Zoomorphology (1987) 107:161-168 Zoomorphology © Springer-Verlag 1987

Structural organization of the gills in pipefish (Teleostei, Syngnathidae) M. Prein 1, and A. Kunzmann 2 i Institut für Meereskunde an der Universität Kiel, Düsternbrooker Weg 20, D-2300 Kiel, Federal Republic of Germany 2 Institut für Polarökologie an der Universität Kiel, Olshausenstr. 40, D-2300 Kiel, Federal Republic of Germany

Summary. The morphology and structural features of the gills of the two Western Baltic pipefish Nerophis ophidion and Syngnathus rostellatus were investigated using scanning electron microscopy. The general anatomy of the gills com- plies with the general pattern in fish. Several adaptations though, show the highly specialized nature of pipefish gills. The filaments are extremely short, few in number and carry only a few lamellae due to the limited space in the branchial cavity. The lamellae have a widely projecting form yet still have a small area in comparison to other fish. Gill irrigation is performed by a specialized pumping mechanism which forces respiratory water through the small but densely packed gill sieve. Although both species live in the same habitat and belong to the same family, differences in gill morphology were found and are related to different life- styles. S. rostellatus is the more active species and therefore has more filaments per gill arch, more lamellae per filament, wider projecting lamellae and a more extreme utilisation of available space in the gill cavity through a very densely packed gill sieve. N. ophidion has a stationary mode of life and therefore has a less extreme gill anatomy.

A. Introduction

Together with the sea-horses, pipefish belong to the special- ized family Syngnathidae (Dawson and Vari 1982; Dawson 1985). These are mainly dwellers of the eelgrass zone of coastal water and are highly adapted to this habitat in their morphology and biology (Duncker 1900; Fiedler 1954).

Among the curious adaptations characteristic of this family is the specialized but reduced cranial architecture (McMurrich 1883; Jungersen 1910; Kindred 1921, 1924; Kadam 1958, 1961). Pipefishes are characterized by a pro- longed snout with only a small mouth at its tip. They are diurnally active sight-feeders (Ryer and Boehlert 1983) util- ising bino¢ular vision together with a very efficient feeding mechanism (Palmgren 1977; Osse and Müller 1980). Asso- ciated with a relatively inactive lifestyle between the eel grass leaves, prey is struck from a distance of a few cm using a stationary ambush method (Howard and Koehn 1985). An elaborate suction mechanism creates a strong inhalent current through which prey is sucked into the mouth (Corrigan 1860; Duncker 1900).

The peculiar condition of the skull has direct conse-

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quences for the functional anatomy and morphology of the entire respiratory apparatus (Jungersen 1910; Rauther 1925). The resulting character has lead to the false and misleading name Lophobranchii (Cuvier and Duvernoy 1805, 1840) accompanied by descriptions o f the " loba te" gills, arranged in "grapes or tufts" (Tiedemann 1816), where "the filaments do not stand in parallel rows, but rather stand together in bushes, tree- or featherlike forma- tions" (Harder 1964).

These erroneous notes are preceeded by the oldest de- scriptions of syngnathid gills, which already note correctly that their principle of construction does not differ from the general pattern in fish (Artedi 1738; Villeneuve 1756 in Meckel 1883; Lacépède 1800). Further reports on the gills of different species of the Syngnathidae were presented by Rathke (1832), Meckel (1883) and Retzius (1835). The most detailed examinations have been conducted by Riess (1881), Ryder (1882), Huot (1902) and finally Rauther (1925) in an extensive monograph.

The two examined species, Nerophis ophidion (Linné, 1758) and Syngnathus rostellatus (Nilsson, 1855) occur fre- quently in the same habitats of the brackish water of Kiel Bight, Western Baltic. N. ophidion attains a length of 30 cm and a weight of 2 g, while S. rostellatus has a maximum length of 17 cm at a weight of about 1.6 g. The purpose of this study is to investigate the gross morphology of the relatively small gills with scanning electron microscopy (SEM), compare the results with older findings and discuss any differences between these two small species.

