The Works of Francis Balfour 2-19

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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

The Ovum and Spermatozoon | The Maturation and Impregnation of the Ovum | The Segmentation of the Ovum | Dicyemae and Orthonectidae Dicyema | Porifera | Coelenterata | Platyhelminthes | Rotifera | Mollusca | Polyzoa | Brachiopoda | Chilopoda | Discophora | Gephyrea | Chaetognatha | Nemathelminthes | Tracheata | Crustacea | Pcecilopoda | Echinodermata | Enteropneusta | Bibliography
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This historic 1885 book edited by Foster and Sedgwick is the second of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.

The Works of Francis Balfour Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.

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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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Vol II. A Treatise on Comparative Embryology (1885)


THE groups dealt with in the present Chapter undoubtedly belong to the Arthropoda. They are not closely related, and in the case of each group it is still uncertain with which of the main phyla they should be united. It is possible that they may all be offshoots from the Arachnidan phylum.


The development of Limulus has been studied by Dohrn (No. 533) and Packard (No. 534). The ova are laid in the sand near the spring-tide marks. They are enveloped in a thick chorion formed of several layers ; and (during the later stages of development at any rate) there is a membrane within the chorion which exhibits clear indications of cell outlines 1 .

There is a centrolecithal segmentation, which ends in the formation of a blastoderm enclosing a central yolk mass. A ventral plate is then formed, which is thicker in the region where the abdomen is eventually developed. Six segments soon become faintly indicated in the cephalothoracic region, the ends of which grow out into prominent appendages (fig. 245 A) ; of these there are six pairs, which increase in size from before backwards. A stomodaeum (m) is by this time established and is placed well in front of the foremost pair of appendages'*-.

In the course of the next few days the two first appendages of the abdominal region become formed (vide fig. 245 C shewing those abdominal appendages at a later stage), and have a very different shape and direction to those of the cephalothorax. The appendages of the latter become

1 The nature of the inner membrane is obscure. It is believed by Packard to be moulted after the formation of the limbs, and to be equivalent to the amnion of Insects, while by Dohrn it is regarded as a product of the follicle cells.

2 Dohrn finds at first only five appendages, but thinks that the sixth (the anterior one) may have been present but invisible.



flexed in the middle in such a way that their ends become directed towards the median line (fig. 245 B). The body of the embryo (fig. 245 B) is now distinctly divided into two regions the cephalothoracic in front, and the abdominal behind, both divided into segments.


A. Embryo in which the thoracic limbs and mouth have become developed on the ventral plate. The outer line represents what Packard believes to be the amnion.

B. Later embryo from the ventral surface.

C. Later embryo, just before the splitting of the chorion from the side. The full number of segments of the abdomen, and three abdominal appendages, have become established ; m. mouth ; I IX. appendages.

Round the edge of the ventral plate there is a distinct ridge the rudiment of the cephalothoracic shield.

With the further growth of the embryo the chorion becomes split and cast off, the embryo being left enclosed within the inner membrane. The embryo has a decided ventral flexure, and the abdominal region grows greatly and forms a kind of cap at the hinder end, while its vaulted dorsal side becomes divided into segments (fig. 245 C). Of these there are according to Dohrn seven, but according to Packard nine, of which the last forms the rudiment of the caudal spine.

In the thoracic region the nervous system is by this stage formed as a ganglionated cord (Dohrn), with no resemblance to the peculiar cesophageal ring of the adult. The mouth is stated by Dohrn to lie between the second pair of limbs, so that, if the descriptions we have are correct, it must have by this stage changed its position with reference to the appendages. Between the thorax and abdomen two papillae have arisen which form the



so-called lower lip of the adult, but from their position and late development they can hardly be regarded as segmental appendages. In the course of further changes all the parts become more distinct, while the membrane in which the larva is placed becomes enormously distended (fig. 246 A). The rudiments of the compound eyes are formed on the third (Packard) or fourth (Dohrn) segment of the cephalothorax, and the simple eyes near the median line in front. The rudiments of the inner process of the chelae of the cephalothoracic appendages arise as buds. The abdominal appendages become more plate-like, and the rudiments of a third pair appear behind the two already present. The heart appears on the dorsal surface.

