Introduction

Readers not yet weary of the metaphor may realize that the first six chapters have examined gentle pluckings of the spider's ecological web: field experiments designed to probe the strength of threads connected directly to neighboring actors in the ecological drama. Experimental evidence has been evaluated for food limitation and intraspecific competition, competition between spider species, limitation of spiders by natural enemies, and the impact of spiders upon their prey populations. Most of these interactions yield what conventionally are termed direct effects, though exploitative competition is actually an indirect interaction mediated through impacts on shared prey populations. The last chapter expanded the scope by examining how other components of the environment influence the biotic interactions that have formed the threads of the metaphor. Now it is time to probe consequences of persistent plucking and poking of more-distant regions of the web. What do field experiments reveal about the larger set of connections, links between spiders and other taxa of predators, and organisms on trophic levels several energy-transfer steps away? In short, what do field experiments reveal about indirect effects in complex communities of which spiders are an integral part?

Indirect effects in a simple system

What community could be simpler than two spider species and their prey? David Spiller uncovered both exploitative competition for prey and interference competition in the ecological web comprised of the orb weavers Metepeira grinnelli and Cyclosa turbinata and their prey in a salt marsh (Spiller 1984a,b; Chaps. 4,5).

Food limitation of terrestrial carnivores

The concept of resource limitation is so central to ecological thinking that it might seem unnecessary to justify examining the impact of prey supply upon spider populations. However, attempts to uncover broad patterns in resource limitation frequently have generated controversy. One that directly engulfs spiders started with a brief, carefully argued communication by Hairston, Smith & Slobodkin (1960). They concluded that the carnivore trophic level of terrestrial ecosystems is ‘resource-limited in the classical density-dependent fashion.’ In particular, they argued that predators are food limited, and that competition occurs on this trophic level. Hairston et al. did not propose that every group of terrestrial carnivores is food limited. Nevertheless, because spiders are major terrestrial predators, it follows that a shortage of prey should frequently affect spider densities. As a model terrestrial predator the spider cannot escape the controversy created by the sweeping predictions made by Hairston et al.; indeed, continuing interest in testing their predictions in conjunction with disagreement over the prevalence of competition has already drawn spiders into the fray (Wise 1975, Schoener 1983a, 1986a).

Prey is conventionally defined to be a limited resource if an increase in the prey supply increases the predator survival and/or fecundity. If increases in one or more of these parameters cause the average population density of the next generation to increase, the population is food limited. Thus, food limitation is defined ultimately in terms of population density, but evidence that food is limiting frequently comes from within-generation measurements of individual survival rates or fecundity.

Reasoning by means of analogies is risky. The metaphors of the preceding pages arose as innocently concocted literary devices and nothing more; they were not intended to parallel nature's deeper structure. Yet stylistic creations spring from particular world views, which filter results of scientific investigations and gaze more favorably on some approaches than others. I have tried to shape the spider as a model terrestrial predator, who acts out the script of a drama staged and casted in the complexities of the ecological web. As interpreters of this theater, we cannot sit back and watch passively, because we are ignorant of what occurs behind the scenes, offstage. In order to understand the hidden scripts, we must jump onto the stage and challenge the actors - probe and poke, remove their masks and look behind the props. In short, we must rely on field experiments. My biases have been clear. They merit scrutiny, because they color my interpretation of what has so far been learned of spiders in their ecological webs.

Ecological dramas

The spider persona

What have we discovered about the spider persona? The spider is usually hungry. When given more prey than it normally encounters, the spider grows faster and produces more eggs. Sometimes it will wander less when food becomes more abundant, but at other times it apparently behaves independently of its recent feeding history. Despite the fact that food is frequently a limited resource, spiders do not commonly compete with other spider species for prey.

Introduction

All the animals that are included within the arthropod assemblage show a degree of similarity frequently lacking in other groups that are nervertheless recognised without dispute as single phyla. For example it is quite easy to accept a relationship between all the leg-bearing spiders and insects, crabs and woodlice; but difficult to appreciate the common ancestry of the snails, clams and squids that together constitute the molluscs. It is therefore odd, at first sight, that there should be -particular disagreement about the status of arthropods as a single phylum.

