Tuatara: Volume 16, Issue 2, July 1968
The world of eels
The world of eels
Mammals and Birds are often distinguished from other vertebrates in having complex behavioural patterns and ecological relationships of a type not shown by the “lower’ groups. From a human point of view they would thus seem to be of much greater interest. However, the counterparts of these patterns and relationships are also highly complex in fishes but unfortunately they are not so readily observable. In addition, fishes are interesting as a group in the way in which they have diversified in time and space so that they now form the largest section of the vertebrates with more than 20,000 living species. Many new forms are described each year and no doubt more have yet to be recognised as various habitats are examined more closely, especially that of the deep sea. It is for this reason that description and classification is still an active field in ichthyology, while such studies have largely been replaced by other disciplines in the study of terrestrial vertebrates.
The bony fishes (or Osteichthyes), which make up the bulk of the fishlike vertebrates, have been undergoing a vast “adaptive radiation’ since their firm establishment as a diverse group in the middle of the Mesozoic. At that time, the reptiles were at their peak and the mammals were also becoming established. The huge diversity of modern bony fishes resulting from this radiation has come about by considerable physiological and morphological adaptations, for which the bony fishes are well known. It is true to say that while individual species of bony fishes are more restricted to particular physical conditions than are species of birds and mammals, their multitude and variety of adaptations have also enabled them as a whole to enter a variety of habitats. Thus, bony fishes may be found from high mountain streams almost to the page 86 greatest depths of the oceans; they inhabit hot freshwater lakes through to the coldest of polar seas; a few are capable of limited flight and some are active on land; and others even lead parasitic lives.
The study of the many structural modifications of living fishes has a very real part to play in modern ichthyology, including classification and phylogeny. Greenwood et. al. (1966: 346) point out that classificatory schemes for teleosts (the bulk of living bony fishes) must necessarily be based on the study of extant forms, because the fossil record is so poor.
The main bulk of the Teleostei comprises a large group of rather generalised forms (the spiny-finned teleosts, or Acanthopterygii) with a number of smaller specialised groups which probably arose from a variety of ancestors in the late Mesozoic. As a result of the early divergence of the more specialised groups, they bear little resemblance to the main stream of teleosts.
One of these specialised offshooots is the Anguilliformes, or eel-like fishes. This contains at least 100 genera and several hundred species, all of which are elongate in form with many vertebrae (as many as 500-600, but in most species there are about 100-200). Eels show a marked reduction in the bones of the skull and associated structures, and pass through an extended pelagic larval phase in early life. The sinuous body form is also seen in various other teleosts which are not related to eels, and nearly always seems to be associated with a bottom-dwelling, fossorial (burrowing) or crevice-dwelling mode of life. However, no other teleosts have the peculiar, leaf-like transparent larva (or leptocephalus) as well as the elongate body which are so characteristic of the Anguilliformes.
In some eels elongation of the body has been carried to the extreme. For example, the tropical moray Thyrsoidea macrura has been reported to reach 13 ft. in length while others of unrelated groups are also markedly elongate. In contrast, some of the tropical eels which inhabit the minute crevices and perforations in coral reach only a few inches at full growth, as does the little bathypelagic eel, Cyema atrum.
The eels which must surely be familiar to all are those of freshwater streams and lakes. There are two such species in New Zealand and, as has often been observed, numbers of individuals in these species are extremely high. Despite their relative abundance as individuals, the Anguillidae, to which freshwater eels belong, represents only a fraction of the whole eel group. The three much larger and systematically more complex families: Congridae (conger eels), Ophichthidae (worm eels) and Muraenidae (moray eels) make up the bulk of the eel genera and species. The two latter families are essentially tropical in distribution and are particularly characteristic of the coral reef habitat. Although the diversity of page 87 eels of these families in such places is astounding, their individual numbers are generally much less when compared with freshwater eels of the temperate regions. This is often the case with tropical fishes and other animals.