B. Material and methods

Live specimens were caught in several different eelgrass meadows of the Kiel Bight to a maximum depth of 6 m with a small beam trawl on board FB SAGITTA or during SCUBA dives. Besides Nerophis ophidion and Syngnathus rostellatus, few specimens of Entelurus aequoreus (Linné, 1758) and Syngnathus typhle Linné, 1758, were caught and partly included in our examinations. Morphological exami- nations and dissections of fresh material were conducted under a binocular microscope. Section cuts 7 lam thick for compound light microscopy were prepared from gill sam- ples stained with the Goldner method.

Scanning electron microscope (SEM) samples were fixed in 2.5% glutaraldehyde (0.1 M phosphate buffer) and rinsed 5 times for 10 min in Soerensen phosphate buffer (pH 7.4) with an additive of saccharose to adjust for their ambient environmental salinity of 17%0 or 450 m osmol

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~ , - " - - - v ~ ~ ~ r - - - ' ~

Ps 1 2 3 4

l _ _ 1 l a 1mm

Ps 1 2 3 4

I I

l b 1~~

Fig. la, b. Flow of respiratory water current (arrows) through gill arches, opercular cavity and egestion porus with opercle removed. a N. ophidion, b S. rostellatus. Striped area denotes cross-cut tissue. White area between gills and striped area represents cranial encasement reaching almost up to opercle, thereby limiting gill expansion. Filaments are slightly schematic. Note interlocking arrangement of filaments of different arches. Ps pseudobranch; 1-4 number of gill arch

Fig. 2 a, b. Total preparation of branchial apparatus attached to pin. a N. ophidion, ventral view. b S. rostellatus, lateral view. Pseudobranch missing in this object (lost during preparation). Note more dense packing of filaments and lamellae in S. rostellatus; A anterior end; P posterior end; V ventral side and D dorsal side of gill. Lines indicate limits of single gill arches; 1~4 number of gill arch

which should prevent shrinkage of the delicate and spongy gill tissue. This was followed by postfixation in 2% osmium- tetraoxide with phosphate buffer and dehydration over sev- eral steps in an ethanol series. Ethanol was exchanged against freon in an ascending seiles of freon-ethanol mix- tures. The objects were dried in pure freon in an Omar-SPC- 900/EX critical point dryer with carbondioxide. To enable viewing of the objects from all sides, 1 cm pins were pasted vertically on stubs with conductive carbon cement (Neu- bauer Leit-C-Paste). The objects were mounted onto the pins with Emetron Leitsilber 2000 and sputtered with gold- palladium in a Technics Hummer I. Finally the gills were observed and photographed with a Zeiss-Semco nanolab 7 SEM.

C. Results

In both species, the gills are completely covered by the oper- cle which is fused to the body by an elastic membrane, leaving only a dorsal aperture as gitl-opening with a valve- like closure (Fig. 1). This is common to all syngnathids, enabling a very efficient pumping mechanism for gill venti- lation in their mainly stationary lifestyle.

1. General arrangement

The structural pattern maintained throughout consists of an anterior pseudobranch followed by four complete arches with five gill slits (Figs. 1, 2). The branchial apparatus as a whole is more elongate and wedge-shaped in N. ophidion than that of S. rostellatus which is relatively compressed, higher and rounded posteriorly. The water flow pattern in the cavity is essentially the same in both species (Fig. 1). It shows that the greatest gill expansion has resulted in the small cavity volume, indicating possible problems for adequate irrigation when the already elaborate pumping apparatus is overcharged duilng high oxygen demand. This explains why pipefish are difficult to handle upon capture and great care is required to avoid overstressing leading to immediate mortality.

2. Pseudobranch

A "f ree" pseudobranch is present in both species, always consisting of 3 well-developed, posteriorly pointing fila- ments. The form of the filaments does not differ from that of those on the other gill arches (Fig. 3). They are relatively small in comparison to other gill filaments.

