further studies on the evolution of land and freshwater nemerteans: generic relationships among the...

J . Zoo(., Lond. (1 988) 216, 1-20

Further studies on the evolution of land and freshwater nemerteans: generic relationships among the paramonostiliferous taxa

JANET MOORE Department of Zoology, Downing Street, Cambridge

AND RAY GIBSON Department of Biology, Liverpool Polytechnic, Byrom Street, Liverpool

(Accepted 8 December 1987)

(With 2 figures in the text)

Morphological characteristics of the terrestrial (Acteonemertes, Antiponemertes, Argonemertes, Katechonemertes, Leptonernertes) and freshwater (Campbelionemertes, Potamonemertes) paramonostiliferous nemerteans, all of which are at present unplaced at the family level, are compared and contrasted with those of the marine genera Plectonemertrs (Plectonemertidae), Cratenr- mertes, Korotkeuiischia and Nipponnemerfes (Cratenemerlidae). I t is concluded that whilst Acteonemertes. Antiponemertes, Argonemertes. Campbeilonemertes and Potamonemer tes can with certainty be placed in the family Plectonemertidae, the unspecialized and geographically isolated genera Katechonemertes and Leptonemertes, although lacking positive grounds for their exclusion, are only questionably included in this taxon. The possible evolutionary relationships of the plectonemertid genera are discussed and a diagnosis of the family is provided.

Contents Page

. I

3 4 4 6 I 7 8 8 9

10 11 12 14 14 18 18

Introduction.. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Morphological features distinguishing Plectonemertes and the Group 2 genera from the

Cratenemertidae . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Body wall, musculature and parenchyma . . . . . . . . . . . . . . . . . . . . Proboscisapparatus . . . . . . . . . . . . . . . . . . . . . . . . . . . . Alimentary canal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nervous system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Eyes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cephalic furrows and cerebral sensory organs . . . . . . . . . . . . . . . . . . Reproductive system . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cephalic glands and frontal organ . . . . . . . . . . . . . . . . . . . . . . Blood system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Excretory system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary of assessment of morphological features . . . . . . . . . . . . . . . .

Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diagnosis of the family Plectonemertidae . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Morphological features of Plectonemertes and the Group 2 genera . . . . . . . . . .

Introduction Nemertean taxonomists experience considerable difficulty over the allocation of genera to families. Indeed, since so many named taxa have never been adequately described, the

1 0952-8369/88/009001+20 $03'00 0 1988 The Zoological Society of London

2 JANET MOORE A N D RAY GIBSON

classification of nemerteans is uncertain at many taxonomic levels (Gibson, 1985). Recent descriptions of several new genera and species, based upon detailed and extensive histological studies, have clearly demonstrated that most of the traditionally accepted family groupings are inadequate or inappropriate. In 1955, Friedrich proposed that family names in use within the monostiliferous Hoplonemertea should be abandoned, so that more extensive modern information could be employed for regrouping genera. Recently Gibson (1982a: 828) echoed Friedrich’s sentiments in commenting that many of the monostiliferous genera ‘are only provisionally included in particular families, and familial groupings need to be revised.’

Terrestrial nemerteans, all of which belong in the class Enopla, provide one such opportunity for regrouping. Marine ancestors have colonized land on several separate occasions; Moore & Gibson (1981, 1985) recognize two major groups which have evidently evolved in parallel, each group characterized by a distinctive combination of morphological features. The first group, comprising the genera Geonemertes and Pantinonemertes, has been aligned with the recently redescribed marine genera Prosorhochmus and Prosadenoporus (Gibson & Moore, 1985; Moore & Gibson, 1988), with all four taxa now placed in the family Prosorhochmidae sensu Moore & Gibson (1988). No place has yet been found for the second group, which contains the fully terrestrial genera Antiponemertes, Argonemertes, Katechonemertes and Leptonemertes. Other taxa apparently related to these terrestrial nemerteans are Acteonemertes, a transitional upper littoral/ terrestrial form, and Campbellonemertes and Potamonemertes from fresh water (Moore & Gibson, 1972, 1973, 1981, 1985). All seven of these taxa will subsequently be referred to as the Group 2 genera, a term previously restricted to include only the terrestrial forms.

Now for the first time a fully marine taxon has been found which shares many morphological characters with the Group 2 genera: Gibson (In press) describes a new genus from Hong Kong, Plectonemertes, with features which exclude it from any known hoplonemertean family. He accordingly establishes for this form a new family, Plectonemertidae. One of the most distinctive characters of Plectonemertes, to which it owes its name, is that the rhynchocoelic musculature is organized into a single wickerwork coat of interwoven circular and longitudinal fibres rather than forming separate circular and longitudinal layers as in most Hoplonemertea. The only other monostiliferous genera known which possess this type of arrangement are Cratenemertes, Korotkevitschia and Nipponnemertes, united in the family Cratenemertidae, and the Group 2 forms mentioned above.

