Aspects of Malacostracan Evolution

Acta Zoologica (Stockholm), Vol. 73, No. 5 , pp. 33S346, 1992 Printed in Great Britain

0001-7272M$S.oO+ .oO Pergamon Press Ltd

The Royal Swedish Academy of Sciences

Aspects of Malacostracan Evolution Erik Dahl Department of Zoology. University of Lund, Helgonavagen 3. S-22 362 Lund, Sweden

Abstract Dahl, E. 1992. Aspects of malacostracan evolution.-Acra Zoologica (Stockholm) 73: 33S346.

The outstanding success of the Crustacea Malacostraca is largely due to the tagmatization of the malacostracan body and its appendages, which has permitted the evolution of a wide spectrum of adaptations, particularly within caridoid taxa with series of specialized appendages. Non-caridoid ancestral malacostracans have not materialized, and recent proposals by Schram (Schram, F. R. 1986. Crustacea), according to which the Phyllocarida should be removed from the Malacostraca and transferred to a re-defined class Phyllopoda, was found to be built upon false premises. Manton (Manton, S . M. 1953.Symposia ofthe Society for Experimental Biology 7 : 33S376), discussing a hypothetical malacostracan ancestor, was of the opinion that in such an ancestor walking preceded swimming, an opinion which has received considerable support. This also implies that the Malacostraca were originally epibenthic, retaining a number of primitive features. The hypothetical ‘generalized malacostracan’ envisaged by Calman (Calman, W.T. 1909. A treatise on zoology, Part 7 , pp. 1-346) was also presumed to be epibenthic, representing what Calman called a caridoid facies, thereby emphasizing an important aspect of the eumalacostracan structural and functional plan.

Erik Dahl, Skogsrnyrsvagen 19, S-75 245 Uppsala, Sweden.

Introduction

The Crustacea Malacostraca have been outstandingly successful in establishing themselves in a multitude of niches both in salt and fresh waters and also in repeatedly invad- ing terrestrial habitats. Undoubtedly this has been at least partly due to the tagmatization of the malacostracan body.

Manton (1953) maintained that in the Malacostraca walking preceded swimming and that ‘no functional expla- nation for the evolution of the thorax seems to be forth- coming from a primary swimming creature’. Instead she called attention to the advantages inherent in the evolution of ambulatory legs in the anterior part of the body near the mouth opening. She also presumed that the differentiation of thorax and abdomen was associated with an epibenthic mode of life. The thoracic endopods could be adapted for walking and for collecting and hand- ling food, exopods specialized for swimming, and epipods transformed into respiratory organs. Thoracic exopods could take over ventilatory functions.

The establishment of a thoraco-abdominal tagmosis as a prerequisite for malacostracan evolution has opened two main alternatives for further development. One of these (cf. Rolfe 1962, 1969, 1981) indicates that the Phyl- locarida with a number of primitive features, e.g. a furca and a free seventh abdominal segment, should stand close to the ancestor of more advanced Malacostraca. Another alternative was presented by Calman (1909), whose ‘generalized malacostracan’ was provided with the basic features of a caridoid.

Hessler & Newman (1975) noted that ‘the leptostracan Phyllocarida are too similar in form and function to the Cephalocarida for this to be a simple convergence’, and

Hessler (1982) stated that the Leptostraca represent the most primitive grade of evolution among the living Mala- costraca and that ‘the function and morphology of the thoracic limbs are quite close to those of the cephalocarids and branchiopods, reflecting a primitive crustacean condition’.

The Phyllocarid Facies

The fact that the thoracopods of all well-preserved Phyllo- carida from the Silurian up to the present were non- locomotory make them unlikely as direct ancestors of the Eumalacostraca, in the functional systems of which locomotory thoracopods play important parts. Cannon (1924) concluded, as a result of a study of filter feeding in Nebaliu, that any similarity with the Branchiopoda is coincidental, and the analysis of the development of Brunchinecru by Fryer (1987) indicates no closer relationships between branchiopods and phyllocarids.

Schram (1986), however, proposed that the Phyllocar- ida should be removed from the Malacostraca and placed in his re-defined class Phyllopoda, but Dahl (1987) after a re-examination of the arguments presented by Schram, found that they were partly based on misunderstandings concerning phyllocarid morphology. The Phyllocarida have a typically malacostracan structural plan with a malacostracan type tagmosis, a malacostracan pleon, the pleopods provided with an appendix interna, and, most sig- nificant, malacostracan compound eyes with a chiasma between the lamina ganglionaris and the lamina interna (Elofsson & Dahl 1970).

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340 E. Dahl

The place of the Phyllocarida among the Malacostraca can be regarded as firmly established. According to Cal- man (1909) the Phyllocarida probably constitute an early lateral branch of the Malacostraca.

In the light of the observations summarized above it appears probable that the Phyllocarida, although undoubtedly malacostracans, deviated early from any evolutionary line leading towards the Eumalacostaca.

