HARMS (1928) observed the early stages and the external transformation during the metamorphosis of Periophthalmus vulgaris s. argentilineatus. He found that just hatched Periophthalmus species are hardly distinguishable from the larvae of Gobius and are still typical benthic fish, while animals in the metamorphosis (see HARMS 1928, Fig. 23b and c) inhabit riparian zones and already leave water for a short time. These later stages as well as the stages in which metamorphosis has not yet much advanced, and also animals after finishing metamorphosis could be investigated for the formation of the respiratory organs, in addition to young fish of Boleophthalmus boddarti,*6P1 which were
completely similar to the animals in the stationary phase in the outer body form*1P86.
1. Boleophthalmus boddarti.*6P1 In the youngest stages of 1.8 cm length, the gills are completely developed. The epithelium of the buccal and branchial cavities is bilayered and very thin; at its base there is already an extensive capillary net, which indents the epithelium from the inside. The distribution of the vascularized epithelium is already the same as in an adult animal.
In contrast, the development of the skin papillae could be followed in the available material. First (Fig. 43), a network of capillaries (Kap.) appears in the uppermost layer of the dermis (C.), which vertically ascends in the dermis in several branches Fig. 42 Cross section through the bulbus arteriosus of Periophthalmodon
schlosseri,*8P1 schematic representation. LEITZ Objective 3, Ocular 1, Tblg. 152, reduced to 2/3.
Fig. 43 Cross section through the dorsal trunk skin of 2 cm long Boleophthalmus boddaerti*6P1 (stage I of papillary development). For explanation see Fig. 44.
56 An annotated translation of Schöttle (1931)
and lie closely against the exterior surface (stage I).
The germinative stratum (St.g.) is flattened where the capillaries run closely under it; however, the overall height of the epidermis has not yet decreased. Then, individual connective-tissue fibers split off from the tight dermis (Fig. 44, B.g.), which pushes the capillary loops (Kap.) outward, so that the epidermis is arched and pressed flat from downside at this site. In this stage II, it can be clearly seen that the epidermal cover of the papilla consists of the germinative stratum (St.g.), a layer of turgor cells (ves.Z.) and a cover layer (D.), all of which are strongly flattened. The capillary no longer lies close to the dermis, but is held in the periphery of the still flat dermal papilla*2P86 through more and more radially arranged supporting fibers. Pigment cells (P.) are also found between the connective tissues of the papilla anlage.
In this developmental stage, the capillary still forms a simple loop, a condition which is continuously retained in the skin of the operculum in Scartelaos histophorus.*7P1 In the next stage III, small side branches come off from the capillary loop, which insert between the basal epidermal cells over the papilla and therefore are covered only by the thin outermost layer. The dermal papilla*2P86 expands and becomes higher with the increase of the epidermal layers; the afferent and efferent vessels branch out, in order to be able to supply the increased papillary surface with sufficient blood. Thus, the final stage is reached. — Only when the papillae are almost completely developed, the scales are formed; in the stages I, II and III of papilla formation they are missing. The
scale formation proceeds in such a way that connective tissue cells in the loose connective tissue at the base of a papilla merge flat into two layers and then the scale substances deposit between the two layers. Even later, the scleroblasts of the scale lie on the outside at large intervals. The process of the formation of hard substance and the further development of the scales were not analyzed closely, but seem to agree with the conditions described for other teleosts (see.
BIEDERMANN 1928).
The respiratory papillae develop first in the posterior region of the head: In a young fish of 1.8 cm length, the stage II is found in this area, while only the stage I is developed in the skin of the operculum and the anterior head region. Starting from the posterior region of the head, the papillary development first proceeds cranially, and to the sides, then also more and more caudally. In an animal of 2 cm length, the stage II was present up to the posterior edge of the eyes (Fig. 44), and also the stage II began to gradually develop laterally in the dorsal region of the operculum, while the stage I occurred dorsally in the trunk (Fig. 43). On the other hand, in young fish of 2.1 cm length, the stage II occurs in the dorsal skin of the trunk, on the entire top side of the head to the upper jaw and laterally on the operculum, while only the stage I is found in the cheek region and laterally at the trunk.
With further growth the papillae are developed also here.
2. Periophthalmus vulgaris.*9P1
The smallest individual available was 0.95 cm Fig. 44 Cross section through the dorsal skin of the posterior head region of 2 cm long Boleophthalmus boddarti*6P1 (stage II of papillary development). Susa fixative, Azan staining; LEITZ Immersion 1/12, Ocular 4, Tblg. 152, reduced to 4/5. B.g. connective tissue fibers, C.
dermis, D. cover layer, Kap. capillary, P. pigment, St.g. germinative stratum, ves.Z. vesicular cell.
57 Bull. Fac. Fish., Nagasaki Univ. No. 101
long and was in the metamorphosis; the exophthalmos*1P88 was clear but still incomplete.
The gills (Fig. 45) resemble completely those of Gobius, because the lamellae are covered by an epithelium of flat cover cells (Fig. 45, D.), and no gland cells occur on the lamellae, while in the epithelium of the gill filament trunk mitochondria-rich cells (e.E.dr.)*7P11 are abundant. In young fish of 0.98‒1.1 cm length the gill lamellae begin to transform (Fig. 46). The epithelium contains gland cells, above all mitochondria-rich cells (e.E.dr.),*7P11 besides isolated mucous and granular
glands*2P12 (Fig. 46, K.dr.). Gland cells occur particularly at the base of the lamella, while they are missing on the outside and the epithelium here consists only of flat cover cells (D.). The thickening of the surface epithelium begins in the proximity of the gill filament trunk and increasingly proceeds to the outside. In completely metamorphosed young fish of 1.25 cm length and larger, the gland cells have spread over the whole lamellar surface up to the periphery; as in an adult animal, most flat cover cells alternate with mitochondria-rich cells, which are apposed underneath the cover cells and
Fig. 45 Cross section through the gill lamella of 0.95 cm long Periophthalmus vulgaris.*6P5 Susa fixative, DELAFIELD Hematoxylin and eosin staining; LEITZ Immersion 1/12, ZEISS Composite Ocular 12, Tblg. 152, reduced to 4/5. Explanation as in Fig. 46.