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Fig. 3. N. ophidion. Completely "free" pseudobranch and first gill arch of left gill side. There a rea few remnants of mucus between lamellae. Note alternating insertion of lamellae to filaments

Fig. 4. Single filament of S. rostellatus attached to pin. Arrows indicate path of water flow. Note size distribution of lamellae over filament

Fig. 5. View of gill arch of S. rostellatus from gill slit. Note "crowding" of filaments at points of insertion to gill arch in S. rostellatus and shapes and distribution of lamellae over filament. Arrows indicate direction of water flow

3. Fi laments

While the pseudobranch is a hemibranch, all other gill arches are holobranchs on which the gill filaments are ar- ranged in alternating positions (Figs. 1, 2). Counts of the number of filaments per arch support the indication from

the overall form of the entire gill. The gradually increasing numbers from the first to the fourth arch are characteristic for N. ophidion, whereas in S. rostellatus the second and third arches carry the most filaments. These and other inter- specific differences compiled from the literature are listed in Table 1. The filament numbers increase only slightly with

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Table 1. Numbers of filaments on both sides of gill arches in the Syngnathidae. W fish weight; Ps pseudobranch; T N F total number of filaments in both gill sides without pseudobranch. Odd sums originate from differences in both sides

Species Gill arch Author

W (g) Ps. 1 I1 II1 IV TN F

Neroph& maculatus 2 8 9-10 10 8-11 74 Rauther 1925 N. ophidion - - max 8 Rathke 1832

3-4 8 10 10-11 10-11 78 Rauther 1925 0.14 3 8 10 11 11 78 Present study 0.25 3 8 10 11 11 78 Present study 0.29 3 8 10 10 10 76 Present study 0.32 3 6 8 8 9 62 Present study 0.36 3 8 10 11 11 78 Present study 0.54 3 8 10 11 11 77 Present study 0.95 3 8 11 12 11 88 Present study 1.10 3 8 I0 10 11 78 Present study 1.12 3 8 10 11 11 77 Present study 1.34 3 8 11 11 11 82 Present study 1.35 3 8 10 10 10 76 Present study

Entelurus aequoreus 8.14 3 12 15 15 15 120 Present study Syngnathus sp. - 1 ~ 2 0 Huot 1902

. . . . 80 Tiedemann 1816 S. acus - max 12 Rathke 1832

- - 16 - Retzius 1835 - 3-4 10 12 13 11-12 10-11 89 Rauther 1925

S. typhle - max 12 Rathke 1832 - 3-4 1~13 15-16 16 14-15 117 Rauther 1925 0.50 3 11 16 16 14 116 Present study 0.97 3 11 15 16 14 117 Present study 2.59 3 11 16 14 14 113 Present study

S. rostellatus 0.16 3 10 12 12 10 88 Present study 0.26 3 10 12 12 11 89 Present study 0.33 3 12 16 16 14 115 Present study 0.35 3 10 12 12 11 90 Present study 0.45 3 10 12 12 10 88 Present study 0.49 3 10 12 12 11 90 Present study 0.54 3 10 12 12 11 90 Present study

- 3 10 12 12 10 88 Present study 0.62 3 10 12 12 11 90 Present study 0.99 3 11 15 15 12 105 Present study 1.37 3 12 15 16 14 113 Present study

Hippocampus sp. - - 11 15 15 11 104 Cuvier and Duvernoy ! 805, 1840

H. antiquorum max 20 Ryder 1882 H. hippocampus - 3-4 12 13 16-18 14-16 12-13 114 Rauther 1925 H. ramulosus 3-4 13-14 16-17 15 16 1~15 118 Rauther 1925

Fig. 6a-e . Compar ison of mean lamellar forms of different fish species (adapted and modified from Hughes and Morgan 1973a). a Flounder; b eel; c horse mackerel; d N. ophidion; e S. rostellatus. Note direction of water flow (arrow) in relation to form of lamellae. Pipefish are of mean sizes

Fig. 7. Schematic diagram of irrigation of filaments and lamellae in syngnathids. Lines on filaments indicate insertion of lamellae. Black arrows indicate water flow pattern. Note interlocking of filaments of neighboring arches and limited space in opercular cavity

Fig. 8. Tip of filament and lateral view of lamellae in N. ophidion. Arrows indicate flow of respiratory water that emerges from the gill slit to the left of the filament

