Zoologica Scripta. Vol. 5 , 163-166, 1976 Proceedings of the First Scandinacian Symposium on Systematic Zoology, Stockholm 7-9 January 1976

Structural Plans as Functional Models Exemplified by the Crustacea Malacostraca Erik Dahl

Zoological Institute, University of Lund, Lund, Sweden

Abstract

Dahl, E. (Zoological Institute, University of Lund, S-223 62 Lund, Sweden.) Structural plans as functional models exemplified by the Crusta- ceu MalacoJtraca. Zoo]. Scr. 5 (3-4): 163-1 66, 1976.-The structural plans of higher taxa also represent integrated functional model systems which may be of value in dealing with evolutionary and phylogenetic problems. The model concept is tested on the Crustacea Malacostraca. Their origin and interrelationships are discussed, and a new alternative for their derivation is presented for criticism and comparison with previous hypotheses.

1. Structural plans and functional model systems

Higher taxa are constellations of lower taxonomic units characterized by an essentially similar structural plan. In the case of taxa at the order or higher levels this structural plan is, as a rule, very clearly separated by morphological criteria from corresponding plans of other taxa at the same level. This is due to the fact that the higher taxa also constitute con- stellations of evolutionary lines which have for a long time been separated from other comparable lines. In invertebrates splittings at the order level generally seem to be of Mesozoic age or even older. This also implies a high degree of genetic isolation from other groups.

Although definitions of higher taxa are invariably based on comparative anatomical criteria, these higher taxa can also be regarded as functional model systems, the flexibility of which is both granted and limited by their structural and genetical isolation. In order to understand the evolutionary processes which have taken place within a higher taxon analy- ses and comparisons of such functional model systems would seem to constitute a promising approach. In the case of the Crustacea which are the main subject of the present paper, such an approach has been implicit in papers e.g. by Cannon (1927, 1928, 1933), Cannon & Manton (1927), Manton (1930), Fryer (1964, 1968, 1974), and Sanders (1963). Nevertheless its value as a tool in tracing evolutionary relationships has hardly been fully exploited.

In principle all functions should be included in the models, but in practice aspects of functional morphology are those which most readily lend themselves to this kind of approach and if, as is often desirable, comparisons should be made with fossil material, they are the only ones available. It is obvious that the morphological expressions of mechanisms for alimentation, locomotion, respiration, sensory perception, re- production, brood care etc. are all to a higher or lesser degree interdependent and, when seen together, they will generally give a good picture of the system as a whole with its possi-

bilities and its limitations. Even when, as in the case of fossils, more simplified models must be considered, they can still be very useful.

In the present paper the ideas outlined above will be tested on some questions concerning the phylogeny and basic inter- relationships of the Crustacea Malacostraca.

2. Malacostracan origin and evolution

2. I . The ,fossil record

The Malacostraca constitute a large, highly diversified but simultaneously very well-defined Crustacean superorder. It can hardly be doubted that they represent a natural taxonomic unit. At least one of the two main groups, the Phyllocarida, was present as early as in the Cambrian, and the roots of the Malacostraca certainly lie far down in the Crustacean system. According to Hessler & Newman (1975) the comparatively high number of segments and the full complement of segmen- tal appendages are to be regarded as primitive features.

Otherwise we have little actual evidence concerning the structural plan of the Urmalacostracan. Calman (1909) saw it as a primitive caridoid form, and Siewing (1963) in presenting his concept of the Urcrustacean also drew a caridoid, the main organization of which obviously points in the direction of the Malacostraca. Other writers, e.g. Rolfe ( I 969), Brooks ( 1 969a), Schram (1969a), Hessler & Newman (1975) maintain that the Phyllocarida are the ancestors of all other Malacostraca. This view is supported by the fact that while the Phyllocarida were present in the Lower Cambrian, no fossils of the other main group, the Eumalacostraca, are known until the Devonian. Also certain similarities between the appendages of the Cepha- locarida and the Phyllocarida found by Sanders (1963) have been quoted in support of a phyllocaridan derivation of the Malacostraca.