An ecdysis now takes place, and in the stage following the limbs have approached far more closely to their adult state (fig. 246 A). The cephalothoracic appendages become fully jointed ; the two anterior abdominal appendages (vn.) have approached, and begin to resemble the oper




(After Dohrn.)

A. An advanced embryo enveloped in the distended inner membrane shortly before hatching ; from the ventral side.

B. A later embryo at the Trilobite stage, from the dorsal side. I., vii., VIII. First, seventh, and eight appendages.

cs. caudal spine ; se. simple eye ; ce. compound eye.

culum of the adult, and on the second pair is formed a small inner ramus. The segmentation of the now vaulted cephalothorax becomes less obvious, though still indicated by the arrangement of the yolk masses which form the future hepatic diverticula.

Shortly after this stage the embryo is hatched, and at about the time of hatching acquires a form (fig. 246 B) in which it bears, as pointed out by Dohrn and Packard, the most striking resemblance to a Trilobite.

Viewed from the dorsal surface (fig. 246 B) it is divided into two distinct regions, the cephalothoracic in front and the abdominal behind. The cephalothoracic has become much flatter and wider, has lost all trace of its previous segmentation, and has become distinctly trilobed. The


central lobe forms a well-marked keel, and at the line of insertion of the rim-like edge of the lateral lobes are placed the two pairs of eyes (se and ce). The abdominal region is also distinctly trilobed and divided into nine segments ; the last, which is merely formed of a median process, being the rudiment of the caudal spine. The edges of the second to the seventh are armed with a spine. The changes in the appendages are not very considerable. The anterior pair nearly meet in the middle line in front or the mouth ; and the latter structure is completely covered by an upper lip. Each abdominal appendage of the second pair is provided with four gill-lamellas, attached close to its base.

Three weeks after hatching an ecdysis takes place, and the larva passes from a trilobite into a limuloid form. The segmentation of the abdomen has become much less obvious, and this part of the embryo closely resembles its permanent form. The caudal spine is longer, but is still relatively short. A fourth pair of abdominal appendages is established, and the first pair have partially coalesced, while the second and third pairs have become jointed, their outer ramus containing four and their inner three joints. Additional gill-lamellae attached to the two basal joints of the second and third abdominal appendages have appeared.

The further changes are not of great importance. They are effected in a series of successive moults. The young larvae swim actively at the surface.

Our, in many respects, imperfect knowledge of the development of Limulus is not sufficient to shew whether it is more closely related to the Crustacea or to the Arachnida, or is an independent phylum.

The somewhat Crustacean character of biramous abdominal feet, etc. is not to be denied, but at the same time the characters of the embryo appear to me to be decidedly more arachnidan than crustacean. The embryo, when the appendages are first formed, has a decidedly arachnidan facies. It will be remembered that when the limbs are first formed they are all post-oral. They resemble in this respect the limbs of the Arachnida, and it seems to be probable that the anterior pair is equivalent to the cheliceras of Arachnida, which, as shewn in a previous section, are really post-oral appendages in no way homologous with antennae 1 .

The six thoracic appendages may thus be compared with the six Arachnidan appendages; which they resemble in their relation to the mouth, their basal cutting blades, etc.

The existence of abdominal appendages behind the six cephalothoracic does not militate against the Arachnidan affinities of Limulus, because in the Arachnida rudimentary abdominal appendages are always present in the embryo. The character of the abdominal appendages is probably

1 Dohrn believes that he has succeeded in shewing that the first pair of appendages of Limulus is innervated in the embryo from the supra-cesophageal ganglia. His observations do not appear to me conclusive, and, arguing from what we know of the development of the Arachnida, the innervation of these appendages in the adult can be of no morphological importance.


secondarily adapted to an aquatic respiration, since it is likely (for the reasons already mentioned in connection with the Tracheata) that if Limulus has any affinities with the stock of the Tracheata it is descended from airbreathing forms, and has acquired its aquatic mode of respiration. The anastomosis of the two halves of the generative glands is an Arachnidan character, and the position of the generative openings in Limulus is more like that in the Scorpion than in Crustacea.