Fig. 9. Nerophis ophidion. Ultrastructure of trailing edge of lamellar epithelium. Note moderate lengths of microvilli and microridges, and twin-rimmed cell borders and pores between two or more pavement cells

Fig. 10. Syngnathus rostellatus. Ultrastructure of lamellar epithelium on leading edge of lamellae. Note concentrically whorled microridges on filament and twin-rimmed cell junctions between polygonal pavement cells on lamellae. Arrows indicate flow of respiratory water

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a

6

E~

BUCCAL CAV lTY

I 0 " 5 m m I

d e 7 ~OPERCLE

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increasing fish size. The total numbers per gill range from 62 to 88 in N. ophidion and 88 to 115 in S. rostellatus. Newly hatched pipefish are already equipped with a nearly complete set of filaments. Numbers on individual arches may be odd due to the alternating mode of insertion to the arch. Sums of both gill sides may also be odd due to differences between the complementary arches on either side.

Due to limited space in the opercular cavity, syngnathids show a slightly modified form of the general teleost gill. Compared to normal proport ions in fish gills, the limited space between arches and opercle restricts the length of the filaments, which appear shortened and thickened (Fig. 4). In viewing from the gill slits, the filaments are pear-shaped, being thickened distally and very slim at their point of insertion to the gill arch, where they are close to adjacent filaments pointing in the opposite direction.

4. Lamellae

The compressed and stunted impression of the filaments is caused by the size and form of the lamellae in proport ion to the filaments. The lamellae seem extremely widened and project far in comparison to the length of their insertion to the filament (Fig. 6), thereby achieving a relatively large surface area in a limited space (Figs. 5, 8). This is also shown in cross-sections through the filaments. Together with the SEM observations, these reveal another character- istic difference between the two species. The lamellae of S. rostellatus are more projecting than those of N. ophidion (Fig. 6). The marked slanting of lamellae towards the water current is also apparent in syngnathids. Mean lamellar sizes o f both pipefish are smaller than those in other fish, yet not unusual for their small body size.

On the filaments, the lamellae are also arranged in an alternating sequence. The size distribution of the lamellae over the filaments is much more obvious than in other fish since the absolute number o f lamellae on a single filament is extremely low. The maximum number of lamellae on a single filament is around 32 in S. rostellatus and only 20 in N. ophidion.

5. lrrigation of lamellae

The filaments and lamellae are aligned in such a manner that the watercurrent emerging from the gill slits is diverted by an angle o f about 45 ° for the irrigation of the lamellae (Fig. 7). The straightest possible passage of the water through the gills is not chosen, rather the longest possible contact surface betwen respiratory epithelium on the lamel- lae and the oxygen-supplying water is established. The gen- eral outward curvature o f the filament tips is maintained also in syngnathids. The extremely short filaments have a boot-like appearance from a lateral viewpoint (Fig. 7). Through the outward curvature and an interlocking of op- posite filaments o f neighbouring arches, the lamellae find adequate exposure to the respiratory water current. There- by the most efficient use is made of the limited space in the gill cavity. This arrangement takes the highest possible advantage o f the counter-current principte of blood oxygen- ation in the fish gill and may be regarded as a further adaptat ion of the gills to the lifestyle of pipefish.

6. Surface ultrastructure

The epithelial surface of the filaments reveals the common microridge structure in concentric whorls, while the surface of the lamellar epithelium is characterized by polygonal cells with microvilli (Fig. 10). The twin-rimmed cell borders are conspicuous in both species. On the trailing edge of the lamellae, pores are present on all gill arches between cell junctions where several cells meet (Fig. 9).

D. Discussion

In the Syngnathidae, gill ventilation is performed mainly by the opercular suction pump. The buccal pressure pump plays only a minor role, also due to the extreme pipe-form of the mouth (Hughes 1960). The Syngnathidae lack a true branchiostegal apparatus (Jungersen 1910). Pipefish rely en- tirely on the highly efficient mechanism for breathing con- stituted by the closed opercular cavity with the minute dor- sal exhale porus. This mechanism, with its dimensions, seems adequate for their stationary mode of life, but should make them highly sensitive to cases of severe stress. The " c rowded" situation in the gill cavity (Fig. 1) leaves only minor reserves for an increase in efficiency of oxygen up- take. Mechanisms employed in fish gills include vasodila- tion, leading to an increase in lamellar volume through swelling, and active repositioning of the filaments in the water current through branchial musculature (Laurent 1984). These are bound to give poor results due to the limited space in the opercular cavity.