Certainly the early fossil record of the Eumalacostraca is not very helpful. The oldest undoubted Eumalacostracans known to us were Devonian Eocarids (Brooks, 1962a, 6, 1969a), one of them, Eocaris, clearly caridoid, others probably so. On the other hand, with the exception of the Phyllocarida, early Crustacean fossils from marine deposits are rare. Most of the older eumalacostracan fossils come from fresh water or from marine estuaries and lagoons. A Mid-Paleozoic marine first radiation of the Eumalacostraca may have left very few traces in the fossil record (cf. Brooks, 1969~). The fact that among the very few fossil genera reported from the Devonian and the Lower Carboniferous-Mississippian there are no less

Zoologiro Sctipta 5

164 First Scandinavian Symposium on Systematic Zoology

than three widely different superorders represented (Eocarida, Hoplocarida, and Syncarida) (Schram, 19696), and that such a very advanced Isopod as the phreatoicid genus Hesslerella is known from the Pennsylvanian (Schram, 1970), rather speaks in favour of such an early radiation.

2.2. Malacostracan functional models

It remains to see whether a study of Malacostracan functional models can throw any light on basic evolutionary trends.

The Phyllocarida as we know them to-day are, with one exception, benthic forms, provided with a large carapax with an adductor muscle and with a movable rostrum. Alimentation is by means of a thoracopod filter mechanism, described by Cannon (1927, 1960). The food current enters anteriorly and particles are filtered off by thoracopod setae and transported forwards to the mouth parts. There is no independent maxillary or other cephalic feeding system. The food current may be shut off by depressing the movable rostrum against the carapax valves. The metachronal beating of the thoracopods is not in- volved in locomotion which is effected by the four strong anterior pairs of pleopods. It is not known whether the filter mechanism of the benthic forms functions when the animal is swimming. Fertilized yolky eggs are carried in a brood chamber formed by the distal parts of the female thoracopods, which are during this stage provided with long feathery setae. The young, when leaving the brood chamber, resemble the adults in all but minor details. The main respira- tory organs are the epi- and exopods of the thoracopods and the ventral surface of the carapax.

The Eumalacostraca are so diverse that it is impossible to formulate a similar brief and relevant model description which fits them all. But there are a number of functional fea- tures in which all Eumalacostraca differ from the Phyllo- carida. Thus, no Eumalacostraca possess a thoracopod filter feeding system. Instead filter-feeding in the Eumalacostraca, when present, is effected by a maxillary filter system, unknown in the Phyllocarida. The carapax is never involved in Eumala- costracan filtering. The Eumalacostraca have no counterpart of the Phyllocarid brood chamber, a functionally similar device in the Peracarida being derived in a different manner.

Some further points should be mentioned. Other multi- segmented Crustacea with a thoracopod filter system, i.e. the Cephalocarida and the Branchiopoda, have feeding current systems very different from those found in the Phyllocarida (Cannon, 1927). Locomotion in Cephalocarida and un-modi- fied Branchiopoda is effected by means of the metachronal thoracopod beating which also produces the feeding currents. The division of labour between filtering and non-natatory thoracopods and natatory pleopods in the Phyllocarida results in different current systems. Cannon (1927) was aware of this basic difference between the Phyllocarida and other thoracopod filter feeders, but recently there has been a tendency to neglect it and to include the results of Cannon in broad generaliza- tions (cf. e.g. Lauterbach, 1975). In the Phyllocarida which, in contrast to the Branchiopoda, the Cephalocarida, and certain Eumalacostraca, possess no alternative feeding method even in the juvenile stages, it is obviously necessary to produce eggs rich in yolk and to provide a brood chamber in which

Zoologica Scripta 5

the young can develop to a stage when they can directly adopt the feeding mechanism of the adult. Even in the pelagic genus Nebaliopsis which sheds its eggs into the water there is enough yolk to see the larvae through to a stage resembling the adult (Cannon, 1960).