Cannon (1924), as a result of his studies of filter feeding in Nebalia, concluded that any similarity between filter feeding in Nebalia and the Branchiopoda is coincidental.

Some Proposals Concerning Eumalacostracan Systematics

Calman (1904, 1909), Siewing (1956, 1958), Bowman & Abele (1982), Kunze (1981)

For a long time eumalacostracan systematics has been based upon the conclusions drawn by Hansen (1893) and accepted by Calman (1904, 1909). Calman (1909) recognized four higher eumalacostracan taxa, called ‘divisions’, namely Syncarida, Eucarida, Peracarida and Hoplocarida, to which he referred the eumalacostracan orders then known. This system remained practically unchallenged for nearly 50 years.

Siewing (1956, 1958), however, no longer accepted the taxon Eumalacostraca, but gave the same rank (‘Reihe’) to all the major Malacostracan taxa, i.e. the Phyllocarida, Hoplocarida, Syncarida, Eucarida, Peracar- ida, and Thermosbaenacea. This levelling of systematic rank does not appear justified and has not been generally accepted.

Schram (1981, 1983, 1986)

The long period of a general concensus with respect to the broad outlines of eumalacostracan systematics came to an end when Schram (1981) began to present a series of new alternative proposals. He built his approach on a comparison between cladograms based on what he called ‘alternative arrangements and weightings of the major morphotypes’. The choice of ‘major’ features was based upon their importance having been established by their having been used by taxonomists during the present century, a criterion the value of which is not self-evident. The result was 16 basic morphotypes of which 10 could be affiliated to known fossil or recent taxa.

In the present context it is worth noting that of the 10 features used in constructing the cladograms no fewer than 6 refer to properties of the carapace, namely carapace ‘complete’, ‘fused to the thorax’, ‘unfused to the thorax’, ‘imperfect’, ‘no carapace’, ‘short carapace’, and only 4 refer to other features, namely the presence or absence of a brood pouch and the presence or absence of thoracopod exopods.

A computer analysis led to the division of the Eumala- costraca into five ‘cohorts’, mostly based diagnostically upon the condition of the carapace. These cohorts were the Arthrostraca (no carapace), Brachycarida (short carapace), Eucarida (complete carapace fused to the

thorax), Mysoida (complete carapace unfused to the thorax), and an uncertain cohort created to receive the extinct Eocaridacea.

The most important difference relative to Calman (I.c.) was the abolition of the taxon Peracarida and the splitting of its members upon three different cohorts. The Amphi- poda and Isopoda were ranged together with the Syncar- ida in the cohort Arthrostraca, the Spelaeogriphacea, Tanaidacea, Cumacea, and Thermosbaenacea in the cohort Brachycarida, and the Lophogastrida and the Mys- ida in the cohort Mysoida, together with the genera War- erstonella and Belotelson, both extinct. Later on this ‘cohort’ concept was abandoned by Schram, without comments.

But in 1986 Schram again went over the whole ground, making 4 cladistic analyses based on 31 characters, classi- fied as ‘primitive’ or ‘derived’.

The results of the analyses are rather similar. They indicated the existence of a limited but from case to case slightly variable number of evolutionary lines, and it is worth noting that three of these, which can all be discerned in the cladograms, correspond to the three eumalacostracan ‘divisions’ of Calman (I.c.), namely the syncarid, eucarid, and peracarid lines.

Considering the Mysidacea, Schram (1986, p. 125) stated that in the mysid Neomysis arnericana all eight pairs of thoracopods are closely associated and separated by ‘a distinct skeletal bar’ from ‘the cephalon’. He presumed that in Mysida the first thoracic segment is not fused to the cephalon despite the fact that there is ‘a tendency’ to develop maxillipeds. This claim made Schram (I.c.) split up the taxon Peracarida, making the Mysida a sister group to all other peracarids.

This is a remarkable claim which I have made efforts to verify. The collection of sectioned Crustacea at the Department of Zoology, Lund, contains great numbers of slides of many different Mysidacea, with the species Neomysis integer, PraunusfZexuosus, and Boreomysis arc- rica particularly well represented by many series of trans- verse, sagittal and horizontal sections, treated with a variety of stains.

For a long time it has been known that the cephalothoracic shield of the Mysida covers and is fused to one to three anterior thoracic segments (Calman 1909), and this arrangement could be verified in all the species mentioned above. The study of sections of all of them failed to reveal the presence in the cephalothoracic region of any ‘skeletal bar’.

Observations on the ventrum of the cephalothorax of whole specimens of N . integer showed the presence of eight closely but evenly spaced pairs of thoracopods plus maxillae and maxillulae. The ventral furrow between the bases of these appendages continues unimpeded all the way up to the paragnaths. Consequently the paragnaths separate the unbroken sequence of eight thoracopods and two pairs of maxillae from the mandibles which constitute the only pair of ‘anterior’ mouth parts. The only possible interpretation appears to be that Schram saw but failed to recognize the paragnaths and that they represent the ‘skeletal bar’, referred to by him. The Peracarida remain intact.