The elongate body in all members of the 20 or more eel families is an example of the essential conformity of basic body plan in the group. Freshwater eels (Anguilla) are possibly the least specialised (Fig. 1: 1). There are, nevertheless, a number of adaptations which have evolved in association with the relatively sedentary life that most eels lead. Some of the more extreme adaptations are illustrated in Fig. 1. These are less obvious to the non-specialist but serve to distinguish in part the many different genera of eels in the same family. The mesopelagic eels, which inhabit the ocean depths between surface and bottom, have their own set of adaptations and are usually delicate fishes (Fig. 1: 8).
The eel-like body form does not allow for sustained speed of movement through the water. It is, however, an admirable body shape by which eels may insinuate themselves into crevices in rock or coral or into bottom sediments, their favourite habitats. In burrowing species, like the spectacularly-coloured worm eel illustrated (Fig. 1: 2), a number of similar adaptations of external structures have appeared independently in unrelated families. For example, the nostrils (which in the most generalised eels (e.g. Anguilla) are relatively unmodified apertures on the sides of the snout), are often tube-like and may bear flaps. The posterior nostril may even move into the side of the mouth cavity (Fig. 1: 3). Presumably in this way bottom sediments are prevented from being drawn into the olfactory passages, and in addition there is the advantage of the streamlining of the profile. The nostril tubes in at least one crevice-dwelling moray, on the other hand, are markedly expanded (Fig. 1: 4), probably as enlarged sensory surfaces. In most burrowing forms the fins are usually reduced or lost so that the body has become a simple unimpeded cylinder with the tail tip hardened into a burrowing point without a caudal fin (Fig. 1: 2). The speed at which some eels can move backwards through sand with a snake-like motion must be seen to be believed.
Most eels are rapacious feeders and many display considerable enlargement of the teeth and jaws. Commonly the jaws are much elongated and the dentigerous areas increased by the forward prolongation of the snout and tooth-bearing bones (Fig. 1: 8). The mouth may also have enlarged by a backward elongation coupled with the throwing of the main jaw support (the hyomandibula) into a backwardly-oblique angle (Fig. 1: 4, 1: 5). These modifications enable very large prey to be seized and devoured.
As an example of the many adaptations in eels, a few have even become plankton feeders. The so-called “garden eels’ of the congrid sub-family Heterocongrinae are a case in point. These page 88 eels live in “colonies’ in fine coral sand, usually in reef areas where there is a relatively strong current (Fig. 1: 9). A tube is excavated in the sediment by the tail of each eel so that the animal may sink out of sight in its burrow, or hold a portion of its body out into the food-bearing current. Although eels of this type are sometimes referred to as “Röhrenaale’ (or “tube-eels’ in German), the term “garden eels’ seems to be a more expressive one. To the observer a colony of these fishes appears as a vast garden of delicately waving spindly plants, and is a sight to be remembered. The jaws of heterocongrines are much foreshortened and the large eyes are placed close to the tip of the snout (Fig. 1: 6), so that better binocular vision is possible. This would be of great advantage in feeding on the small planktonic animals as they are borne past the eel extended from its burrow. Eels of this type have recently been found for the first time in the southern Pacific on the barrier reef surrounding New Caledonia. In the deep water eel, Simenchelys parasiticus, which may spend some of its life feeding parasitically on the tissues of other fishes, the mouth is reduced and modified into an effective sucking mechanism (Fig. 1: 7).
1. Anguiflla ausfralis schmidfi (Anguillidae), the New Zealand short-finned freshwater eel — an example of a generalised eel with few specialisations.
2. Leiuranus semicincfus (Ophichthidae), a tropical sand-dwelling worm eel, showing marked elongation of the body, hard finless caudal tip and reduction of pectoral fin. The spectacular coloration shown is not uncommon in tropical eels.
3. Cirricaecula johnsoni (Ophichthidae), a tropical sand-dwelling worm eel, showing acute burrowing snout with modified nostrils and labial cirri.
4. Rhinomuraena ambonensis (Muraenidae), a tropical moray with expanded antetior nost. ils.
5. Brachysomophis crocodilinus (Ophichthidae), a tropical sand-dwelling worm eel, with marked enlargement of jaws and teeth and a labial posterior nostril.