Thus the functional model of the Phyllocarida does not seem to provide a good basis for Eumalacostracan evolution and radiation. On the contrary it looks remarkably like a dead end. It should be noted that the movable rostrum was present also in the early Paleozoic Phyllocarida (Rolfe, 1969) and that might indicate a mode of feeding resembling that found in the recent species. Unfortunately thoracopod struc- ture in the early forms is unknown, but the pleopod system appears to have been essentially the same throughout the known history of the group.

Schram (1969a, c, 1973) made an interesting attempt to derive the Hoplocarida directly from Phyllocarida. Inevitably the arguments must be largely conjectural and some of the steps involved appear difficult in the light of what has been said above. In any case, however, the Hoplocarida, as also noted by Schram, are hardly on the main line of descent of the Eumalacostraca and they will not be discussed in the present connexion.

2.3. Functional aspects of a hypothetic ancestor

Hessler & Newman (1975) in their discussion of a possible trilobitomorph origin for the Crustacea presented a hypo- thetical Urcrustacean with ].a. numerous segments, no tagmo- sis behind the head region, and a complete set of appendages. These appendages were supposed by metachronous beating to serve simultaneously as a filtering and a locomotory mechanism. This means that the locomotory-alimentary sys- tem corresponds closely to that of the adult Cephalocarida and Branchiopoda. In both the last-mentioned groups, how- ever, the larval stages also possess, though in different form, a feeding mechanism involving the cephalic appendages. In the Cephalocarida this type of feeding persists simultaneously with the thoracopod filtering through all the numerous larval stages and is lost only in the adult (Sanders, 1963). It seems reasonable to assume the presence of such a double feeding mechanism also in the common ancestor of the Crustacea. In thoracopod filterers it is a prerequisite for the existence of autonomous early larvae.

We might for the sake of argument accept an Urcrustacean along the lines suggested by Hessler and Newman. This crea- ture would in a general way resemble a Cephalocaridan, al- though it would have a full complement of appendages. It would have, in earlier stages, a cephalic feeding mechanism, probably persisting even after thoracopod filtering had started. Locomotion would be by means of rnetachrcnms thoracopod beating, simultaneously producing the feeding current. Start- ing from this Urcrustacean the main steps in a Malacostracan direction would be the following ones.

1. A functional sub-division of the postcephalic appendages into non-natatory thoracopods and natatory pleopods. Such a step was postulated by Lauterbach (1975) and 1 share his views on its fundamental importance, although I find it

First Scandinavian Symposium on Systematic Zoology 165

impossible to accept a Conchostracan type as the ancestor of the Malacostraca.

2. To produce a Phyllocaridan the thoracopod filter feeding should be retained. It seems reasonable to assume that it would be the acquisition of a set of powerful natatory pleopods which called for a change in the current systems as discussed above. These changes may have been responsible for the development, alternatively the enlargement, of a carapax and a movable rostrum.

3. To produce an Eumalacostracan, by-passing a Phyllo- carid stage, thoracopod filter feeding should be suspended but cephalic feeding retained. Thoracopods would be trans- formed into ambulatory legs as present in all Eumalacostraca including the pelagic groups. This implies that evolution has taken place in benthic-epibenthic habitats. The presence of 8 pairs of ambulatory legs, only few of which are really in- dispensable for effective walking, would seem to offer a practi- cally unlimited field for specialization as found in the recent Eumalacostraca.

2.4. The carapas and the caridoid form

There exists no obvious reason why a primitive epibenthic Eumalacostracan with a basic functional pattern of the type outlined above should have a caridoid habitus of the types proposed by Calman (1909) or Siewing (1963), i.e. that it should have been generally prawn-like and provided with a large carapax.