A fuller study of the development would be very likely to throw further light on the affinities of Limulus, and if Packard's view about the nature of the inner egg membrane were to be confirmed, strong evidence would thereby be produced in favour of the Arachnidan affinities.

(533) A. Dohrn. "Untersuch. Ub. Bau u. Entwick. d. Arthropoden (Limulus polyphemus)." Jenaische Zeitschrift, Vol. vi., 1871.

(534) A. S. Packard. "The development of Limulus polyphemus." Mem. Boston Soc. Nat. History, Vol. II., 1872.


The embryos, during the first phases of their development, are always carried by the male in sacks which are attached to a pair of appendages (the third) specially formed for this purpose. The segmentation of the ovum is complete, and there is in most forms developed within the eggshell a larva with three pairs of two-jointed appendages, and a rostrum placed between the front pair.

It will be convenient to take Achelia kevis, studied by Dohrn (No. 536), as type.

The larva of Achelia when hatched is provided with the typical three pairs of appendages. The foremost of them is chelate, and the two following pairs are each provided with a claw. Of the three pairs of larvalappendages Dohrn states that he has satisfied himself that the anterior is innervated by the supra-cesophageal ganglion, and the two posterior by separate nerves coming from two imperfectly united ventral ganglia. The larva is provided with a median eye formed of two coalesced pigment spots, and with a simple stomach.

The gradual conversion of the larva into the adult takes place by the elongation of the posterior end of the body into a papilla, and the formation there, at a later period, of the anus ; while at the two sides of the anal papilla rudiments of a fresh pair of appendages the first pair of ambulatory limbs of the adult make their appearance. The three remaining pairs of limbs become formed successively as lateral outgrowths, and their development is accomplished in a number of successive ecdyses. As they are formed caeca from the stomach become prolonged into them. For each of them there appears a special ganglion. While the above changes are taking place the three pairs of larval appendages undergo considerable reduction. The anterior pair singly becomes smaller, the second loses its claw, and the third becomes reduced to a mere stump. In the adult the


second pair of appendages becomes enlarged again and forms the so-called palpi, while the third pair develops in the male into the egg-carrying appendages, but is aborted in the female. The first pair form appendages lying parallel to the rostrum, which are sometimes called pedipalpi and sometimes antennae.

The anal papilla is a rudimentary abdomen, and, as Dohrn has shewn, contains rudiments of two pairs of ganglia.

The larvae of Phoxichilidium are parasitic in various Hydrozoa (Hydractinia, etc.). After hatching they crawl into the Hydractinia stock. They are at first provided with the three normal pairs of larval appendages. The two hinder of these are soon thrown off, and the posterior part of the trunk, with the four ambulatory appendages belonging to it, becomes gradually developed in a series of moults. The legs, with the exception of the hindermost pair, are fully formed at the first ecdysis after the larva has become free. In the genus Pallene the metamorphosis is abbreviated, and the' young are hatched with the full complement of appendages.

The position of the Pycnogonida is not as yet satisfactorily settled. The six-legged larva has none of the characteristic features of the Nauplius, except the possession of the same number of appendages.

The number of appendages (7) of the Pycnogonida does not coincide with that of the Arachnida. On the other hand, the presence of chelate appendages innervated in the adult by the supra-cesophageal ganglia rather points to a common phylum for the Pycnogonida and Arachnida ; though as shewn above (p. 455) all the appendages in the embryo of true Arachnida are innervated by post-oral ganglia. The innervation of these appendages in . the larvae of Pycnogonida requires further investigation. Against such a relationship the extra pair of appendages in the Pycnogonida is no argument, since the embryos of most Arachnida are provided with four such extra pairs. The two groups must no doubt have diverged very early.


(535) G. Cavanna. " Studie e ricerche sui Picnogonidi." Pubblicazioni del R. Institute di Studi stiperiori in Firenze, 1877.

(536) An. Dohrn. " Ueber Entwickhuig u. Baud. Pycnogoniden." Jenaische Zeitschrift, Vol. v. 1870, and " Neue Untersuchungen lib. Pycnogoniden." Mitthdl. a. d. zoologischen Station zu Neafel, Bd. I. 1878.