The main response to situations of elevated oxygen de- mand is the increase in ventilatory stroke volume and not ventilatory stroke frequency (Davis and Cameron 1971). This principle encounters limits in pipefish since the opercle has a limited stroke depth through the elastic membrane connecting the opercle with the cranium (Fig. 7).

Differences in the form of the entire gill are only slight between the two investigated species. At comparable weights, S. rostellatus has 12% to 50% more filaments in the gills than N. ophidion (Table 1) whose filaments and lamellae also appear less densely packed (Fig. 2). The total number of filaments in the gills of the Syngnathidae is ex- tremely low, even for a sluggish bot tom living species (Hughes 1966; Hughes and Morgan 1973a, b; Hughes 1984). The conspicuous form of the filaments in syngnath- ids is mainly a result of the very short filaments in compari- son to most fish (Hughes 1966; Munshi and Singh 1968). This may lead to the erroneous impression that the lamellar area, as the actual site of oxygen uptake in the fish gill, is extraordinarily enlarged. The lamellae are, in spite of their widely projecting form, still comparatively small, and this should have direct consequences for the total respirato- ry surface area. A similar, but not as extreme lamellar form was reported by Schmidt (1942) for a member of the Sti- chaeidae.

Differences between N. ophidion and S. rostellatus in the individual lamellar form, and thereby also the lamellar area, are the most conspicuous feature of their gills. How- ever both have very extreme forms (Fig. 6), in spite of their small size. All peculiarities of gill structure in syngnathids may be regarded as characteristic adaptations to their spe- cialized body form and biology. Consequently, all differ- ences found may be directly related to their mode of life. Both species use their specialized mouth and opercular suc-

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tion apparatus as a highly effective weapon in capturing prey. Although both inhabit the eelgrass zone, they differ in their life habits. N. ophidion lacks tail, anal and pectoral fins and is relatively immobile, in contrast to S. rostellatus which possesses pectoral and caudal fins. While N. ophidion leads a mainly stationary mode of life between the eelgrass leaves, which it grasps with its prehensile tail (Heincke 1880; Duncker 1900), S. rostellatus moves about freely be- tween the eelgrass leaves and even hunts about in the watet column (Duncker 1900; Fiedler 1954).

Another important difference is the mode of paternal care for the eggs and larvae. In N. ophidion, the embryos are attached to the ventral bony plates of the male and have free contact to the surrounding water. In contrast, S. rostellatus embryos are kept in a ventral brood pouch with a placenta-like tissue which is completely sealed from the surrounding seawater. All necessary oxygen must be supplied to the larvae by the father and through his gills.

Taking all differences into account, S. rostellatus re- quires an adequately and more efficiently dimensioned gill apparatus due to its more active mode of life, despite the restrictions imposed by its specialized cranial architecture. This is provided by the characteristic features found in the course of this study of external gill morphology. On the other hand, N. ophidion seldom encounters activity levels beyond routine metabolism. Their gills therefore only need dimensions for lower levels of oxygen delivery. Relation- ships between respiratory surface area and fish size, activity and growth performance have been investigated by Gray (1954), Hughes (1966), Muir (1969), Hughes and Morgan (1973a, b), de Jager and Dekkers (1975) and Pauly (1981). A comparative study of gill morphometry in the two species is presently in progress.

Acknowledgements. We would like to express our thanks to Dr. D. Pauly for encouraging the present investigation and critically reviewing the manuscript. To Prof. W. Nellen go our thanks for the provision of laboratory facilities. Dr. R. Schmaljohann and Mrs. B. von Brevern advised us in the use of the SEM. Prof. B. Tillmann provided helpful suggestions for the preparation of the gills for the SEM and Miss U. Kruse introduced us to the necessary laboratory methods.

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