6. Taenioconger hassi (Heterocongrinae, Congridae), a tropical sand-dwelling congrid with reduction of jaws and enlarged eyes.
7. Simenchelys parasiticus (Simenchelyldae), a deep sea eel with a mouth adapted for parasitic feeding.
8. Nemichthys scolopaceus (Nemichthyidae), a deep sea mesopelagic eel with extended jaws and filamentous caudal region.
9. A portion of a “colony’ of Taenioconger hassi (Heterocongrinae) shown burrowed in coral sand.
Abbreviations: af—anal fin, an—anterior nostril, ba—branchial aperture, c—tip of caudal region, cf—filamentous caudal region, df—dorsal fin, ej—extended jaws, fp—fleshy processes of jaws, Ic—labial cirri, pf—pectoral fin, pn—posterior nostril, v—vent.
Problems of distribution in eels perhaps involve some of the most fascinating aspects of the study of these fishes. Eels are essentially warm water fishes which have diversified extensively to fill the many niches available in the tropical habitat. Their distribution follows that of the shallow-water tropical corals, that is, approximately the 20°C isotherm, as do many other “tropical’ organisms. This means that true Indo-Pacific species would not be expected to occur as far south as New Zealand waters. However, tropical eels are known from the Kermadec and Norfolk Islands and from Queensland and the same species are likely to be found from the shores of the western Indian Ocean and as far eastwards as the offshore islands of Pacific Central America
Undoubtedly such a distribution is contributed to as much, if not more, by the ability of pelagic eel-larvae to traverse considerable oceanic distances, as by the random movement of adults from one island group to another, often across wide and very deep water gaps. The Equatorial Countercurrent in the Central Pacific, flowing eastwards towards the American coast, has been shown as an effective bridge across the so-called “East Pacific Barrier’, especially for fishes and other animals with larval forms (Briggs, 1961: 545). The spread of Indonesian species into the western Indian Ocean is very probably assisted by the west-flowing South Equatorial Current in the east and central Indian Ocean. New Zealand waters, at least those of the northern part of the North Island, are constantly under the general influence of southwestward movements of warmer waters from the Central Pacific.
Although there are no tropical eel species in New Zealand waters, there are a number of forms which show overwhelming affinities with the tropics (in particular, the muraenids and ophichthids). These are no doubt specialised offshoots of a tropical fauna which have become adapted for life in cooler waters. The distribution of eels is closely associated with the availability of suitable oceanic conditions in which spawning of the adults and development of the leptocephalid larvae may take place. It seems likely that all eels, including the temperate species, require water of moderate temperature (about 18°C) and fairly high salinity (about 35°/oo) for spawning to take place, even though the adults may normally live in much warmer or colder waters of considerably lower or higher salinities. This leads to the conclusion that the original page 91 spawning requirements of the group are being retained while certain of the adults are becoming adapted to rather different environments than were normal for their ancestors.
Temperate eels, which probably spawn in areas some considerable distance from the area of adult distribution, appears to take this trend to the extreme. The rapid fall-off in the number of eel-species in temperate regions suggests that it is only those species whose larvae can survive the movement from distant spawning areas as pelagic larvae that become established in the temperate regions as adults. For example, anguillid and congrid larvae commonly have a larval life of a year or more (up to three years in the European freshwater eel) while those of the Muraenidae and Ophichthidae (and other tropical families) are very much more short-lived in the larval stage. This may, in part, explain the relative importance of anguillid and congrid eels and the unimportant of morays and ophichthids in temperate fish faunas.
Information on New Zealand eel-larvae is fragmentary. What evidence has been assembled in recent years suggests that while some species (i.e. certain congrids) may spawn close to the coast of New Zealand in areas of suitable hydrological conditions, it seems more likely that most of them spawn either to the north, around New Caledonia and in adjacent areas, or in the Tasman Sea over the continental slope off the east Australian coast. The south-moving East Australian Current may possibly then operate to bring the developing larvae near to New Zealand where metamorphosis of the leptocephali takes place, followed by invasion of the coastal waters (shallow water marine species) as well as the river systems (freshwater species).