(537) G. Hodge. " Observations on a species of Pycnogon, etc." Annal. and Mag. of Nat. Hist. Vol. ix. 1862.

(538) C. Semper. " Ueber Pycnogoniden u. ihre in Hydroiden schmarotzenden Larvenformen." Arbeiten a. d. zool.-zoot. Instit. Wiirzburg, Vol. I. 1874.


The development and metamorphosis of Pentastomum taenoides have been thoroughly worked out by Leuckart (No. 540) and will serve as type for the group.


In the sexual state it inhabits the nasal cavities of the dog. The early embryonic development takes place as the ovum gradually passes down the uterus. The segmentation appears to be complete ; and gives rise to an oval mass in which the separate cells can hardly be distinguished. This gradually differentiates itself into a characteristic embryo, divided into a tail and trunk. The tail is applied to the ventral surface of the trunk, and on the latter two pairs of stump-like unsegmented appendages arise, each provided with a pair of claws. At the anterior extremity of the body is formed the mouth, with a ventral spine and lateral hook, which are perhaps degenerated jaws. The spine functions as a boring apparatus, and an apparatus with a similar function is formed at the end of the tail. A larval cuticle now appears, which soon becomes detached from the embryo, except on the dorsal surface, where it remains firmly united to a peculiar papilla. This papilla becomes eventually divided into two parts, one of which remains attached to the cuticle, while the part connected with the embryo forms a raised cross placed in a cup- shaped groove. The whole structure has been compared, on insufficient grounds, to the dorsal organ of the Crustacea.

The eggs, containing the embryo in the condition above described, are eventually carried out with the nasal slime, and, if transported thence into the alimentary cavity of a rabbit or hare, the embryos become hatched by the action of the gastric juice. From the alimentary tract of their new host they make their way into the lungs or liver. They here become enveloped in a cyst, in the interior of which they undergo a very remarkable metamorphosis. They are, however, so minute and delicate that Leuckart was unable to elucidate their structure till eight weeks after they had been swallowed. At this period they are irregularly-shaped organisms, with a most distant resemblance to the earlier embryos. They are without their previous appendages, but the alimentary tract is now distinctly differentiated. The remains of two cuticles in the cyst seem to shew that the above changes are effected in two ecdyses.

In the course of a series of ecdyses the various organs of the larval form known as Pentastomum denticulatum continue to become differentiated. After the first (= third) ecdysis the cesophageal nerve-ring and sexually undifferentiated generative organs are developed. At the fourth (=sixth) ecdysis the two pairs of hooks of the adult are formed in pockets which appeared at a somewhat earlier stage ; and the body acquires an annulated character. At a somewhat earlier period rudiments of the external generative organs indicate the sex of the larva.

After a number of further ecdyses, which are completed in about six months after the introduction of the embryos into the intermediate host, the larva attains its full development, and acquires a form in which it has long been known as Pentastomum denticulatum. It now leaves its cyst and begins to move about. It is in a state fit to be introduced into its final host ; but if it be not so introduced it may become encysted afresh.

If the part of a rabbit or hare infected by a Pentastomum denticulatum be eaten by a dog or wolf, the parasite passes into the nasal cavity of the


latter, and after further changes of cuticle becomes a fully-developed sexual Pentastomum taenioides, which does not differ to any very marked extent from P. denticulatum.

In their general characters the larval migrations of Pentastomum are similar to those of the Cestodes.

The internal anatomy of the adult Pentastomum, as well as the characters of the larva with two pairs of clawed appendages, are perhaps sufficient to warrant us in placing it with the Arthropoda, though it would be difficult to shew that it ought not to be placed with such a form as Myzostomum (vide p. 369). There do not appear to be any sufficient grounds to justify its being placed with the Mites amongst the Arachnida. If indeed the rings of the body of the Pentastomida are to be taken as implying a true segmentation, it is clear that the Pentastomida cannot be associated with the Mites.


(539) P. J. van Beneden. " Recherches s. 1'organisation et le developpement d. Linguatules." Ann. d. Sden. Nat., 3 Ser., Vol. XI.

(540) R. Leuckart. " Bau u. Entwicklungsgeschichte d. Pentastomen." Leipzig and Heidelberg. 1860.