The occurrence of a wickerwork rhynchocoelic musculature in a small number of monostiliferous genera can be explained in one of two ways. Either it is a synapomorphic feature, representing an important shared derived character state, or it has a more fundamental significance and is plesiomorphic for a whole group. Gibson (1988), who supports the second hypothesis, argued that a distinction between a wickerwork and a bilayered rhynchocoelic musculature constitutes a major taxonomic feature. He used this as a basis for dividing the class Enopla into two new orders, the Distromatorhynchocoela with a bilayered rhynchocoel muscle plan and the Urichorhynchocoela with a wickerwork arrangement. Gibson accordingly separated the family Cratenemertidae from the remaining enoplans in which the proboscis consists of a single central stylet borne on a cylindrical basis. He developed Stricker’s (1 985) hypothesis on the evolution of the monostiliferous type of proboscis stylet, postulating that the armature in the cratenemertid genera has evolved in parallel with that found in the remaining Monostilifera rather than sharing an immediate ancestry. In his proposed reclassification of the Enopla, Gibson (1988) divided the Urichorhyn- chocoela on ecological grounds into two suborders, the Pelagonemertoidea and the Herponemer- toidea. He placed the Cratenemertidae in a new tribe, the Paramonostilifera, within the

LAND A N D FRESHWATER PARAMONOSTILIFERA 3

Herponemertoidea. The Group 2 genera, which possess a wickerwork rhynchocoelic musculature and a monostiliferous type of proboscis armature, therefore belong in the Paramonostilifera rather than with enoplans in which the rhynochocoel muscles are organized into two discrete layers.

It has already been noted that Plectonemertes and the Group 2 taxa share many features in conimon. The purpose of the present paper is to determine the familial placing of the Group 2 genera by comparing and contrasting their morphological characters with those of Plectone- mrrtes. Gibson (In press) distinguished the Plectonemertidae from the Cratenemertidae primarily through differences in the size and position of the cerebral sensory organs and organization of the blood system, and we first exclude the cratenemertid genera, on the basis of major anatomical differences, from further comparison with the Group 2 taxa. We then examine the morphology of the remaining taxa in detail, so that those features which may be of significance in resolving familial relationships within the Paramonostilifera can be identified and discussed. The nature of these characters within the Group 2 genera is then assessed for the purpose of establishing whether the taxa should be included in the family Plectonemertidae or separated into one or more families on their own.

Many of the older established nemertean genera and species were described with no reference to their internal morphology other than to features, such as the proboscis, brain and intestinal diverticula, which could be distinguished through their body surface. The classification of the phylum, however, has for long been based upon studies of their anatomy involving light microscope histological preparations. More recent ultrastructural investigations (e.g. Gontchar- off, 1957; Gontcharoff & Lechenault, 1966; Pedersen, 1968; Jennings, 1969; Vernet, 1970; Anadbn, 1974,1976; Oaks, 1978; Stricker & Cloney, 1982; Stricker, 1983,1985; Turbeville & Ruppert, 1983, 1985; Norenburg, 1985; Jespersen, 1987a, b; Jespersen & Lutzen, 1987), whilst providing much invaluable new information on aspects of nemertean structure, have inevitably been concerned with comparatively few taxa, and hardly any of these data refer to paramonostiliferous species. Accordingly, our discussion of the morphology of Plectonemertes, the Group 2 genera and the Cratenemertidae is predominantly dependent upon information derived from light, rather than electron, microscopy.

Morphological features distinguishing Plectonemertes and the Group 2 genera from the Cratenemer- tidae

Two major differences between Plectonemertes and the three cratenemertid genera are the number of vascular plugs borne on the mid-dorsal blood vessel or its branches, and the size and position of the cerebral sensory organs relative to the brain lobes; Gibson (In press) concluded that these differences, in combination with other anatomical features, were sufficient to exclude the Hong Kong species from the family Cratenemertidae and justified its placement in a new higher taxon. Table I shows that all the Group 2 genera are also consistently different from the cratenemertid taxa in these features; further, they also differ in the development of their excretory systems throughout most or all of the body length, and in lacking a diagonal muscle layer from the body wall, two additional characters shared with Plectonemertes. This combination of morphological features both supports Gibson’s establishment of the family Plectonemertidae and indicates that the Group 2 genera do not belong with the Cratenemertidae. Other differences which can also be distinguished between the Group 2 genera and individual members of the Cratenemertidae, such as the separation of the mouth and proboscis pore in Korotkevitschia and

4 JANET MOORE AND RAY GIBSON

TABLE I Morphological differences which enable PIectonemertes and the Group 2 taxa to be distinguished from the genera belonging to

the family Cratenemertidae ~~

Cratenemertidae Plecto- Group 2 genera ~- nemer- tidae

m

Number of vascular plugs 1 Excretory system absent or restricted to

foregut region (0) or extending throughout most or all of body length ( + I 0

Cerebral sensory organs below/posterior to brain lobes (0) or situated in front of cerebral ganglia (+) 0

without (0) diagonal layer + Body wall musculature with (+) or

_ _ _ 1 1 2 2 2 2 2 2 2 2

o o + + + + + + + +

o o + + + + + + + +

+ + " 0 0 0 0 0 0 0 0

Compiled from Biirger(l890), Coe(1905), Wheeler (1940), Korotkevitsch (1961,1983), Kirsteuer (1965), Pantin (1969), Moore & Gibson (1972, 1973, 1981), Berg (1972, 1985) and Moore (1973, 1975). "resent in N. punctatulus (Coe, 1905), several undescribed Antarctic species (R. Gibson, unpubl. obs.) and probably

N. pulcher (Johnston, 1837), but apparently missing from N. africanus (Wheeler, 1940) and N . madugascarensis (Kirsteuer, 1965).

Cratenemertes vuriubilis Korotkevitsch, 1983 (Korotkevitsch, 1961,1983), reinforce the exclusion of the family Cratenemertidae from further comparison with the remaining paramonostiliferous genera.

Morphological features of Plectonemertes and the Group 2 genera

In the following section the various morphological characters of Plectonemertes and the Group 2 genera are discussed in turn and their potential significance in higher taxonomy is assessed.