Fig. 46 Cross section through the gill lamella of 0.98 cm long Periophthalmus vulgaris.*6P5 Susa fixative, Azan staining; Magnification as Fig. 44. D. cover layer, e.E.dr.
invaginated mitochondria-rich cell, K.dr. granular gland, Pil. Pillar cell.
58 An annotated translation of Schöttle (1931)
apparently form the second layer.
In this stage, the epithelium of the branchial cavity is also completely differentiated: the capillaries run at the basis of the bilayered epithelium and reach closely under the surface, while in animals up to 1.2 cm body length, it*1P90 consists only of one cell sheet and is not particularly heavily supplied with blood.
It is remarkable that the skin is vascularized already in the youngest stages of 0.95 cm length.
The skin capillaries that ascend vertically and branch out in the uppermost surface layers of the epidermis are typically formed (see also Fig. 15 of one individual of 0.98 cm length, Kap.), and in fact spreading dorsally in the entire body up to between the eyes but scarcely in the region of the operculum toward the side. In animals of 1.2 cm length, blood vessels in the epidermis appear for the first time also laterally underneath the eyes. In the further process of the development, the vascularization of the epidermis on the sides spreads to the entire head and trunk. Scales are formed only later, namely the scale development begins in animals of 1.25 cm length laterally on the tail and spreads subsequently more cranially and dorsally, until the normal scaling is reached in approximately 2.3 cm length.
The blood vessels of the head were reconstructed from a 0.98 cm long Periophthalmus vulgaris.*9P1 The large vessels of the head as well as principal arteries and veins of the skin and epithelium of the buccal and branchial cavities are present, but do not
branch out yet in the same extent as in sexually matured animals.
Also, the bulbus arteriosus shows a progressive complication during the developmental process: In young fish up to approximately 1.2 cm length only narrow longitudinal septa are present in the bulbus, which radiate inwardly and do not touch each other (Fig. 47). The bulbus is formed here very similarly to for example that of Gobius auratus. In animals of 1.25 cm length and larger, the bulbus wall gradually thickens, and the septa widen increasingly (Fig. 48), until the final condition is reached (see Fig. 40).
From the mentioned findings, it can be seen that the skin first functions as an accessory respiratory organ in Periophthalmus vulgaris.*9P1 Then, the vascular net develops under the epithelium of the branchial cavity. At the same time, gland cells emerge on the gill lamellae and finally occupy their whole surface. Only then the wall of the bulbus arteriosus thickens.
3. Periophthalmodon schlosseri.*8P1 In a young fish of 1.5 cm length, shortly after the metamorphosis with completely developed exophthalmos, the gill lamellae are not yet coalesced; they are closely occupied with cuboidal, usually tubular*1P91 mitochondria-rich cells and resemble in this stage those of Periophthalmus chrysospilos or of those types of P. vulgaris,*9P1 whose gill lamellae are built according to the Fig. 47 Fig. 48
Fig. 47 Cross section through the bulbus arteriosus of 1 cm long Periophthalmus vulgaris,*6P5 schematic representation. LEITZ Objective 7, Ocular 1, Tblg. 150, reduced to 1/2.
Fig. 48 Cross section through the bulbus arteriosus of 1.7 cm long Periophthalmus vulgaris,*6P5 schematic representation. LEITZ Objective 7, Ocular 1, Tblg. 152, reduced to 1/2.
59 Bull. Fac. Fish., Nagasaki Univ. No. 101
second type (see page 17*2P91).
Also the epidermis still shows a more primitive structure than in larger animals; due to the lower height, no arterioles with circular muscle cells advance toward the epidermis, but capillaries that ascend perpendicularly and are only accompanied by a thin connective tissue membrane advance toward the epidermis,*3P91 as in the other Periophthalmus species. On the top of the head, the terminal branches of the capillaries bulge the surface between the surface layers outward in a crest shape,*4P91 a peculiarity, which is also found in adult Periophthalmodon schlosseri*8P1 (see. Fig.
16).
The epithelium of the branchial cavity resembles that of Periophthalmus vulgaris*9P1; at this stage, it is still very flat, has two layers and contains numerous, slightly invaginated mitochondria-rich cells.*3P12 The capillaries lying on basis of the epithelium bulge it*5P91 only slightly.
The mucous membrane of the buccal cavity is built even more primitively; it also resembles that of Periophthalmus vulgaris*9P1 and yet has no respiratory function, since capillaries are absent either in the epithelium basis or in the dermis.
The septa of the bulbus arteriosus are broad and partially touch each other near the center line; they do not carry secondary ridges, and therefore the bulbus completely resembles that of Periophthalmus vulgaris.*9P1
Also, a young Periophthalmodon schlosseri*8P1 o f 3.5 cm length still has no fused gill lamellae. In contrast, the epithelium of the buccal and the branchial cavities was further differentiated; it is very heavily supplied with blood, and indeed the capillaries penetrate between the cells of the upper layers as in an adult animal.
In the bulbus arteriosus the ventral septa carry small projections on the side, while the dorsal ones are still undivided.
These observations suggest that Periophthalmodon schlosseri*3P9 passes through a stage similar to Periophthalmus vulgaris*9P1 in the course of ontogenesis.
VI. Contribution to the physiology of the