Very little is known with reference to the development of the Tardigrada. A complete and regular segmentation (von Siebold, Kaufmann, No. 541) is followed by the appearance of a groove on the ventral side indicating a ventral flexure. At about the time of the appearance of the groove the cells become divided into an epiblastic investing layer and a central hypoblastic mass.

The armature of the pharynx is formed very early at the anterior extremity, and the limbs arise in succession from before backwards.

The above imperfect details throw no light on the systematic position of this group.


(541) J. Kaufmann. " Ueber die Entwicklung u. systematische Stellung d. Tardigraden." Zeit.f. wiss, ZooL, Bd. HI. 1851.

Summary of Arthropodan Development. The numerous characters common to the whole of the Arthropoda led naturalists to unite them in a common phylum, but the later researches on the genealogy of the Tracheata and Crustacea tend to throw doubts on this conclusion, while there is not as yet sufficient evidence to assign with certainty a definite position in either of these classes to the smaller groups described in the present chapter. There seems to be but little


doubt that the Tracheata are descended from a terrestrial Annelidan type related to Peripatus. The affinities of Peripatus to the Tracheata are, as pointed out in a previous chapter (p. 386), very clear, while at the same time it is not possible to regard Peripatus simply as a degraded Tracheate, owing to the fact that it is provided with such distinctly Annelidan organs as nephridia, and that its geographical distribution shews it to be a very ancient form.

The Crustacea on the other hand are clearly descended from a Phyllopod-like ancestor, which can be in no way related to Peripatus.

The somewhat unexpected conclusion that the Arthropoda have a double phylum is on the whole borne out by the anatomy of the two groups. Without attempting to prove this in detail, it may be pointed out that the Crustacean appendages are typically biramous, while those of the Tracheata are never at any stage of development biramous 1 ; and the similarity between the appendages of some of the higher Crustacea and those of many Tracheata is an adaptive one, and could in no case be used as an argument for the affinity of the two groups.

The similarity of many organs is to be explained by both groups being descendants of Annelidan ancestors. The similarity of the compound eye in the two groups cannot however be explained in this way, and is one of the greatest difficulties of the above view. It is moreover remarkable that the eye of Peripatus 2 is formed on a different type to either the single or compound eyes of most Arthropoda.

The conclusion that the Crustacea and Tracheata belong to two distinct phyla is confirmed by a consideration of their development. They have no doubt in common a centrolecithal segmentation, but, as already insisted on, the segmentation is no safe guide to the affinities.

In the Tracheata the archenteron is never, so far as we know, formed by an invagination 3 , while in Crustacea the

1 The biflagellate antennae of Pauropus amongst the Myriapocls can hardly be considered as constituting an exception to this rule.

3 I hope to shew this in a paper I am preparing on the anatomy of Peripatus.

8 Stecker's description of an invagination in the Chilognatha cannot be accepted without further confirmation ; -vide p. 388.


evidence is in favour of such an invagination being the usual, and, without doubt, the primitive, mode of origin.

The mesoblast in the Tracheata is formed in connection with a median thickening of the ventral plate. The unpaired plate of mesoblast so formed becomes divided into two bands, one on each side of the middle line.

In both Spiders and Myriopods, and probably Insects, the two plates of mesoblast are subsequently divided into somites, the lumen of which is continued into the limbs.

In Crustacea the mesoblast usually originates from the walls of the invagination, which gives rise to the mesenteron.

It does not become divided into two distinct bands, but forms a layer of scattered cells between the epiblast and hypoblast, and does not usually break up into somites ; and though somites are stated in some cases to be found they do not resemble those in the Tracheata.

The proctodaeum is usually formed in Crustacea before and rarely later 1 than the stomodaeum. The reverse is true for the Tracheata. In Crustacea the proctodseum and stomodaeum, especially the former, are very long, and usually give rise to the greater part of the alimentary tract, while the mesenteron is usually short.

In the Tracheata the mesenteron is always considerable, and the proctodaeum is always short. The derivation of the Malpighian bodies from the proctodaeum is common to most Tracheata. Such diverticula of the proctodaeum are not found in Crustacea.

1 This is stated to be the case in Moina (Grobben).