Body wall, musculature and parenchyma

In his review of the ultrastructure of the nemertean integument, Norenburg (1985: 37) concluded that 'The general construction and cell demography of the integument are more or less characteristic for each order, but are not readily generalized to lower taxonomic levels.' Although Norenburg did not investigate any paramonostiliferous species, the present light microscope studies on Plectonemertes and the Group 2 taxa support his interpretation and do not indicate any features of significance to the arrangement of genera into families.

The organization of the body wall muscle layers into outer circular and inner longitudinal coats is a fundamental feature of all enoplans. The degree of development of these muscles, however, varies considerably according to the size and way of life of the species concerned. The thickness of

‘I I

S VXI3dI7IISONOVJVXVd VFIIVMHS3Xd CINV aNV7

FIG. 1, Schematic diagrams showing the various relationships between the body wall longitudinal musculature, proboscis insertion and pre-cerebral septum. (a) Body wall longitudinal musculature divided, no pre-cerebral septum present. (b) Body wall longitudinal musculature divided, pre-cerebral septum split. (c) Body wall longitudinal musculature not divided, pre-cerebral septum closed. Abbreviations: CG, cerebral ganglion; CM, circular muscle layer of body wall; DE, dermis; EP, epidermis; IL; inner longitudinal muscle layer; LM, longitudinal muscle layer of body wall; OL, outer longitudinal muscle layer; PI, proboscis insertion, PP, proboscis pore; PR, proboscis; PS, pre-cerebral septum; RD, rhynchodaeum.

the muscle layers, either as a direct linear measurement or as a ratio between them, is also highly variable intraspecifically and, in histological sections, depends largely upon the degree of contraction or elongation at the time of fixation. This is also true for the epidermis and dermis (Berg, 1972). Although it is possible to distinguish subjectively between, for example, the strongly developed musculature of Camybellonemertes (Moore & Gibson, 1972) and the much weaker muscle layers in Leptonemertes (Moore & Gibson, 198 l), such differences cannot be used as a basis for uniting or separating genera at higher taxonomic levels.

One further feature of the muscle system requires discussion; this is the nature of the pre- cerebral septum, established by Kirsteuer (1 974) as a generic character amongst enoplans which possess an anteriorly divided body wall longitudinal musculature. Various grades of pre-cerebral septum can be defined; these are a closed septum, which may or may not be dissolved into discrete bundles of radial muscle fibres, a split septum, and no septum (Fig. 1). Their distinction rests on the origin of the muscle fibres leading to the proboscis insertion in relation to those of the body wall longitudinal musculature. Most of the Group 2 genera have either no septum or one of the closed type, In Antiponemertes and Argonemertes, however, the situation is complicated by the fact that the level at which the bundles of fibres leading to the proboscis insertion emerge from the body wall longitudinal muscle layer may vary according to both the size of the individual concerned and the side of the body examined. In these taxa it is thus not possible clearly to distinguish between a closed and no pre-cerebral septum, and various intermediate conditions can be identified. This degree of intrageneric variation amongst the Group 2 taxa indicates that the nature of the pre- cerebral septum cannot be used in an assessment of their intergeneric relationships.

The amount of parenchyma varies both intragenerically and within an individual and is at least partly dependent upon the state of development of the gonads. Parenchymal extent thus appears to have no systematic significance at the familial level.


TABLE I1 Some features of the proboscis apparatus in Plectonemertes and the Group 2 genera

Rhynchocoel full body

Proboscis length (+) or short (0)

large ( + ) or small (0) relative to body employed in locomotion (+) or not so used (0) nerve numbera circular muscle fibres enclosed by connective tissue (+) or forming distinct layer (0) central bulb region with (+) or without (0) broad duct containing acidophilic cells

0 +

0 0

O? + 12 15-18

0 0

0 +

+

+ +

10-21

0

0

+ + + +

+ 0 + 0

+ ? ? 0 11-21 12 19 12-13

0 + 0 0

0 + 0 0

+

+ +

11-12

0

0

Compiled from Pantin (1961,1969), Moore & Gibson (1972,1973,1981,1985), Moore (1973,1975), Gibson (In

‘Variations in nerve number probably depend upon the number of specimens examined press) and the present studies

Proboscis apparatus

The proboscis apparatus of nemerteans includes the rhynchodaeum, rhynchocoel and proboscis itself. Fundamental characters shared by all the Paramonostilifera are the development of a wickerwork rhynchocoelic musculature and a monostiliferous type of proboscis armature, as discussed in the Introduction. Certain differences, however, are evident between the various taxa.

The rhynchocoel itself in all the Group 2 genera extends to, or almost to, the posterior end of the body (Table 11). In contrast, it reaches only just beyond half the body length in Plectonemertes (Gibson, In press). Amongst monostiliferoidean nemerteans, rhynchocoel length is widely used as a generic character (Friedrich, 1955), but its value in defining higher taxonomic categories is dubious. For example, the family Emplectonematidae ‘usually includes slender-bodied hoplonemerteans in which the rhynchocoel is less than about three-quarters of the body length’ (Gibson, 1982a: 829), yet the various genera contained in this taxon are in other ways very different from each other. The difference in rhynchocoel length between Plectonemertes and the Group 2 taxa therefore cannot be regarded as necessarily significant above the generic level.