Finally Schram 1986 found that the application of a hypothesis, according to which the carapace was postu-

Malacostracan Evolution 341

lated to be a derived feature, gave longer Wagnerian trees and produced complications. But as shown by Dahl (1991) it is now obvious that the classical carapace hypothesis is untenable, and the preliminary views concerning its validity briefly presented by Dahl (1976), although later verified, need not be discussed here.

In the third version of this discussion about eumalacostracan interrelationships Schram (1986) discerned four lines of evolution, namely:

(1) a eucarid line, characterized by the possession of a zoea larva and a carapace fused to the thorax;

(2) a belotelsonid line, the only known representative of which is the Pennsylvanian genus Belotelson;

(3) a syncarid line without a carapace; and (4) a waterstonellid-peracarid-pancarid line.

In this version of his malacostracan system, Schram recognized no taxa between subclass and order levels. The ‘cohorts’ Arthrostraca, Brachycarida, Eucarida, and Mysoida introduced by Schram (1981) were no longer mentioned. The Eumalacostraca and Hoplocarida were retained as malacostracan subclasses but the Phyllocarida were removed from the Malacostraca and placed among the Phyllopoda, the result of a misunderstanding of phyllocarid and eumalacostracan structural patterns (cf. Dahl 1987).

In all 13 eumalacostracan orders were recognized, 3 of them only known as fossils, namely the Waterstonellidea, Belotelsonidea, and Pygocephalomorpha. The recent orders are the Syncarida, Euphausiacea, Amphionidacea, Decapoda, Mysida, Lophogastrida, Mictacea, Edri- ophthalma, Thermosbaenacea, and Hemicaridea.

The taxon Edriophthalma was introduced by. Leach (1814), who divided the Malacostraca into two main groups, the stalk-eyed Podophthalma and the sessile-eyed Edriophthalma. As shown by Boas (1883) and Calman (1904, 1909) this subdivision is artificial, and it was excluded from the system proposed by Calman (1909). The hypothesis of a closer amphipod-isopod relationship was again taken up by Reibisch (1927), but Siewing (1951) definitely proved that amphipods and isopods are not closely related and that the occurrence of sessile eyes is a case of convergence without deeper phylogenetic significance.

The introduction of the taxon Hemicaridea as an expression of a somewhat closer interrelationship between Cumacea, Tanaidacea, and Spelaeogriphacea is more realistic. On the other hand the lowering of the systematic status of the three last-mentioned taxa to subordinal level is neither congruent with general trends within malacostracan systematics, nor supported by any closer morphological similarity between these three well-defined taxa.

Schram (1986) did not recognize the Eucarida as a separate taxon, but from the text it is possible to conclude that the eucarid line is presumed to include the orders Euphausiacea, Decapoda, and Amphionidacea. This means that with the addition of the last-mentioned order, not recognized at the time of Calman, the coverage of the presumed eucarid evolutionary line coincides with that of the ‘division’, later superorder, Eucarida.

The syncarid line coincides with the ‘division’ Syncarida (Calman 1909) with the later addition of the Bathynella-

cea. The postulated derivation of the Syncarida from a common eumalacostracan stock by means of the loss of the carapace (Schram 1986, cladogram fig. 43-3 character 16) appears unlikely in the light of the results presented by Dahl (in 1991), and no evidence exists indicating that the Syncarida ever possessed a carapace.

The postulated belotelsonid line, represented by the single genus Belotelson, may constitute one of many extinct malacostracan lines.The presence of eight pairs of undifferentiated thoracopods without exopods indicates that it was benthic-epibenthic (Schram 1974). A good deal later than the earliest known decapod genus, Palaeo- palaemon from the late Devonian (Schram et al. 1978), it probably was outside the main stream of eumalacostracan evolution and is without any direct bearing upon the present discussion.

Obvious and serious difficulties arise in connection with the fourth evolutionary line postulated by Schram (1986), the so-called waterstonellid-pancarid-peracarid line. As shown in his diagram (1986, fig. 43-3) the following 11 orders are presumed to belong to this line, namely the Waterstonellida, Pygocephalomorpha, Mysida, Lopho- gastrida, Amphipoda, Isopoda, Mictacea, Thermosbaena- cea, Cumacea, Tanaidacea, and Spelaeogriphacea.

As shown in the cladogram and confirmed by Schram (1986) the presumed basic synapomorhy of this large constellation of orders is the ‘loss of thoracopod epipoditic gills-2’, i.e. character No. 19. In the case of the Amphi- poda and Mysida, however, a character - 19 is introduced into the cladogram, implying ‘re-developed thoracopodal gills’. The inclusion of the Mysida is incomprehensible, for the Mysida is one of the few eumalacostracan orders which does not possess epipodial branchiae. By contrast the Lophogastrida with their exceptionally large epipodial branchiae are covered by character 19 and are therefore presumed to lack this kind of respiratory structure. A detailed account of the structure and attachment of the respiratory epipods of the Lophogastrida is to be found in Siewing (1956). My own observations on serial sections of the branchiae of Lophogaster typicus agree with those made by Siewing (1956).