Nevertheless the presence or absence of a carapax in the ancestors must certainly be discussed in connexion with Malacostracan evolution, for the carapax plays an important part both in the caridoid and the phyllocarid hypotheses. Hessler & Newman (1975) presented diverging views con- cerning the Urcrustacean, Newman postulating a form with a short carapax, Hessler preferring one without a carapax but with a broad head-shield and well-developed thoracic pleura, i.e. a creature with many Cephalocaridan traits. Lauterbach (1974) although from a different starting point arrived at an interpretation of the Urcrustacean which in this respect re- sembles that of Hessler.

Although no comprehensive discussion is possible within the limited space of the present paper, it can be said that there does not seem to exist any compelling reasons why the inter- pretations of Hessler and Lauterbach should be rejected. Several important Crustacean groups lack a carapax, and the Cephalocarida, the only known recent or fossil Crustacean group which could possibly appear to stand in the neighbour- hood of the roots of the Malacostraca, is one among them.

Lauterbach (1 974), however, postulated that the acquisition of a carapax was a key event in Malacostracan evolution and as such unique. He therefore introduced a new taxon, the Palliata, to receive all carapax-bearing Crustacea. The Palliata, then, with the carapax as the single diagnostic feature, is supposed to comprise the Phyllopoda, the Ostracoda, the Cirripedia (including the Ascothoracica), and the Mala- costraca, a constellation which appears strangely heterogene-

The carapax, when present, is a fold growing out from the posterior margin of the cephalic shield. This shield, firmly

ous.

anchored by the musculature of the cephalic appendages, is the only part of the dorsal exoskeleton strong enough to sup- port such an outgrowth of any considerable size and weight. It may be symptomatic that when the carapax becomes par- ticularly strong and heavily calcified as in the Decapoda it fuses with the dorsum of the thorax. It should also be noted that the carapax fulfills a variety of functions. It is probably always respiratory, it may be involved in the regulation of feeding (Cirripedia, Phyllocarida), in brood protection (Thermos- baenacea, Cirripedia), in protecting branchial structures (De- capoda), in giving general protection to the body (Cirripedia, many Decapoda), and in many caridoid forms and Mala- costracan pelagic larvae it probably gives hitherto largely unexplored hydrodynamic advantages. Provided that the Ur- crustacean had no carapax, as postulated by Hessler and Lauterbach, it would seem surprising if this simple extension of the posterior edge of the cephalic shield had not been formed more than once to meet various functional demands.

As pointed out above the Phyllocaridan carapax is func- tionally important and it was present in the early Paleozoic representatives of the group. Of the three known Devonian and Lower Carboniferous-Mississippian Eumalacostracan superorders the Eocarida and the Hoplocarida had a carapax but the Syncarida had not. Nor had the earliest known Pera- carid, the Pennsylvanian Isopod Hesslerella.

Looking briefly at the distribution of the carapax-bearing caridoid types among the Eumalacostraca we find such types among the Eocarida (especially in certain Pennsylvanian forms), in the Eucarida, and among the Peracarida in the Lophogastrida, and, in somewhat less typical form in the Mysidacea s.str. which may represent a separate order. As evident from the reconstructions by Schram (1974) the step from such an Eocarid form as the Pennsylvanian genus Pea- chella to a typical Eucarid caridoid is certainly not wide. It may indeed be that the main evolutionary significance of the Eocarida lies in their being ancestral not to the Eumalacostraca but to the Eucarida.

The relationships between the oostegite-bearing Carboni- ferous Pygocephalomorpha and the Peracarida remain obscure, and in any case there exists no strong evidence in favour of a Pygocephalomorph derivation of the Peracarida. The finding of Hesslerella makes it possible that the origin of the Peracarida was earlier than in the Carboniferous.