As already pointed out, the eel-like fishes are unique in passing through an extended, pelagic, larval phase early in their life-histories. This phase may last only a few months or may be as much as two or three years in duration. Many other unrelated groups of fishes have an extended larval phase but in none does the larva assume such a characteristic importance as it does in the eels.
Larval eels (or leptocephali, as they are sometimes known) are relatively uncommon in New Zealand waters, but they occasionally appear in whitebait nets, in fish stomachs, stranded on beaches, as well as in trawls. It seems likely that New Zealand lies beyond the main oceanic areas where leptocephali make up an important part of the planktonic community. Off the west coast of Australia, in areas of mixed oceanic waters, recent studies have shown that leptocephali contribute as much as 5% of the total number of small free-swimming organisms in the upper layers.
Despite their rarity around New Zealand, the eel-larvae that have been reported provide valuable clues to the mysteries of the early life-histories of New Zealand eels, which at the moment are page 92 entirely unknown. Further to the north, in the areas around New Caledonia, eel-larvae are extremely abundant and indicate that New Caledonia and adjacent waters are close to, or coincident with, areas where spawning and early development of many eels takes place. Obviously, very small larvae (i.e. those of about 5 mm to 10 mm in length) must indicate the close proximity of a spawning area. Quite small larvae of the New Zealand short-finned freshwater eel (Anguilla australis schmidti) have been collected in recent years in these northern waters. This suggests that, like their Atlantic counterparts, mature adults of this species and probably also those of the New Zealand long-finned eel (A. dieffenbachii) undertake a long oceanic migration to distant areas where spawning and early development is more favoured.
Even to the non-specialist, a leptocephalus shows such distinctive characters that it cannot be mistaken for any other marine creature. Fig. 2 shows a few of the diverse types of leptocephali known. The body is almost transparent and leaflike (sometimes filamentous), and the head is small with prominent eyes and sharp, conspicuous larval teeth (Fig. 2: 1, 2: 2). The segmental muscles (myomeres) of the body are characteristic. The intestine is a long straight tube (variously modified in different species) which follows the ventral margin to the posteriorly-placed anus. A large liver is present (Fig. 2: 3), together with a functional pronephros (head kidney) placed far forward near the heart. The long pronephric ducts lead to the opisthonephros (the adult functional kidney). The blood is unpigmented, as in many fish larvae.page 93
1. Leptocephalus larva of Anguilla (freshwater eel), showing the major features of a typical eel-larva.
2. Head region of same.
3. Viscera of a muraenid leptocephalus.
4. Leptocephalus of Cyema atrum (Cyemidae), a deep sea mesopelagic eel.
5. Head of a nettastomatid leptocephalus (Nettastomatidae), a deep sea mesopelagic family of eels (rostrum not completely shown).
6. Leptocephalus of same, collected off Cape Brett, New Zealand.
7. Leptocephalus of a worm eel (Ophichthidae), showing the characteristic festooned intestine.
8. Generalised growth curves for (a) noith Atlantic Anguilla, and (b) a tropical shallow water congrid (Ariosoma), both showing the essential features of growth including the reduction of length of the leptocephalus during metamorphosis.
Abbreviations: af—anal fin, b—brain, br—branchiostegal rays, da—dorsal aorta, df—dorsal fin, e—eye, gb—gall bladder, h—heart, i—intestine, im—intestinal melanophore, l—liver, lm—lateral melanophore, It—larval teeth, m—mesonephros, my—myomere (lateral muscle), n—olfactory organ, p—pronephros, pc — pyloric caecum, pd — pronephric duct, pf — pectoral fin, r—rostrum, rbv—renal blood vessel (its position along the body is of considerable importance in the identification of larvae), te—telescopic eye, v—vent, vc—vertebral column.