Proboscis size varies considerably in the different genera (Table 11); in the terrestrial forms of both Group 1 (the prosorhochmid Monostiliferoidea) and Group 2 it tends to be large and well developed and, commensurate with its size, is in most species used for a particular type of ‘escape’

LAND A N D FRESHWATER PARAMONOSTILlFERA 7

TABLE 111

Characters of the alimentary tract in Plectonemertes and rhe Group 2 genera; see Table II for sources of data

Oesophagus present, ciliated (+) or unciliated (0) 0 0 0 0 0 0 0 + or always in normal position (0) 0 + + 0 0 0 0 0

diverticula (+) or only with lateral pouches (0) 0 + + + + + + + or variable (V) - + v V + + + +

Stomach region sometimes pushed forwards (+)

Intestinal caecum with lateral and anterior

Anterior diverticula of intestinal caecum long (+)

locomotion (Moore & Gibson, 1981, 1985). One of the freshwater taxa included in Group 2 (Potamonemertes) is also known to employ its proboscis in a similar fashion (Moore & Gibson, 1973), as does the marine monostiliferoidean Divaneiia (Gibson, 1973). Acteonemerfes, however, has only a small-sized proboscis yet is still able to use it for rapid movement. Proboscis size and function appear to be related to the species’ way of life rather than to its taxonomic position. The different species of the Group 1 genus Pantinonemertes support this conclusion, for whereas the terrestrial or supralittoral forms use their proboscis for rapid movement, the fully marine species do not.

Other features of the proboscis apparatus which have been recorded (Table 11) may be of specific importance but appear to have no value in determining generic relationships.

Alimentary canal

The available data on enoplan gut morphology indicate that differences in structure may vary intraspecifically according to the preservation procedures employed, may be related to the ecological habitat occupied or, as in the Cratenemertidae, depend upon the genus concerned. The conclusion at present must be that no character of the alimentary system which has been described for Plectonemertes and the Group 2 genera (Table 111) can be used in any determination of familial relationships.

Nervous system

Friedrich (1 959, in his key to the genera of monostiliferous hoplonemerteans, included several features of the nervous system as major characters. These were:

1. Whether or not the lateral nerve cords contained one or two fibrous cores, i.e. whether only the ventral cerebral lobes contributed to the single longitudinal bundle of nerve fibres, or whether a second bundle, derived from the dorsal ganglionic lobes and forming an accessory lateral nerve, was present;


TABLE IV Features of rhe nervous system in Plectonemertes and the Group 2 genera; see Table II for sources of data

Y

Accessory lateral nerves present (+) or absent (0) 0 0 0 - + + 0 0 + 0

contribution from dorsal cerebral ganglia 0 + 0 0 0 0 0 0

posterior (P) ar no (0) projections 0 D 0 0 0 0 0 P

developed (+) or normal (0) + 0 0 0 0 0 0 0

Lateral nerve cords with (+) or without (0)

Ventral cerebral commissure with dorsal (D),

Peripheral nervous system unusually well

2. Whether or not the accessory lateral nerves, when present, were restricted to the anterior

3. Whether or not the nervous system contained neurochords and neurochord cells; 4. Whether or not the dorsal cerebral lobes were posteriorly bifurcated. Neither PZectonemertes nor any of the Group 2 taxa possesses neurochords, neurochord cells or

bifurcating dorsal cerebral lobes, and the presence or absence of accessory lateral nerves can vary within a genus. The only conclusion at present must be that neither these nor other defined features of the nervous system (Table IV) can be used in the determination of intergeneric relationships.

region of the body;

Eyes

Within the Enopla, the primitive number of eyes is four (Norenburg, 1986) and, with occasional minor variations (Moore, 1973), this condition is typical of most of the Group 2 genera. A few taxa, however, show major deviations from this number. Thus many freshwater genera, including Campbellonemertes and Potamonemertes amongst the Group 2 forms (Moore & Gibson, 1972, 1973), do not possess eyes, whilst at the other extreme there is the mass multiplication in eye number found in Argonemertes (Hickman, 1963; Moore & Gibson, 1985) and, to a lesser extent, Plectonemertes (Gibson, In press). There are so many variations in eye number, distribution and occurrence amongst nemerteans in general (Gibson, 1972) that it is at present impossible to assess their significance, if any, in the higher taxonomy of the group.

Cephalic furrows and cerebral sensory organs

Cephalic furrows of one form or another are very characteristic of the Enopla (Gibson, 1972) and amongst aquatic taxa typically are lateral with a longitudinal or oblique orientation. Plectonemertes and the freshwater genera of Group 2 possess lateral or ventrolateral furrows (Moore & Gibson, 1972, 1973; Gibson, In press) into which the cerebral sensory organs open;

LAND AND FRESHWATER PARAMONOSTILIFERA 9

TABLE V Features of the cephalic,furrows and cerebral sensory organs in Plectonemertes and the Group Zgenera; see Table IIfor sources

of data

d

~ _ _ _ _ _ _ _ _ __- - ~ _ _ _ _ _ _ _ _ _ ~ -~ -- _ _ _ _ ~ _ Cephdlic furrow5 lateral, horizontal and

Cerebral sensory organs longitudinal (L) or ventral and transverse (V) L V V v L' v V L

large with a branching canal, anterior sac and posterior gland (+), small and simple (0) or

open ventrally (V), laterally (L) or * unique with two glandular regions (*) 0 0 + + 0 0 0

ventrolaterally (VL) VL v V V L V V L

' Campbellonemertes possesses two pairs of longitudinal furrows arranged in tandem, the cerebral organs open from the hind pair (Moore & Gibson, 1972)

Cumphellonemertes is unusual in having two pairs of furrows in tandem, the cerebral organs in this taxon opening into the posterior pair (Moore & Gibson, 1972). Not surprisingly in the land- dwelling taxa, the lateral furrows are replaced by a single transverse ventral furrow, with the result that the cerebral organs in these forms open ventrally rather than laterally or ventrolaterally (Table V). These differences in cephalic furrow pattern are evidently related to the adoption of terrestrial habits and are thus of no value in determining generic affiliations.