As pointed out above the Lophogastrida alone among the Peracarida represent the typical caridoid facies postulated by Calman (1909). As shown by Siewing (1956) they also retain in their internal anatomy more features of a presumably primi- tive pattern than any other Malacostraca, the recent Phyllo- carida not excepted. This, however, does not necessarily warrant that they are also more or less directly ancestral to other Peracarida. Instead they may represent an early adapta- tion to a holopelagic mode of life and they may have been preserved materially unchanged in the oceanic pelagial for a very long time. In this they would be by no means unique. In fact the Eucarida provide us with two other instances of typi- cal caridoids adapted to the oceanic pelagial and representing what must be on morphological grounds regarded as primitive exponents of their respective groups, viz. the Euphausiacea as

Zoologicn Scripta 5

166 First Scandinavian Symposium on Systematic Zoology

early Eucarida and the Penaeida as early Decapoda. In all three groups a caridoid functional pattern, including e.g. a well-developed carapax and strongly natatory pleopods, may have been super-imposed on a more generalized basic model.

Under the assumption of a caridoid or phyllocarid-caridoid derivation of the Malacostraca it has always been more or less an axiom that forms without a carapax (Syncarida, Iso- poda, and Amphipoda) have lost it secondarily and that others, where it is small (Tanaidacea and Spelaeogriphacea) have re- tained it in reduced form. The Syncarida, among which Paranaspides represents a fairly typical caridoid without a carapax (Manton, 1930), have for a long time provided a difficulty in this respect (cf. Brooks, 1962a, 1969b). The carid- oid ancestry of the Peracarida, on the other hand, has been universally accepted. However, this acceptance is not founded upon actual evidence but upon the time-honoured hypotheses quoted above.

Both the Isopoda and the Amphipoda possess well-developed head-shields and more or less distinct thoracic pleura. Thoracic pleura are never found in carapax-bearing forms. How can we really know that either of these groups ever had a carapax? And how do we know that the small cavity below the shield of the Tanaidacea was not formed within that group as a respiratory device, which is its function to-day? How do we even know that in the Mysidacea with their rotating exopods the carapax was not formed as a respiratory structure replacing lost epipodial branchiae? In short, is it necessary to assume that the Urmalacostracan possessed a carapax? The tentative functional models discussed above do not seem to require it.

In fact the assumption of a Malacostracan ancestor without a carapax might let us escape some of the difficulties now confronting us. One of the obvious consequences would be that the Phyllocarida are not ancestral but represent an early branch, an interpretation to which the functional considera- tions recorded above lend a certain support. Also it would be compatible with the independent evolution of typical caridoid forms within different groups. Furthermore, it permits us to presume a small thin-shelled, marine ancestral form and a Mid-Paleozoic radiation, an idea which seems to rhyme better with the scanty fossil evidence than a derivation from De- vonian-Carboniferous Eocarids.

3. Conclusions

What has been said above and especially on the last few pages presents a tentative third alternative for the derikation and differentiation of the Malacostraca, explicitly and implicitly based upon the concept that the structural plans of the respec- tive groups do also represent integrated functional model sys- tems. It is obvious that this functional model concept makes certain demands on functional coherence in the formulation of evolutionary hypotheses, demands which sometimes tend to be neglected in discussions on a purely comparative ana- tomical basis.

It is not immediately obvious, even to its author, whether this third alternative is preferable to the older caridoid or phyIlocarid-caridoid hypotheses of Malacostracan evolution. Its main value may lie in its being really a third alternative

Zoologica Scripta 5

looking upon basic problems from a new angle and calling for new facts and arguments to support or to refute it.

References

Brooks, H. K . 1962a. The Paleozoic Eumalacostraca of North America. - Bull. Am. Paleont. 202: 159-338.

- 1962b. Devonian Eumalacostraca. - Ark. Zool. (2) 15: 307-315. - 1969a. Eocarida. l n R. C. Moore (ed.), Treatise on Invertebrate

Paleontology: R 332-R 345. - Geol. SOC. of America and Univ. of Kansas, Lawrence.

