Macrobenthic and Nektobenthic Arthropods Disparity as a Key to Ecologic Complexity

This category, although cumbersome, is nevertheless meant to identify a large and ecologically coherent group of arthropods, those of relatively large size and that interact with the sediment or other taxa living on or in it. Such taxa have been the focus of most of the studies of morphology and phylogeny in Cambrian nontrilobite arthropods, such as those previously mentioned of Briggs and Whittington (1985) and Fortey (1985). Further, and of importance to their ecology, they have also been the focus of some morphologic studies.

It is possible to examine the morphology of arthropods at more than one level. One approach is that of Wills et al. (1994), who used an overall morphology metric for assigning a concrete measure of what has rather loosely been called disparity between Cambrian and Recent arthropods. Perhaps surprisingly, they discovered that the disparity, when considered as morphospace occupancy and thus a measure of the total morphometric distance between taxa, was more or less identical between the representative groups of taxa they chose from the Cambrian and the Recent. From these results, one might make an allied claim that Cambrian arthropod ecology (in some way surely a reflection of morphology) has also remained at a similar level of complexity throughout the Phanerozoic.

Although the general approach of Wills et al. (1994) seems reasonable, it appears to contradict earlier (if rather neglected) work by Flessa et al. (1975) and Cisne (1974), which employed a remarkably novel technique for examining the change in arthropod ecology through time—that of information theory analysis. By taking a measure of the complexity of particular arthropod body plans, based on the permutations available of segment types, they demonstrated that during the Phanerozoic there had been a striking monotonic increase in body-plan complexity among marine arthropod orders (see also Wills et al. 1997).

I have adapted and simplified their approach here to deconvolute segmentation and segment types to demonstrate very similar patterns. Using the data of Wills et al. (1994), in terms of a morphospace defined only by segment diversity and numbers, both Cambrian and Recent arthropods have been plotted (figure 18.1). As may be seen, those of the Cambrian occupy a significantly different (and smaller) region than that of the extant ones. Cambrian arthropods—considered at the level of their tag-mosis—are less complex and occupy a smaller morphospace than their Recent counterparts. However, the question may be asked, why is this analysis not rendered invalid by the more detailed and more multimetric approach of Wills et al. (1994)? To address this point, one needs to turn to the interaction between the hierarchical organization of the genome and its role in specifying body plan. Briefly, it is possible to argue that there is a fairly clear correspondence between the region of operation of

Figure 18.1 Plot of arthropods from Wills et al. (1994), showing segment diversity and number for Cambrian and extant arthropods. Two arthropods that significantly increase the range of extant morphology are also included:

Pycnogonum and Homarus, an advanced decapod. Most of the Cambrian Problematica lie within the oval marked. Data from Cisne (1974), Wills et al. (1994), and personal observation.

Figure 18.1 Plot of arthropods from Wills et al. (1994), showing segment diversity and number for Cambrian and extant arthropods. Two arthropods that significantly increase the range of extant morphology are also included:

Pycnogonum and Homarus, an advanced decapod. Most of the Cambrian Problematica lie within the oval marked. Data from Cisne (1974), Wills et al. (1994), and personal observation.

specific and hierarchically arranged genes (segmentation and homeotic genes) and how the body plan develops at a gross level, including numbers and diversity of segments (see Akam 1995). In other words, the rather diffuse concept of a "body plan" may be broken down into hierarchical levels, which are each in principle open to analysis. By examining the body plan at these levels, one is examining a partially decoupled level of operation of the genome. If, conversely, all morphologic information is considered together in an undifferentiated manner, then the signal coming from specific types of morphology—in this case, tagmosis—may be obscured.

The results of this analysis confirm some rather widely held prejudices that Cambrian arthropods are in general much simpler in terms of within-body segment differentiation than arthropods of the later Phanerozoic. A view sometimes expressed, that trilobites (for example) would not be out of place in a modern benthic commu-

Figure 18.2 Plot of Cambrian and extant taxa falling within the "crustacean" clade of Wills et al. (1994), showing segment diversity and number.

nity, therefore seems unjustified. Trilobites, like most other Cambrian arthropods, and in particular almost all of the "problematic" arthropods (cf. Gould 1989) may be seen to have a distinctly archaic look. Only the pycnogonids of extant arthropods are as lacking in tagmosis as the trilobites (figure 18.1). By contrast, the number of segments tends to decrease from the Cambrian to the Recent, although somewhat less dramatically and with some notable exceptions, such as Vachonisia from the Devonian Hunsrück Shale (Stürmer and Bergström 1976), and some of the modern myriapods. One of the reasons for this change is the great rise to dominance of the crustaceans, especially after the eumalacostracan radiations of the Carboniferous. To demonstrate therefore that one is not simply seeing an effect of "clade replacement," one can plot the difference between taxa that fall into a crustacean clade (as identified by Wills et al. 1994) and their selection of extant crustaceans (figure 18.2), with Homarus added as an example of the most complex types of crustaceans. It should be noted that severe doubts have been expressed as to the true affinities of some of these taxa (e.g., Walossek 1999). The total morphospace occupancy is greater in the extant fauna (although not greatly so), but the most striking point is that the two areas of morphospace occupancy have no overlap: in terms of tagmosis the most highly differentiated Cambrian taxa are less complex than the least differentiated of the extant examples. Clearly, within what is allegedly the same clade, an increase in complexity is taking place.