Most nemerteans possess cerebral sensory organs. In the Group 2 genera, they are always situated in front of, rather than as in the cratenemertid taxa alongside or behind, the cerebral ganglia, but their degree of development is enormously variable and, in general, the more specialized a species is for life on land, the more elaborate are its cerebral organs (Moore & Gibson, 1985) (Table V). In contrast, the cerebral organs of freshwater taxa do not usually appear to be significantly more complex than those of marine species, so that in both Plectonemertes and Potamonemertes the structures are small and comparatively simple (Moore & Gibson, 1973; Gibson, In press). Campbellonemertes is an exception, for it possesses large, well developed cerebral organs with a unique construction in which two distinct glandular regions can be recognized (Moore & Gibson, 1972). Moore & Gibson (1985: 280) comment that if the Group 2 freshwater genera 'are indeed derived from terrestrial ancestors such an anomaly [in the size and complexity of the cerebral organs] is perhaps less surprising.' Theclear correlation between habitat and cerebral organ elaboration within the Group 2 genera, however, indicates that their form cannot be used in assessing higher taxonomic affinities.

Reproductive system

Most nemerteans are oviparous and dioecious, with gonads arranged singly or in small groups throughout the intestinal region (Gibson, 1972). Variations from this generalized condition

10 JANET MOORE AND R A Y GIBSON

include hermaphrodity, ovoviviparity, multiplication of gonad number and differential distribution of testes and ovaries; the latter condition is found in Potamonernertes amongst the Group 2 freshwater forms.

All the taxa under consideration appear to be oviparous and most are dioecious, although where very few specimens of a species have been found their possession of separate sexes and oviparity cannot be confirmed. The reproductive strategy of Leptonemertes is uncertain because all 64 specimens which have been examined are female. Hermaphrodity occurs in all known freshwater enoplans, including Campbellonemertes and Potamonemertes (Moore & Gibson, 1972, 1973). It may also have considerable advantages for terrestrial nemerteans (Moore, 1985) and occurs in one species of Argonemertes. All of these hermaphroditic species show evidence of protandry.

Clearly, since hermaphrodity may have an adaptive significance, and does vary intragenerically, it has no taxonomic value in the grouping of genera. More generally, the degree of variation between the repioductive strategies of the different species makes it very unlikely that any features of their reproductive system are significant in the higher classification of nemerteans.

Cephalic glands and frontal organ

The degree of development of the cephalic glands in marine nemerteans is extremely variable, but no doubt as a consequence of the need for copious mucus secretion on land, cephalic glands in all known terrestrial nemerteans are very extensively developed and reach a considerable distance behind the cerebral ganglia (Pantin, 1969; Moore & Gibson, 1981, 1985). Similarly extensive glands are also found in Plectonemertes (Gibson, In press) and Campbellonemertes (Moore & Gibson, 1972); their role in aquatic habitats is presumably less important for the secretion of mucus than on land and this reduction in significance is reflected in the other freshwater genus, Potamonemertes, where the glands are confined to a small anterodorsal cap of cells near the tip of the head (Moore & Gibson, 1973).

Moore & Gibson (1985) distinguish three principal types of cephalic glands in terrestrial nemerteans and their relatives. These are: typical basophilic lobules, similar to those found in most marine nemerteans as well as in freshwater species, which stain positively with methods for the demonstration of acid mucopolysaccharides; acidophilic cells containing large prominent nuclei, embedded in and sometimes largely replacing the basophilic lobules; and coarsely granular glands, characteristically staining orange, yellow or brown with Mallory trichrome, which may surround and invade the basophilic tissues and are apparently proteinaceous. Basophilic glands are to some extent present in all land nemerteans (Moore & Gibson, 1985) and are also found in Plectonemertes (Gibson, In press) and the Group 2 freshwater genera (Moore & Gibson, 1972, 1973) (Table VI). In contrast, the acidophilic and proteinaceous types of cephalic glands are sporadically distributed among terrestrial species. Orange-staining proteinaceous glands are also present in the prosorhochmid genera Pantinonemertes (Moore & Gibson, 198 I ) , Prosorhochmus (Gibson &Moore, 1985) and Prosadenoporus (Moore & Gibson, 1988) but have never been seen in the fourth member of the family, the genus Geonemertes (Moore & Gibson, 1985). A fourth type of gland, comprising strongly acidophilic cells whose function is unknown, forms the ‘dorsal gland cells’ characteristic of all species of Argonemertes (Moore & Gibson, 1985).

In nemerteans the cephalic glands characteristically discharge through the frontal sensory organ. A feature of the Group 2 genera, however, is that they have lost their frontal organ and the cephalic glands instead open to the exterior via large numbers of improvised pores (Moore & Gibson, 1981, 1985); a notable exception to this rule is the freshwater taxon Potamonemertes,


TABLE VI Characters relating to the frontal organ and cephalic glands of Plectonemertes and the Group Zgenera; see Table IIfor sources

of data

Frontal organ present (+) or absent (0) + 0 0 0 0 0 0 + Cephalic glands

confined to pre-cerebral region (0) + + + + 0 + + 0 extensive and reaching behind brain (+) or

discharging only via numerous improvised pores (+ +), by single median pore separate from frontal organ (+), or through frontal organ supplemented by improvised ducts (0) 0 + + + + + + + + + + + + + basophilic lobules extensive (+) or largely

dorsal acidophilic head glands present (+) or replaced by acidophilic glands (0) + + + + + + 0 + absent (0) 0 0 0 + 0 0 0 0

where a frontal organ is present although the basophilic glands open through a separate median pore situated just above this organ (Moore & Gibson, 1973). Plectonemertes also possesses a small frontal organ, the basophilic lobules opening through this but having their discharge supplemented by large numbers of independent ducts scattered over the dorsal and dorsolateral surfaces of the head (Gibson, In press); similar improvised openings supplementary to the principal route through the frontal organ have also been found in species of Geonemertes and Pantinonemertes (Moore & Gibson, 1981). Although the need for copious mucus secretion in land habitats could well account for the multiplication of independent pores amongst the terrestrial taxa, and is indeed the only route once the frontal organ has been lost, the presence of similar ducts in a marine form is very unusual and may be indicative of taxonomic affinities between Plectonemertes and the Group 2 genera.