In the Tanaidacea, Cumacea, and Spelaeogriphacea the epipodial branchiae of the first thoracopod are enlarged and respiratory and also act as their own ventilators. Nevertheless, in Schram (1986) these three orders are all to be found in the part of the diagram covered by character 19 ‘loss of thoracic epipodite gills’. At the basis of the branch leading only to these three orders, however, a character 29 is inserted, noting the presence of a maxillipedal epipodite as ‘a cup- or spoon-like respiratory structure’. The reader is not told whether these respiratory epipods are presumed to have been ‘re-developed’ or whether maxillipedal epipodites were not included among the ‘thoracopodal epipodite gills’ claimed to have been lost in conformity with the definition of character 19.

In summary it can be stated that out of the 14 eumalacostracan orders dealt with only 4 are without respiratory thoracic epipods, namely the Mysida, Thermosbaenacea, Mictacea, and Isopoda. Of these 4 orders the Mysida and Thermosbaenacea retain the typical peracarid ventilatory mechanism in the shape of a ventilatory maxilliped epipod. The respiratory function, however, has shifted to the thin-walled and vascularized dorsal fold.

342 E. Dahl

In Mictocaris halope Bowman & Iliffe (1985) indicated that an area above the two pairs of maxillae and the maxilliped may be respiratory, but confirmation is lacking. If confirmed this would be another example of respiratory functions being located in the dorsal fold as the main respiratory organ.

On the whole, however, the respiratory system of the Eumalacostraca is conservative. The temporary sup- pression of characters is a well-known phenomenon. But the hypothesis implicit in the legend of fig. 43-3, characters 19 and -19 according to which malacostracan taxa should have lost their respiratory system, lived for milli- ons of years without it and then re-developed it, is not supported by any presented facts.

No facts supporting the postulated derivation of the non-caridoid Thermosbaenacea from the caridoid Wuter- stonella were presented. Thanks to the re-description of Waterstonella by Briggs & Clarkson (1986) many new observations have become available, but no thoracic epipodites were among them. A derivation of Thermosbaen- acea from Waterstonella remains conjectural.

Nor does there exist any evidence supporting a derivation of the Peracarida from Thermosbaenacea.

As a general conclusion concerning a number of the proposals dealing with eumalacostracan interrelationships and presented by Schram (1981, 1983, 1986), it must be stated that some of them are conjectural and/or not sufficiently supported by observed facts. As noted above they contain certain errors.

The most interesting innovation proposed by Schram is the introduction of the new taxon, Brachycarida, intended to receive the orders Tanaidacea, Cumacea, and Spelaeogriphacea.

Of the other evolutionary lines proposed by Schram (1986) the syncarid and eucarid lines conform to the views concerning eumalacostracan interrelationships presented by Calman (1909) and now generally accepted. The belotelsonid line, based on the single extinct genus, Belotelson, is probably only one of similar extinct constellations and calls for no comments here. As noted above the argument in favour of the postulated waterstonellid-pancarid-peracarid line is conjectural.

Watling ( 198 1 , 1983)

Watling (1981), choosing as his starting point the hypothetical epibenthic praecaridoid crustacean envisaged by Man- ton (1953) and discussed by Dahl (1976), proposed an alternative phylogeny of the peracarid crustaceans, based on an analysis of 29 morphological characters. Watling (1981) concluded that within the Peracarida two main evolutionary lines exist, one leading from a hypothetical peracarid ancestor to the Isopoda, Spelaeogriphacea, Tanaidacea, and Cumacea, and the other one to Amphi- poda, Mysidacea, and Thermosbaenacea.

A second paper (Watling 1983) contained a comparative study of the status of the carapace, compound eyes, mandible, maxilliped, blood vascular system, and devel- opmental patterns in all Eumalacostraca except the Deca- poda and Amphionidacea.

As a result of this investigation Watling (1983) concluded that there are three main eumalacostracan evolutionary

lines, namely, one syncarid-eucarid line, including the Syncarida, Decapoda, Amphionidacea, Euphausiacea, and also the Mysidacea, a further one isopod line, leading from the Isopoda to the Cumacea, Spelaeogriphacea, Tanaidacea, and Thermosbaenacea, and finally one amphipod line, well defined but including only the Amphipoda and without any clear relationships to other eumalacostracan taxa.

This interpretation includes some major innovations, in the first place the transfer of the Mysidacea from the peracarid to the eucarid group of taxa and the elevation of the Amphipoda and Isopoda to superordinal rank, also leading to the rank of order being given to the amphipod and isopod suborders as traditionally understood.