- 19696. Syncarida. lbid.: R 345-R 359. Calman, W. T. 1909. Crustacea. I n E. R. Lankester (ed.), Treatise on

Zoology 7: 1-346. - Adam and Charles Black. London. Cannon, H. G. 1927. On the feeding mechanism in Nebalia bipes. -

Phil. Trans. R. SOC. (B) 212: 395-430. - 1928. On the feeding mechanism of the fairy shrimp, Chirocephalus

diaphanus Prevost. - Trans. R. SOC. Edinb. 55: 807-822. - 1933. On the feeding mechanism of the Branchiopoda. - Phil.

Trans. R. SOC. (B) 222: 267-352. - 1960. Leptostraca. Dr H. G. Bronns Klassen u. Ordn. d. Tierreichs.

5: I: 4: 1-81. Cannon, H. G. & Manton, S. 1. 1927. On the feeding mechanism of a

mysid Crustacean, Hemimysis lamornae. - Trans. R. SOC. Edinb.

Fryer, G. 1964. Studies on the functional morphology and feeding mechanism of Monodella argentarii Stella (Crustacea: Thermos- baenacea). - Trans. R. SOC. Edinb. 64: 49-90.

- 1968. Evolution and adaptive radiation in the Chydoridae (Crustacea: Cladocera): a study in comparative functional morpholog) and eco- logy. - Phil. Trans. R. SOC. (B) 254: 221-385.

- 1974. Evolution and adaptive radiation in the Macrothricidae (Crustacea: Cladocera): a study in comparative functional morpho- logy and ecology. - Ibid. (B) 269: 137-274.

Hessler, R. R. & Newman, W. A. 1975. A trilobitornorph origin for the Crustacea. - Fossils and Strata 4: 437-459.

Lauterbach, K.-E. 1974. Uber die Herkunft des Carapax der Crustaceen. - 2001. Beitr. (N. F.) 20: 273-327.

- 1975. Uber die Herkunft der Malacostraca (Crustacea). - Zool. Anz.

Manton, S. 1. 1930. Notes on the habits and feeding mechanisms of Anaspides and Paranaspides (Crustacea, Syncarida). - Proc. zool. SOC. Lond. 1930: 791-800.

Rolfe, W. D. I. 1969. Phyllocarida. I n R. C. Moore (ed.), Treatise on Invertebrate Paleontology: R 296-R 331. - Geol. SOC. of America and Univ. of Kansas, Lawrence.

Sanders, H. L. 1963. The Cephalocarida, functional morphology, larval development, comparative external anatomy. - Mern. Conn. Acad. Arts Sci. 15: 1-80,

Schram, F. R. 1969a. Polyphyly in the Eumalacostraca. - Crustaceana 16: 243-250.

- 19696. The stratigraphic distribution of the paleozoic Eumalacostra- ca. - Fieldiana, Geol. 12: 213-234.

- 1 9 6 9 ~ . Some middle Pennsylvanian Hoplocarida (Crustacea) and their phylogenetic significance. - Fieldiana, Geol. 12: 235-189.

- 1970. Isopod from the Pennsylvanian of Illinois. - Science 169:

- 1973. On some Phyllocarids and the origin of the Hoplocarida. - Fieldiana, Geol. 26; 77-94.

- 1974. The Mazon Creek caridoid Crustacea. - Fieldiana, Geol. 30: 9-65.

Siewing, R. 1956. Untersuchungen zur Morphologie der Malacostraca. - 2001. Jb., Anat. 75: 39-176.

- 1963. Studies in Malacostracan morphology: results and problems. In H. B. Whittington & W. D. I. Rolfe (eds.), Phylogeny and Evolu- tion of Crustacea: 85-103. - Mus. Comp. Zool. Spec. Puhl.

55: 2 19-254.

194: 165-179.

8 54-8 5 5.

Professor Erik Dalil Zoological Institute University of Lund Helgonavagm 3 S-223 62 Lund Sweden

Printed 1976-09- I5