The leptocephalus is an active feeder on minute plankton and reaches its full growth after a time which varies from species to species. When fully grown the majority of eel-larvae are about 50 mm - 100 mm (2′ - 4′) in length but some are very much larger. The most extreme are the “giant’ leptocephali collected by the Danish Dana Expedition off southern Africa. These were as long as 1800 mm (6 ft.)! A larva similar to these was collected in a commercial trawl of South Westland some years ago. Although it was only. half as large as the largest Dana giant it was still a remarkable creature and certainly an exception amongst leptocephali.
At the completion of full growth, and under the influence of stimuli the nature of which have yet to be determined (but which may in part be external factors such as appreciable changes in temperature and/or salinity), the larva begins the remarkable process of metamorphosis. The body thickens and becomes rounded in section, pigment appears on the surface of the body, the larval teeth are lost to be replaced by the definitive teeth, and the intestine actually shortens so that the anus becomes placed further forwards along the body. What is more startling is that the body actually undergoes a reduction in length so that at completion of metamorphosis it may perhaps be only about a third as long as that of the fully grown leptocephalus. Surely this is an astounding process which must have few parallels in animal growth. Features of the life history are illustrated in Fig. 2: 8. In the European freshwater eel full larval growth is reached at about 70 mm after approximately 2 1/2 years, metamorphosis takes 3-4 months, and maturity is reached at about 700 mm after a further 5 years or so (Fig. 2: 8a). The congrid eel Ariosoma scheelei, from the tropical Indo-Pacific, grows to about 250 mm as a larva, metamorphosis is probably more rapid than in Anguilla and the elver is only about 80 mm in length; maturity is reached at about 200 mm very rapidly. This means that the leptocephalus of the species can be larger than the mature adult (Fig. 2: 8b).
The young eel is now termed an elver and has all the essential features of the adult. Subsequent growth proceeds as in other fishes. The remarkable process of metamorphosis, as outlined above, has been closely studied in certain European species and others elsewhere but similar studies have yet to be made on larvae in the Australasian region. It is not an easy process to observe in the laboratory because there are difficulties in obtaining ripe male and female eels for artificial fertilisation and rearing of the larvae produced. Even then, young larvae cannot readily be reared beyond the yolk-sac stage, while older larvae seldom survive the trawl net for transport to shipboard or laboratory aquaria.
Metamorphosis is almost certainly common to all eels, although it has been actually observed in only a relatively few species. The profound structural changes involved in this process are of page 95 considerable relevance to systematic studies on leptocephali and adult eels since they introduce into these studies a fundamental and what has been an almost insuperable problem. Many characters of the larvae do not survive this process and the young elvers are quite unlike their larvae. This means that great difficulties arise in identifying particular larvae with their appropriate adult species. In fact, although several hundred different larval forms are known, only a few have been firmly identified with adults.
Recent studies on large collections of eel-larvae, however, have shown that encouraging progress can be made in the difficult task of correlating the various larval types with their adults. The essential features which identify a particular leptocephalus with the eel family to which it belongs are now fairly well known. The characters which identify the larva to its genus have also been established for quite a number of forms. These are mainly structural, but an important breakthrough in larval studies has been made with the discovery that the broad patterns of distribution of black pigment cells (melanophores), which are commonly present in larvae, is of generic importance. In other words, generic “categories’ can be readily recognised by attention to the precise nature of larval pigmentation. This pigment often remains throughout metamorphosis to the elver, and is a useful way of linking a particular larval type with its appropriate adult genus.