Blood system

The basic plan of the enoplan blood system is of three longitudinal vessels (single mid-dorsal and paired lateral), often linked by pseudometameric transverse connectives throughout the intestinal region (Gibson, 1972). Valves are a characteristic feature of these vessels but are mostly absent from taxa in which distinct vessels are replaced by lacunae. In the head there is typically a simple vascular loop whose cephalic vessels or lacunae, in the cerebral region, join directly with the lateral vessels.

Amongst the Group 2 genera, Camphellonemertes and Potamonemertes possess lacuna-like lateral vessels (Table VII) which lack cross connectives between the anterior and posterior ends of the body; this latter feature is shared by all freshwater nemerteans (Gibson & Moore, 1976; Moore


TABLE VII The organization of the blood system in Plectonemertes and the Group 2 genera: see Table Ufor sources of data

w

Blood vessels distinct (+) or lacunar (0) + + + + 0 + + 0 transverse connections between brain and posterior end of body present (+) or absent (0) 0 + + + 0 + + 0 capillary network present throughout body (+ +). in foregut region only (+) or absent (0) + + + + + + + 0 0 0 0 valves numerous (+) or rare (0) + + + + + + + 0 cephalic system a simple loop (+) or a capillary network (0) + 0 0-+ 0-+ + t + +

Two vascular plugs situated either on anterior projections of mid-dorsal blood vessel (D) or on posterior portions of cephalic vessels, which do not join (C) C D D D C D D C

& Gibson, 1985), and is also found in Plectonemertes (Gibson, In press). Except in Katechone- mertes and Leptonemertes, which possess typical pseudometameric transverse vessels, distinct transverse connectives in all the terrestrial genera are replaced by a complex subdermal capillary network which, in Acteonenzertes and some species of Antiponemertes and Argonernertes, may also substitute for the cephalic vascular loop (Pantin, 1969; Moore, 1973, 1975). Plectonemertes also possesses a capillary arrangement (Table VII), but in this form it is confined to the foregut region of the body (Gibson, In press). In the taxa possessing a specialized capillary network, its branches are nearly always closely associated with the excretory tubules. Because of its unusual nature, the presence of a capillary system may be of higher systematic significance.

An unusual feature shared by Plectonemertes and the seven Group 2 genera is the presence of two vascular plugs projecting into the rhynchocoel, borne either on the posterior portions of the cephalic vessels where these pass through the cerebral ring or on anterior branches of the mid- dorsal vessel (Table VII). Most enoplans, including the Cratenemertidae, the monostiliferoidean family Prosorhochmidae and the freshwater tetrastemmid genus Prostoma, have only a single vascular plug projecting into the rhynchocoel from the mid-dorsal vessel (Berg, 1972; Gibson & Moore, 1976; Moore & Gibson, 1988). Apart from Plectonemertes and the Group 2 genera, the occurrence of two vascular plugs is known only from Oerstedia (P. Sundberg, pers. comm.) and may thus be of higher taxonomic value.

Excretory system

All terrestrial and freshwater enoplans have outstandingly well developed excretory systems which extend throughout the body, with large numbers of flame cells and subdivision of the


TABLE VIlI Some characters of the excretory system in Plectonemertes and the Group 2 genera: see Table I I for sources of data

Excretory system very extensive with numerous flame cells (+) or moderately extensive with many flame cells (0) 0 + + + 0 + 0 0

Nephridiopores exceptionally multiplied (+ ) or numerous (0) 0 + + + 0 0 0 +

Excretory tubules extend pre-cerebrally (+ ) or confined to post-cerebral regions of body (0) 0 + + + + + + +

Terminal portion of tubules specialized with thick walls and microvilli (+) or not modified (0) 0 0 + + 0 0 0 +

Excretory ducts wide and vacuolate (+) or normal (0) 0 0 0 0 + 0 0 0

Flame cells aggregated around lateral blood vessels (+) or scattered throughout parenchyma (0) 0 0 0 0 0 + 0 0

excretory ducts to open by varying (often very large) numbers of pores (Moore & Gibson, 1985). This condition is strikingly different from the almost universal state in marine taxa, where the excretory tubules are restricted to the foregut portion of the body and typically open via a single or a few pairs of nephridiopores. The extensive development found in land and freshwater species appears to be a necessary adaptation to the osmotic gradients encountered in rivers and streams or flooded situations on land. Relationships may be revealed when the same physiological problem is resolved in different ways. What may vary is the structure of the flame cells and the degree of specialization of the excretory ducts. Group 1 terrestrial nemerteans (Geonemertes, Punfinone- mrrtes) have highly specialized flame cells, fused in pairs and reinforced with cuticular support bars (Moore & Gibson, 1981; Gibson, Moore & Crandall, 1982). Group 2 terrestrial taxa (indeed all seven genera contained in this assemblage) have flame cells of a more primitive kind in that they are simple mononucleate structures without cuticular reinforcement, usually prominent and numerous in the parenchyma throughout the body. There may be many thousands of excretory pores, and the terminal regions of the excretory tubules in Anfiponemertes, Argonemertes and also Potumonemertes are particularly thick-walled with unique specializations (Moore & Gibson, 1973, 1981, 1985) (Table VIII). Plectonemertes, although a fully marine form, also possesses an unusually well developed excretory system, extending throughout the post-cerebral portion of the body and provided with numerous mononucleate flame cells which lack support bars, and opening via several nephridiopores (Gibson, In press). A comparably well developed and extensive excretory system, whilst very unusual amongst marine taxa, is present in the marine relatives of the Group 1 terrestrial genus Puntinonemertes and in the brackish-water and salt-marsh inhabiting form Cyunophthufmu (Moore & Gibson, 1981; Gibson, 19823, In press; Norenburg, 1986); Norenburg (1986) suggests that C~yanophthalma appears more closely related to the Amphiporidae


