verhand. d. Anat. Gesellschaft in Pavia,’
1900
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Bühler
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Ruckbildung der Eifollikel bel Wirbelthieren
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Clark
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Ursprung, Wachstum und Ende des Corpus luteum, etc
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vii
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1899
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Coiin
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Zur Histologie und Histogenesis des Corpus luteum und des interstitiellen Ovarialgewebes
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Cunningham
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On the Histology of the Ovary and of the Ovarian Ova in certain Marine Fishes
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‘Q. J. M. S.,’
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xl
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1897
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Doering
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Beitrag zur Streitfrage iiber die Bildung des Corpus luteum
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‘Anat. Anz.,’
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Giacomini
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Contributo all’istologia dell’ovario dei Selaci
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Heape
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The Menstruation and Ovulation of Macacus rhesus
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Heape
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His
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Honoré
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Jankowsky
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Beitrag zur Entstehung des Corpus luteum der Saugetiere
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Köllikeb
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Ueber der Entwickelung der Graafschen Follikel
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Köllikek
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Ueber Corpora Lutea Atretica bei Saugetieren
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‘Verb. d. Anat. Gesell.’ Kiel
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Kbeis
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Über Entwickelung und Ruckbildung des Corpus luteum spurium beim Menschen
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Lucien
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Note préliminaire sur les premières phases de la formation des corps jaune chez certains reptiles
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Marshall
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“The Œstrous Cycle and the Formation of the Corpus Luteum in the Sheep,“
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Corpi lutei veri e Galsi da rettili
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Nagel
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Paladino
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Per la dibuttata questione sulla essenza del corpo lúteo
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Rabl
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Sandes
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The Corpus Luteum of Dasyurus viverrinus, etc
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Schmidt
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Beitrage zur Physiologie der Bruust beim Rinde
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Über die Bildung des Corpus luteum bei der Maus
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Über die Bildung des Corpus luteum bei der Maus
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Sobotta
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Über die Bildung des Corpus luteum beiin Kaninclien, etc
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Sobotta
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Sobotta
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Über die Entstehung des Corpus luteum der Saugetliiere
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, 1899,
1902
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Das Wesen die Entwicklung und die Funktion des Corpus luteum
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‘S. B. der phys.-med. Gesell. zur Würzburg,’
1904
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Stöcked
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Ueber die cystisclie Degeneration der Ovarien bei Blasenmole, etc
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‘Sep. Ausdruck aus der Festschrift für Fritsch.’
Stratz
. —
‘Der Geschlechtsreife Saugethiereierstock,’ Haag
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1898
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Stricht (van der)
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La ponte ovarique et l’histogenese du corps jaune
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Stricht (van der)
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La rupture du follicule ovarique et [‘histogénèse du corps jaune
,”
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.
Stbicht (van der)
. —“
Une anomalie intéressante de formation du corps jaune
,”
Gand
,
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.
Stricht (van der)
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L’atrésie ovulaire et l’atrésie folliculairs du follicule de Graaf, dans l’ovaire de chauve souris
,”
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1901
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Völker
. —“
Über die Histogenèse Corporis lutei bei den Ziesel (Spermophilus citillus)
,”
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1904
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Wallace
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Observations on Ovarian Ova and Follicles in certain Teleostean and Elasmobranch Fishes
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1903
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Wendeler
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Williams
. —
‘Obstetrics,’ New York and London
,
1904
.
1

Vide Sobotta, Merkel and Bonnet’s ‘Ergebnisse d. Anal. u. Entwick.’ vol. xi, 1902.

1

Schmidt’s paper, besides containing observations on the corpora lutea, has also an interesting account of the variation noted in the duration of the œstrous cycle, or the interval between two successive “heat” periods, in cattle, as deduced from the study of 500 cases. The most usual length of this period appears to be twenty-one days, but the variation was found to range from six days to one hundred and twenty-one, or even more days. All variations between these periods were noted to occur. Schmidt’s observations are in direct opposition to Beard’s speculation regarding the “Span of Gestation and the Cause of Birth” (Jena, 1897), according to which the interval between two “heat” periods is assumed to bear a fixed relation to the length of the gestation period.