Compared with the considerable structural and ecological differences which distinguished genera of eels, rather insignificant differences apply in the separation of eel species. More commonly, specific criteria in adults are those based on differences in proportions of the body, the distribution and number of teeth, the nature of the fins, coloration etc. For many years, after the outstanding researches of the Danish scientist Johannes Schmidt on the north Atlantic freshwater eels, it has been recognised that an important systematic feature of eels is the number of vertebrae they possess. This also applies in many other fishes, including sharks. The vertebral number in fishes is subject to certain variation partly resultant from variations in external factors (mainly temperature and salinity) during very early development, but such variations are usually small. Thus, eel species are often (but not always) distinguished in part by marked differences in their total numbers of vertebrae. For example, the small congrid eels of the genus Gnathophis which inhabit offshore waters around the New Zealand coast are clearly separated as two species: G. habenatus with 120-127 vertebrae, and G. incognitus with 139-147. Such differences between the two species can often be recognised externally as a marked discrepancy in the relative slenderness of the body, as would be expected when one species has more vertebrae than the other.page 96
The definitive number of segments (and hence vertebrae) is laid down early in embryonic development. It has yet to be shown that vertebrae can be added as growth proceeds, although this has been suggested as an explanation of the wide variation in vertebral numbers in eels. In the larva, vertebrae are not clearly differentiated until late in larval growth but the number of muscle segments (myomeres), which amounts to the same thing, makes its appearance early. Furthermore, the number of myomeres remains unchanged throughout the growth of the larva, through metamorphosis, and into the elver and adult. Here then, is an answer to the problem of correlating larvae with adult species.
As a practical demonstration of the usefulness of larval studies in eel systematics, a local example could be pointed out. The existence of Gnathophis incognitus in Australasian waters was first suspected after noting that gnathophid larvae from collections made in this area could be readily and effectively divided into two groups on the basis of myomere numbers, one with 116-131 (corresponding with G. habenatus), the other with 134-150 (with no known adult counterpart). A close examination of collections of adult G. habenatus revealed the presence of the second species, with matching vertebral data. Such a useful approach is now being widely explored in the study of various groups of eels elsewhere in the world.
The brief outline of the typical eel life-history given above shows that in effect it is divided into two fairly discrete portions: one involving larval growth in the planktonic habitat in the open ocean or far offshore, the other subsequent to metamorphosis as a benthic or mesopelagic adult. The transparent body of the larva favours survival in the plankton where it competes with other similarly organised animals, and much of its movement occurs passively by ocean currents. After metamorphosis, which takes a relatively short time in the life of the eel, the young elver enters a markedly different environment where body shape, differentiated feeding mechanisms, sense organs and body coloration play an important part in survival of elver and adult.
During its life then, an eel is exposed to physical and biological environmental factors which in the young differ markedly from those in the adults. Clearly, natural selection must operate in different ways in these two stages so that one might expect eel-larvae to have evolved rather differently than have their adults. We might further expect the larvae and the adults to have quite different sets of adaptations on which their classification might be based. The present classification of eels is not entirely satisfactory and perhaps a more effective scheme might be proposed in which larval features are taken more into account. If the larvae have been more conservative in their evolution than adults, they could be expected to show more accurately the generic relationships of living groups of eels page 97 and perhaps suggest a basis on which the phylogeny of the group might be established. There are parallels in other animal groups (e.g. Crustacea, Insecta, Echinodermata) where a larval phase is typical. However, a great deal more knowledge about eel-larvae is required before such proposals can be brought to a workable conclusion; in any case, it would be unwise to use only larval characters as a basis for classification and phylogeny.
This article is intended to demonstrate that the study of an isolated animal group (and here, the eels in particular) need not be one of little more than sterile academic interest. Rather, such a study is often capable of involving a wide range of biological problems. With the increased world attention to the resources of the oceans, eel-larvae are proving to be of considerable importance in studies on the complex nature of planktonic communities and the movement of oceanic water masses. Coupled with studies on adult eels, leptocephali are also providing information on the broader aspects of the distribution of marine animals, on their means of dispersal, and on fundamental problems of fish classification and evolution.
I should like to thank Professor J. L. B. Smith of Grahamstown, and Mr. J. M. Moreland, Dominion Museum, Wellington, for their criticism of the manuscript.
Briggs, J. C., 1961. The East Pacific Barrier and the distribution of marine shore fishes. Evolution, 15 (4): 545-554, 3 figs.
Greenwood, P. H., et al., 1966. Phyletic studies on teleostean fishes, with a provisional classification of living forms. Bull. Am. Mus. Nat. Hist., 131 (4): 341-455, 9 figs., 32 charts, 3 pls.