TABLE IX Summary of the principal morphological characters used in assessing intergeneric relationships between Plectonernertes and

the Group 2 taxa

Blood system number of vascular plugs 2 2 2 2 2 2 2 2

or absent (0) + + + + 0 0 0 0

or through frontal organ (0) + O + + + + + + + largely replaced by acidophilic cells (0) + + + + + + 0 +

development of capillary network, present (+)

Cephalic glands open independently (+)

predominantly basophilic (+) or basophils

Excretory system extending throughout length of body (+ +) or only through post-cerebral regions (+), in both instances with pore multiplication + ++ ++ ++ ++ ++ ++ ++

or Tetrastemmidae than to any other monostiliferoidean family. The significant point, however, is that an extremely well developed excretory system extending throughout most of the body length in a fully marine species does appear to be an important factor in any consideration of generic relationships.

Summary of assessment of morphological features

Most of the morphological features discussed and tabulated above are so variable within either species or genera that they afford no useful comparisons at higher systematic levels. The organization of the cephalic glands, blood system and excretory system, however, provides a number of characters shared by many or all of the genera (Table IX). That these are systems concerned with water relations has particular significance to the grouping of genera which include both freshwater and terrestrial taxa.

Discussion

Land and freshwater nemerteans have undoubtedly evolved from marine ancestors, and there is abundant evidence for many phyla, both invertebrate and chordate, that the concept of pre- adaptation may help us to identify the origins of such habitat transitions. For marine nemerteans to colonize fresh water or land must involve the evolution of efficient mechanisms to cope with the

L A N D A N D FRESHWATER PARAMONOSTILIFERA 15

major problem of water relations, and Moore & Gibson’s (1985) review indicates that the cephalic glands, blood and excretory systems are of paramount significance to the solution of this physiological problem. Ferraris (1 985) concluded that eulittoral nemertean species were able to survive osmotic stress through the neuroendocrine control, either directly or mediated via the blood system, of the nephridia and cephalic glands. Although there are no comparable physiological data for terrestrial or freshwater species, it is nevertheless possible to combine Ferraris’ findings with the morphological evidence as a basis for speculation on the likely sequence of evolutionary events which led to the colonization of land and freshwater habitats.

First, an increased development of the excretory system appears to be a fundamental requirement in any evolutionary lineage leading towards the colonization of land. Intertidal species, for at least some of their life, are exposed to the risks of desiccation or dilution and perhaps the greater extremes of temperature and seasonality in rainfall associated with tropical or subtropical regions impose greater evolutionary pressures on such forms. That the intertidal members of the Group 1 genus Puntinonemertes, all of which possess an extremely well developed excretory system, are found only on tropical shores (Australia and Hong Kong) (Moore & Gibson, 1981; Gibson, 1982b, In press) provides circumstantial evidence in support of this hypothesis. Unique specializations of the flame cells, which are fused in pairs and provided with cuticular support bars, provide a major character uniting the Group 1 genera Geonemertes and Puntinonemertes (Moore & Gibson, 1981). The presence of such specialized flame cells in marine intertidal species of Puntinonemertes can therefore be interpreted as an example of pre-adaptation.

The blood system is closely associated with the excretory system in all land nemerteans in that flame cells and excretory ducts are found wherever blood vessels occur in the parenchyma. The blood system itself is always well developed, with some form of cross-connections between the main lateral vessels. The striking specialization found in some Group 2 genera is the evolution of a capillary network, which may possibly allow an improved physiological control under conditions of water stress. A capillary network is characteristic of Antiponemertes and Argonemertes (Moore & Gibson, 1981, 1985); that it also occurs in the transitional genus Acteonemertes (Pantin, 1969) and to some extent in the fully marine taxon Plectonemertes (Gibson, In press) indicates a taxonomic relationship between these forms.

A further important aspect of the blood system is the presence of vascular plugs projecting into the rhynchocoel. All the Group 1 land nemerteans, together with their related marine genera Prosudenoporus and Prosorhochmus (Moore & Gibson, 1981, 1988; Gibson & Moore, 1985), resemble most other monostiliferoideans in having a single vascular plug, whereas the Group 2 genera and Pkctonemertes possess two (Moore & Gibson, 1981; Gibson, In press). The possession of two vascular plugs appears to be a more specialized character, known only in Oerstediu (a monostiliferoidean), Plectonemertes and the seven Group 2 genera.