These and other aspects will be discussed below.

Eumalacostracan Interrelationships

The major taxa

One of the major obstacles to an understanding of the derivation and interrelationships of the higher eumalacostracan taxa was the carapace hypothesis (Calman 1909), according to which all Crustacea possess or once possessed a carapace fold, growing out from the posterior margin of the cephalon. This inter a h made the position of the Syncarida enigmatic, for despite their obviously very primitive organization the carapace hypothesis demanded that they must have been derived from ma- pace-bearing ancestors, in which the carapace fold had been secondarily lost.

As shown by Dahl (1991) a carapace fold or shield of the origin postulated by Calman (1909) does not exist in any malacostracan or in any of the phyllopod taxa exam- ined and the various processes leading to the formation of cephalothoracic shields and thoracic dorsal folds in the Malacostraca have been discussed. Previously all these structures have passed under the name ‘carapace’.

In the light of the new results the various possibilities of a derivation of the Eumalacostraca from early malacostracans were reconsidered. It was found that the Phyllo- carida throughout their long known history have retained a very conservative structural plan, and there is no evidence to be drawn either from the fossil record or from the few surviving taxa indicating a phyllocarid origin of the eumalacostracan type of organization. A growing concensus also appears to exist concerning a very early separation of the hoplocarid evolutionary line from a common and ancestral malacostracan stock (Kunze 1981; Bowman & Abele 1982).

On the other hand the ‘caridoid facies’ postulated and discussed by Calman (1909), recognizable in many eu- malacostracans, was studied above all by Hessler (1982, 1983). Deprived of its large and enveloping carapace fold (cf. Calman 1909, fig. 85, p. 145) and after the adjustment of a couple of minor anomalies the structural plan of the hypothetical ‘generalized caridoid’ of Calman becomes very similar to an anaspidid syncarid. It is also worth noting that the praecaridoid type of crustacean discussed by Manton (1953), Dahl(l976, 1983), and Watling (1981)


could be close to an ancestral type of malacostracan at a lower level of organization than the ‘generalized eumalacostracan’ of Calman but also approaching a syncarid one.

Concerning the systematics of the Eumalacostraca, Cal- man arrived at the same opinion as Hansen (1893), who referred all Eumalostraca to two higher taxa, one com- prising the orders Decapoda and Euphausiacea, the other covering the remaining orders then known, namely, the Mysidacea, Cumacea, Tanaidacea, Isopoda and Amphi- poda. Hansen (1893) did not propose new taxa, but Cal- man was forced also to consider the position of Anaspides tasmaniae, described by Thomson (1894) the year after the publication of the paper by Hansen.

Calman (1904) divided the Eumalacostraca into three ‘divisions’, letting the name Syncarida, previously introduced for some extinct forms, cover also Anaspides, and proposing the names Eucarida and Peracarida for the two new groups of taxa discerned by Hansen (1893).

From his comments it is obvious that the discovery of Anaspides was a surprise to Calman. He recognized its similarity to Uronectes and other extinct forms and he accepted it as a member of the Syncarida. But he noted (1904, p. 155) ‘that this remarkable form presents a combination of characters which indicate for it a very isolated place in our classification. It is not merely a schizopod without a carapace. . . Though Anaspides is not by any means like the hypothetical ancestral malacostracan. . . it is a very ancient type.’

This verdict by Calman (1904, 1909) has influenced carcinologists’ views on the Syncarida up to the present time. Calman appears to have been too influenced by his own conviction concerning the phylogenetic importance of a hypothetic carapace fold to recognize that his own hypothetical ‘generalized malacostracan’ (Calman 1909, fig. 85, p. 145) really differs from an anaspidid syncarid mainly by having been provided, by himself, with an enveloping cephalic carapace fold. Although Calman (I.c.) applied the term ‘generalized’ to his hypothetical primitive malacostracan, it is obvious that to him and to subsequent generations of carcinologists, it came to represent an ancestral malacostracan.

The final outcome of the deliberations by Calman (1904) was the repartition of the Eumalacostraca upon three ‘divisions’, the Syncarida, Eucarida, and Peracarida, still accepted, as superorders, by the majority of carcinologists .

Since 1909 new taxa have been added to all these superorders. The Palaeocaridacea have been recognized as a separate syncarid order, and the Bathynellacea have been added. The Amphionidacea are a new eucarid order, and the Spelaeogriphacea have been added to the Peraca- rida. Probably the same will be the case with the Micta- cea.

Syncarid-eucarid relationships

A comparison between the Syncarida and the Eucarida reveals that these two superorders share some characters not found in any other eumalacostraca, namely:

(1) nauplius eyes; (2) antennular statocysts; and

(3) proximal thoracopod articulation, used in walking, the bodykoxa joint.

It can be added that a petasma is only found in syncarids, eucarids, and certain isopods.