The striking contrast between these two sets of results from the same data set suggests several interesting interpretations. First, it is clear that the Cambrian taxa look odd to our eyes partly because they have their own set of adaptations; an example is the "great appendages" possessed by taxa such as Leanchoilia (Bruton and Whitting-

ton 1983). Yet it is very likely that these appendages, although different in detail, are performing similar tasks to those possessed by extant arthropods. This is therefore a case of similar adaptive needs producing varied responses, although no doubt within a strong constraint of functionality. Given that (it must be repeatedly stressed) we have no particular reason to regard ancient arthropods as merely imperfect versions of more up-to-date representatives (a view perhaps partly engendered by comparison with the development of our own creations such as mechanical means of transport), there is no reason to doubt that they were as well adapted to their conditions as are modern arthropods. With this background, one might therefore expect the detailed complexity of limbs and so on to be equal between the Cambrian and Recent.

Nevertheless, important differences remain at the level of the tagmosis. One may have variations on themes in both the Cambrian and the Recent faunas; but the themes themselves are different. Within a regime provided by homeotic genes interacting in only a simple way, the Cambrian forms elaborate particular segments in unfamiliar ways, but their overall morphologies are strongly constrained by their lack of tag-mosis. The most strikingly different region is the head, where Cambrian taxa in general have almost homonomous limbs, with the exception of a frontal pair. Most of the post-Cambrian change comes about in the reorganization and specialization of head appendages. Trilobites, for example, possess three or four pairs of postoral cephalic appendages, but the morphology hardly differs from that of thoracic ones. Cambrian crustaceans may possess a mandible, but the maxillae are hardly differentiated from the thoracic appendages, a pattern repeatedly seen in Cambrian arthropods. By contrast, an extant decapod crustacean has three highly specialized postoral cephalic appendages (mandible and two maxillae) and may also possess differentiated thoracic appendages. This contrast in tagmosis patterns between the Cambrian and the Recent has important implications for the evolution of arthropod ecology, because segment specialization lies at the heart of arthropod adaption.

The sets of specialized appendages possessed by extant crustaceans can be marshaled to perform a variety of extremely complex maneuvers. For example, extant lobsters such as Homarus and Nephrops have almost all of their appendages functionally differentiated in one way or another: for sensory purposes, feeding (chewing, crushing, shredding), swimming, copulation, grooming, and egg brooding, for example. Barker and Gibson (1977) filmed Homarus gammarus, the European lobster, feeding on pieces of boiled fish. The cephalic appendages are employed in a highly coordinated manner:

1. The morsel is picked up with the second pereiopod, then passed to the third maxillipeds, trapping it between the ischiopodites.

2. As the second and third maxillae move away laterally, the third maxilliped moves up toward the mandibles, which catch hold of the food particle.

3. The third maxillipeds move down again, tearing the food between them and the mandibles, while the other mouthparts move inward to assist in the tearing.

4. The food particle thus removed from the main part is released from the mandibles and pushed downward by the tips of the second maxillipeds.

5. The first and second maxillae curve around the mouth and manipulate the food particle into the mouth.

When a crustacean is faced with live prey, the procedure is likely to be more complex. Observations on the blue crab showed that prey was trapped by the thoracic limbs' forming a sort of cage, while the mouthparts and associated appendages carefully examined and manipulated the prey. In short, modern crustaceans employ a large number of feeding strategies, with often the same taxon utilizing different feeding mechanisms according to circumstance. This adaptability and utility was surely limited in most Cambrian forms. The general lack of well-differentiated cephalic mouthparts would imply, for example, that filter feeding would not even be a possibility for many taxa in the Burgess Shale (the plumose appendages of Marrella seem to be in the wrong position to be able to trap food particles that subsequently could be conveyed to the mouth—see Briggs and Whittington 1985 for discussion). Similarly, for the taxa listed as possible detritus feeders by Briggs and Whitington (1985), the general lack of appendage differentiation would limit the ability of the taxa to sort material prior to ingestion, making this mode of feeding rather inefficient. It thus seems likely that putatively predatory arthropods such as some Naraoia and Sidneyia (see the section "Predation in the Cambrian" below) employed a simple gnathobasic feeding technique like that of the extant Limulus, but that their other ecologic strategies were restricted.

At a deeper level, one might pose the question, what effect does tagmosis actually have on arthropod ecology? Even if it is true that complex tagmosis allows a greater diversity of behavior, what effect does this have on the fundamentals of ecology, for example, on the efficiency of energy transfer from one trophic level to the next? Specialization may on the one hand allow greater efficiency, although the gains from the ability to select food more efficiently may be offset to a certain extent by the greater energy involved in performing more-complicated tasks. Conversely, greater complexity may not imply anagenetic "grade improvement" but rather may be a side effect, either of "ecologic escalation" (Vermeij 1987) or of the dynamics of gene interaction (cf. Kauffman 1993 for a study of the behavior of complex systems). Hard data to study the effects of arthropod specialization are in any case hard to obtain. The only full-scale attempt at ecologic reconstruction of the Burgess Shale fauna (Conway Morris 1986) made estimations of the efficiency of transfer of energy between trophic levels and found that, considered in terms of numbers of individuals at different trophic levels, there was approximately a 7 percent efficiency of energy from primary consumers to predators/scavengers, which may be compared with the 10-20 percent efficiencies quoted for modern communities. If this difference is real and not a taphonomic artifact (predators may be less armored than their prey and thus may be less easily preserved), then Cambrian trophic webs should be correspondingly shorter than modern ones. Arthropod feeding inefficiency may be one determinant factor.

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