Cephalic glands are extensively developed in all terrestrial nemerteans. The variable architec- ture of the components of mucus makes it essential for locomotion and as a potential barrier against excessive water loss. Cephalic glands discharge either through a frontal organ or via numerous improvised pores, or both. The Group 1 genera, like many marine species, all possess a frontal organ but often have improvised pores in addition. This is the condition in Plectonemertes (Gibson, In press), but in all terrestrial Group 2 genera (Moore & Gibson, 1981, 1985) the frontal organ has been lost and improvised openings are the only outlet. Discharge via a large number of pores distributed over the body surface almost certainly represents a more highly evolved condition; out of water a frontal organ ceases to have a useful sensory function, and its loss from the Group 2 land nemerteans is thus readily explained. The functional significance of the various


-1 Adaptations to freshwater: reduction in blood system and cephalic glands; loss of eyes; development of hermaohroditism

[TERRESTRIAL 1

I TRANSITIONAL UPPER 11

s

Potamonemertes

Argonemertes Antiponemertes

Campbellonemertes

I

/ I

Acteonemertes I

'I..' I

\3 /7 \ /

Retention of primitive eye number Plectonemertes \ /

ANCESTRAL FORM Two vascular plugs Excretory system extensive but not specialized Tendency to reduce frontal organ and for cephalic glands to develop improvised pores Primitive eye number of four

FIG. 2. The suggested evolutionary relationships between terrestrial, freshwater and marine paramonostiliferous genera now certainly included in the family Plectonemertidae. Because of the uncertainty regarding both their placement in this family and relationship with the taxa indicated, the genera Katechonemertes and Leptonemertes are omitted from the Figure.

L A N D AND FRESHWATER PARAMONOSTILIFERA 17

types of cephalic glands is not at present understood, but it is possibly of taxonomic importance that the proteinaceous type is found only in the Group 1 genera and their marine relatives, and that the type of glands found in Leptonemertes is unique to this form. What is certain is that unusually extensive cephalic glands are essential for any species colonizing land.

The separation of terrestrial nemerteans into two groups rests largely on those characters concerned with water relations. Moore & Gibson (1985: table 11, p. 268) united the genera Acteonemertes, Antiponemertes, Argonemertes, Katechonemertes and Leptonemertes as the Group 2 terrestrial taxa on the grounds that, in all, the flame cells are simple and not reinforced, there is no frontal organ, there are two vascular plugs and the rhynchocoel musculature is developed as a wickerwork. At the time the wickerwork rhynchocoel musculature was seen as a synapomorphic character strongly uniting these forms. As explained in the Introduction, it has now become the basis for a major taxonomic division of the Enopla (Gibson, 1988). On either view, the two groups of terrestrial nemerteans are firmly separated. Subsequently, Moore & Gibson (1988) placed the Group 1 genera in the family Prosorhochmidae and commented that the familial placing of the Group 2 taxa was entirely obscure, and indeed that this group may not be homogeneous. The recent finding of Plectonemertes, and its placement in a new family, the Plectonemertidae (Gibson, In press), is most significant because this genus shares many of the major features used to define the Group 2 taxa (Table I). This does not necessarily indicate, however, that all the Group 2 genera should be placed in the family Plectonemertidae.

How do the two freshwater taxa fit in? Moore & Gibson (1 972, 1973) extensively tabulated the similarities and differences between Campbellonemertes, Potamonemertes and the New Zealand land nemerteans, concluding (Moore & Gibson, 1985) that whereas Campbellonemertes shared many more features with, and was related to, Acteonemertes, Potamonemertes was morphologi- cally much closer to the members of the genus Antiponemertes, most unusually in sharing the specialized excretory ducts which are otherwise found only in the Australian genus Argonemertes. Their interpretation that the antipodean genera had colonized freshwater habitats from terrestrial ancestors, rather than penetrating lakes and rivers via an estuarine route as postulated for the monostiliferoidean tetrastemmid genus Prostoma (Moore & Gibson, 1973, 1985; Gibson & Moore, 1976), appears fully justified in view of the numerous characters they share with the New Zealand land forms. The only major difference is that neither freshwater taxon possesses a capillary blood network (Table IX). However, a simplified blood system plan, together with other traits such as a tendency to lose eyes and develop hermaphroditism, is typical of freshwater nemerteans and can be interpreted as an at present inexplicable adaptation to life in fresh water (see discussion in Moore & Gibson, 1985).

The conclusion drawn is that there are sufficient similarities between Plectonemertes, the Australian and New Zealand terrestrial genera and the two freshwater taxa for a relationship to be established, and all are accordingly now placed in the family Plectonemertidae. The remaining forms, Katechonemertes and Leptonemertes, are geographically separated from the five genera indicated above and also retain the more primitive feature of pseudometameric transverse blood connectives in place of the capillary development which unites Plectonemertes and the Australasian genera. They cannot, however, be excluded from the Plectonemertidae solely because they lack specializations found in other members, particularly when they do share other significant characters. Whilst provisionally included within the Plectonemertidae, the familial placing of these Atlantic island forms must remain uncertain.

The possible evolutionary relationships between the six genera now certainly united in the family Plectonemertidae are illustrated in Fig. 2.


Diagnosis of the family Plectonemertidae

The following diagnosis, based on the present studies, is proposed for the family Plectonemerti- dae.

Paramonostiliferous marine, terrestrial or freshwater enoplans with rhynchocoel wall com- posed of interwoven circular and longitudinal muscle fibres; blood system with two vascular plugs borne either on anterior branches of mid-dorsal vessel or on posterior portions of cephalic vessels anterior to origin of dorsal channel, usually with variably developed subdermal capillary network; excretory system very well developed, extending at least throughout post-cerebral regions of body, opening through numerous nephridiopores, and with mononucleate flame cells which lack cuticular support bars; cephalic glands mostly extensively developed and reaching post-cerebrally but short in one freshwater form, opening via large numbers of improvised pores, frontal organ rarely present.

Our thanks are due to Dr Per Sundberg for his invaluable and constructive comments on our manuscript.

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