Some other systems should also be mentioned. The jumping reflex system is found in syncarids, eucarids and, among the peracarids, in the Mysidacea but not in any other peracarid taxon. The Euphausiacea do not make the long jumps characteristic of some of the other taxa, but rather jerks resulting in what Kils (1981) called ‘backward swimming’. Mysids, on the other hand, make long jumps like Paranaspides and decapod prawns.

Professor R. R. Hessler (Scripps Institution of Ocean- ography, La Jolla, CA) has informed me that some stoma- topods are effective jumpers, but I have not found any analysis of the jumping mechanism. Jumping in talitrid amphipods is achieved by a completely different and certainly apomorphic mechanism. The typical spiral musculature of the caridoid pleon, one of the prerequisites for caridoid jumping, is lacking in the talitrids, which use the sudden straightening of the bent-in pleon for their take off from the ground.

The ventilatoryhespiratory systems described above also offer some interesting comparisons. The syncarid system with fully exposed respiratory epipods is ventilated by a varying degree of exposure to the surrounding water dependent upon the number of thoracopods and pleopods actively engaged in swimming, the rhythm of their beating, and the resulting speed of the animal through the water. This is a simple system automatically adjusted to the degree of activity of the animal with, at rest, the autochtonous vibration and the slow beating of exopods meeting a minimal requirement of ventilation, and at the other end the full engagement of all thoracopods and pleopods in an activity providing maximal ventilation without specialized ventilators,

Among the Eumalocostraca no ventilatory/respiratory system exists that is more likely to resemble the situation which could be expected to exist in an ancestral malacostracan with newly established thoraco-abdominal tagmosis.

The probably crucial innovation found in the last-mentioned types of taxa is the addition of specialized ventilators in combination with branchial chambers, through which directed respiratory currents are flowing over epi- podia1 branchiae and/or other respiratory surfaces, per- mitting a higher respiratory efficiency and thereby an increased metabolic rate, which probably provided the key to the success of eucarid and peracarid caridoids in comparison with the less advanced syncarid ones.

The euphausiids, highly successful within their pelagic habitat but lacking specialized ventilators, might appear to contradict the tentative conclusion drawn above, but this need not be the case. The Euphausiacea share with the Syncarida and the Decapoda a number of features indicating a close relationship between the three taxa. Others could be added, e.g. the very close resemblance with respect to the larval development with series of corresponding nauplius, calyptopis, and zoea stages in the Euphausiacea and the Dendrobranchiata. The retention of stenopodous thoracic endopods may be taken to indicate that the ancestors of the Euphausiacea were once

344 E. Dahl

epibenthic. As shown by Dahl (1991) it is probably the formation of continuous branchiostegal folds which has led to the obliteration of external segment borders in many Malacostraca, and it is the absence of branchio- stegia which explains the retention of segmental borders in the thorax of the Syncarida, Amphipoda, and Isopoda, and in the part behind the cephalothoracic shield in Mysi- dacea, Cumacea, Tanaidacea, and Spelaeogriphacea. It is the improvement of the efficiency of the respiratory/ventilatory system due to the evolution of ventilated branchial chambers which leads to the formation of dorsal and dorsolateral shields and folds in the thoracic region of most Eumalacostraca, and syncarids, amphipods, and isopods retain a segmented thorax because they never developed this kind of respiratory/ventilatory system.

As noted above, Calman (1904) was mistaken when stating that the Syncarida occupy a ‘very isolated place in our classification’. On the contrary, the Syncarida and Eucarida are in many respects quite close to each other. Postulating an increased degree of morphological compli- cation of the respiratory/ventilatory system leading to an improved efficiency, and a progressive differentiation and specialization of thoracopods, it is not difficult to visualize how a wide spectrum of caridoid Malacostraca could have been derived from praesyncarid or early syncarid ancestors.

Peracarid affinities and differentiation

Within the Peracarida evolution has, on the whole, led to a differentiation away from the typical caridoid facies, which is only found in the Mysidacea, generally recognized as the most primitive representatives of the taxon.

The Peracarida possess two unique and apparently syn- apomorphic features, shared by the majority of the orders, namely:

(1) a female epipodial marsupium, present in all orders

(2) a ventilatory maxilliped endopod, present in all except the Thermosbaenacea; and

orders except the Amphipoda, Isopoda, and Mictacea.

Various peracarid orders deviate, with respect to their general habitus, rather widely from the caridoid facies so characteristic of the Syncarida and Eucarida. The only typically caridoid peracarids are the Mysidacea which are the only peracarids which possess a typical jumping reflex system. Together with the Amphipoda they are alone within the Peracarida in possessing an endodermal midgut. According to Hessler (1982) the structure of the Peracarid thoracopod body/coxa articulation is intermedi- ate between the eucarid and peracarid patterns, and could easily have been derived from the former.

Siewing (1963) and Hessler (1982) have both expressed the opinion that the mysid structural/functional plan forms a link between the eucarid and the more derived peracarid structural and functional systems, and this conclusion deserves attention.

As one of the conclusions from his cladistic analysis of the Eumalacostraca, Watling (1983) went one step further and, abolishing the concept Peracarida, placed the Mysid- acea among the Eucarida. Although I share the opinion

that the Peracarida were derived from syncarid/eucarid ancestors I feel that on this point Watling may have gont somewhat too far. A basically caridoid structural plan the origins of which were discussed by Calman (1909) anc Hessler (1983). is undoubtedly shared by the Syncarida Eucarida, and Mysidacea. But the Mysidacea differ from the two first-mentioned caridoid taxa in having the two basically peracarid synapomorphies, i.e. the ventilatory maxilliped epipod and the epipodial marsupium. On the other hand they lack the nauplius eyes, the antennular statocyst, and the petasma, shared by the Syncarida anc Eucarida.

One may be justified in considering the Mysidacea a5 not too far removed from the syncarideucarid ancestors of the Peracarida, but to remove them from the Peracar ida in order to place them among the Eucarida would ii my opinion constitute a retrograde step, under-rating th value of the important mysid synapomorphies referret to above. It would also lead to breaking up the tar Peracarida, the unity of which will be discussed below the light of the proposals made by Watling (1983). T:,

In my opinion retention of the Mysidacea as a peracai,,. superorder, composed of the two orders Lophogastric and Mysida, is justified. 1

Another group of peracarids has come to be regardel as a natural constellation the nucleus of which are the orders Cumacea, Tanaidacea, and Spelaeogriphacea They all have the ventilatory and in their case also th respiratory peracarid maxilliped epipod, working with. a small branchial chamber, and they have an epipodir. marsupium. In all of them the endodermal part of tht digestive system is restricted to the digestive coeca, the midgut is ectodermal. They also have only a short cephalothoracic shield, covering the anterior part of the thorax.

The presence of a short cephalothoracic shield lee Schram (1981) to group them together in one order, Brachycarida, within which they were given the rank of suborders. This does not appear congruent with the well- established individuality of the three taxa, which durinr practically the whole of the present century have been recognized as orders, a rank given them by Calman (1904) and corresponding to their structural differences.

As shown by Dahl (1991) the relative length of the cephalothoracic shield is hardly a diagnostic feature in it own right but a reflection of the length of the branchio stegal folds and consequently dependent upon respirat

A question which has caused debate and which has 4 bearing upon the discussion of the Brachycarida concere the origin and systematic position of the Thermosbaenb cea. ’1’

The Thermosbaenacea do not carry their eggs in J

ventral marsupium but in a pouch formed by the respiratory dorsal fold, which is ventilated by the beating of th maxilliped palp (Zilch 1974), thus not using the same typ of brood protection but the same type of ventilation a the Brachycarida. Siewing (1956, 1958, 1963) maintain4 that comparatively close relationships exist between the, Peracarida and the Thermosbaenacea and repeate,jy referred to the presence of a lacinia mobilis in boW But the lacinia is present also in other, including n x . peracarid, taxa. In both Decapoda and Euphausiace:, + is present in larval stages and it appears to be absent

ory/ventilatory adaptations. F


the first place in powerfully built and strongly biting handibles (Dahl & Hessler 1982). Despite recognizing traits shared by thermosbaenaceans and typical peracarids, Siewing (1956) found what he regarded as so many material differences between the two taxa that he placed the Thermosbaenacea in a separate ‘Reihe’ (corresponding to a ‘Division’ in the terminology of Calman) under the name Pancarida. This solution was supported by Zilch (1974) after his investigation of the ehbryology of Thermosbaena mirabilis. Siewing and Zilch &so indicated certain eucarid affinities.

On the basis of an investigation of the functional morphology of the thermosbaenacean Monodella argentarii, Fryer (1964) briefly discussed the affinities of the Ther- mosbaenacea. The major difficulty in placing this taxon ffls been the apparent contradiction inherent in the pres- &ce in the Thermoasbaenacea of various peracarid traits rb combination with the absence of an epipodial mar- W u m . Fryer, however, called attention to cases in the ?Ipi’caridea and Sphaeromatidae where, in clearly pera-

id Isopoda, the epipodial marsupium has disappeared dtfd been replaced by other brood-protecting structures. *er (1964) also noted that Monodella uses the thoracic e,idopods in swimming. Hessler (1964), studying ambulat- &y mechanisms in the Malacostraca, noted that in the Peracarida the proximal thoracopod articulation used in Mlking is not the bodykoxa joint as in the Syncarida and Ihcarida but the coxahasis joint. This was interpreted as dFi arrangement leading to the removal of the danger of dBmage to and loss of marsupial eggs by walking. In Monodella, which, in contrast to the Cumacea and the Tanaidacea, is a good swimmer (Fryer 1964), and possibly also in other thermosbaenaceans, the formation of a dorsal brood pouch may be an adaptation to prevent similar accidents.

The arguments presented by Fryer (1964) appear to solve the difficulties involved in the allocation of the Thermosbaenacea by removing obstacles to placing them ;Enong the Brachycarida, with which they have otherwise much in common. Within the Brachycarida, however, the Thermosbaenacea appear to represent a derived rather than an ancestral taxon. The concept Pancarida (Siewing 1958) has lost its justification. The Brachycarida appear 8 constitute a natural group of taxa. On the other hand the Isopoda differ from the Brachycarida in various xspects which appear important. Their respiratoryhenti- I,.tory system is unique and differs fundamentally from tire brachycaridan one, for they have no ventilatory maxil- *bed epipod, no branchial chamber in which it could act, afnd no respiratory thoracic epipods. If the Isopoda ever p. messed a eumalacostracan ventilatory/respiratory sys- b m they have lost all traces of it. Instead they have wolved a completely new system based exclusively on kspiratory and ventilatory pleopods. With this system hey have been very successful with respect to the coloniz- Mion of every possible type of habitat and the evolution 0.’ vast numbers of species and many higher taxa.

The isopods resemble the Brachycarida in having an @%dermal midgut, apparently an apomorphic condition ttle systematic value of which is difficult to judge. They &o resemble the Brachycarida in having maxillary ’’-5hridia. n’If the Isopoda share a root with the Brachycarida the

point of separation must lie very far back and at a rather undifferentiated stage. On the other hand Watling (1981, 1983), in my opinion rightly, laid emphasis upon the isolated position of the Amphipoda within the Peracarida and criticized the views of Bousfield (1978) concerning the origin and differentiation of the taxon.

The Amphipod functional system was studied by Dahl (1977). Both the ventilatory/respiratory and the natatory functions are based on the incessant activity of the three anterior pairs of pleopods. The respiratory organs are the thoracic epipods, and the ventral space in which they are semi-enclosed is unique in having its walls composed of the anterior thoracic coxal plates, coxal and basal expanded articles of the posterior thoracopods, and the three anterior pairs of typical pleopods and behind them three pairs of more or less typical uropods.

The Amphipoda have an endodermal midgut, an antenna1 nephridium, and share with the Mysidacea various aspects of the armature of the cardia (Siewing 1956). Their nearest living relatives may be the Mysidacea (Siewing 1963) but that does not imply that this relationship is a close one.

The amphipods and isopods have hardly anything more than a basic malacostracan structural plan in common, and the attempt by Schram (1986) to resurrect the long- forgotten taxon Edriophthalma to receive them is not based on any relevant new arguments.

Like the Isopoda, the Amphipoda have been successful in colonizing practically all acceptable habitats from moist forests to the deep sea and in producing a high number of species and a number of higher taxa. Their fossil record is extremely poor and does not go back beyond the Eocene. This certainly does not give a true picture of their geological history.

Conclusions

Results obtained in the course of the present investigation and by Dahl (1991) appear to contribute to our understanding of the structural and functional morphology of the Crustacea and in the first place the Eumalacostracan evolution and differentiation, namely

(1) the establishment of the fact that the carapace hypothesis formulated by Calman (1909) is no longer tenable;

(2) the documentation of the profound influence of the respiratoryhentilatory mechanisms upon the modelling of the eumalacostracan thoracic exoskeleton;

(3) that, contrary to current opinion, the Syncarida certainly never had a cephalic carapace fold and that, with respect to their thoracic morphology, they represent a very primitive stage, the mode of ventilation of their epipodial branchiae depending directly upon the varying degree of thoracopod/pleopod activity without any special mechanism for producing and canalizing respiratory currents.

The Syncarida are also unique in possessing, in the orders Palaeocaridacea and Bathynellacea, the original pattern of eight free thoracic segments, and the first indication of a cephalothoracic shield due to the fusion

346 E. Dahl

of the first thoracic segment to the cephalon occurs in the Anaspidacea in connection with the beginning transform- ation of the first thoracopod into a maxilliped;

(4) in the light of the results obtained by previous writers, in recent years above all Hessler and Watling, in combination with the results obtained in the present investigation, a reconsideration of the systematics of the Eumalacostraca appears desirable; and

(5) evidently of the three 'Divisions' proposed by Cal- man (1990) the Syncarida and Eucarida clearly retain their validity and, for reasons presented above, I feel unable to accept the proposal by Watling (1983) according to which the Mysidacea should be transferred to the Eucarida, my main objection being the presence of the two crucial peracarid apomorphies in both mysids and lophogastrids, and the manifestation of the apparently plesiomorphic nature of the caridoid facies throughout the Eumalacostraca.

In my opinion, therefore, the higher taxa proposed by Calman (19O9), namely, the Syncarida, Eucarida, and Peracarida, should be retained.

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Aspects of Malacostracan Evolution