Historically, theories involving monophyly certainly prevailed, and the occurrence of a major dispute about polyphyly is fairly recent. All the arthropods share a cuticle made of chitin and proteins, all show segmentation with at least some segments bearing paired articulated limbs, and all show rather similar patterns of cephalisation and pre-oral segments. Thus early authors found few problems in uniting them as a taxon, and the term ‘arthropod’ itself dates back to von Siebold in the mid-nineteenth century, coined as testimony to the jointed legs of all these animals. Through the nineteenth and early twentieth centuries the group retained its identity, either as a phylum or as a sub-group (with the annelids) of an even larger phylum called Articulata. The main features of the four principal types that constitute the arthropods (Crustacea, Insecta, Myriapoda and Chelicerata) are shown in table 11.1. Different phylogenetic schemes that have been proposed to link these four sub-groups together are usefully reviewed by Tiegs & Manton (1958); it is evident that essentially monophyletic schemes can differ enormously in detail, as virtually every possible pairing and hierarchy of groups has been attempted.

Introduction

Any biological phenomenon must be dependent upon the fundamental activities of cells. Most obviously, cellular differentiation gives rise to the structural features of tissues and organs, and thus to the overall embryology and morphology of organisms that have been the classic materials for phylogenetic studies. In addition, short-term changes in cell structure and behaviour often initiate physiological or mechanical processes affecting the whole animal, influencing its relations with its environment and the selective pressures it experiences. Hence comparative studies of cells themselves should obviously have some role in an analysis of invertebrate relationships.

Some aspects of cell behaviour were considered in the previous two chapters. Virtually all the chemical constituents of the animal (chapter 4) are cellular products, either within the cell membrane or as secretions from it. And the processes of differentiation of embryos (chapter 5), from cell fusion at fertilisation through all stages of ontogenesis, are major cell behaviour phenomena. But now the concern is rather with cell structure and its bearing on phylogenetic matters. This has been an area of growing importance in the last fifteen years, with a literature largely derived from European sources in general and German authors in particular. An appreciation of some of the more important topics by English–speaking audiences has been lacking until very recently.

Clearly comparisons of cell structure rely on different techniques from earlier morphological studies, and have therefore only been possible since electron microscopes became available in the 1950s. Their increasing prevalence has led to the period since 1970 being termed the ‘era of ultrastructure’.

Introduction

In the preceding chapter, some attempt was made to decide where the first metazoan animals came from and what they might have been like. The most plausible answer takes as a starting point a planula/acoeloid form, small, ovoid and ciliated. As discussed in section 7.4, this can give rise both to the cnidarians, which have a planula larva, and to the bilateral acoelomate worms. It also provides a sensible starting point for radiations of pseudocoelomate and coelomate phyla, as the rest of this book should make clear. In effect, the planula can be seen as the early worm, and most of the designs it gave rise to are also elaborations on the theme of being a worm. This chapter deals with a subset of these variations on a theme: the worms that are conventionally regarded as part of the protostome or spiralian assemblage. All are supposed to share the classical patterns of spiralian development set out in chapter 5, so that in comparing them it should also be possible to get a perspective on the Protostomia/Spiralia super-phylum as a whole.

Acoelomate worms

Platyhelmnths

Apart from a predominantly German school of thought requiring flatworms and most other simple worms to be secondarily reduced from a coelomate state, the majority of currently popular theories suggest that flatworms are direct derivatives from the planuloid/acoeloid form. This early metazoan is assumed to settle to a benthic lifestyle, thereby acquiring greater bilaterality in association with moving directionally in two dimensions, and the beginnings of a proper gut as the tissues differentiate fully into three cell layers.

Introduction

The origin of multicellular animal life from single-celled ancestors is perhaps the most enigmatic of all phylogenetic problems, and the least likely to be ‘solved’ by additional evidence from any of the sources already discussed. Most obviously, it remains completely obscure in terms of the final arbiter of a fossil record. The issues with which this chapter is concerned are therefore inevitably highly speculative and any treatment of them is bound to be unsatisfactory. Nevertheless this area is gradually becoming amenable to a more synthetic approach, and it is now possible to bring together some of the problems already raised in part 2, since increasing knowledge of cell biology and biochemistry is beginning to give a fresh perspective to these murky areas of zoology. This is also an area where an increasing stress is being laid on the necessity of proposed ancestors being functionally plausible, and of stages in their evolution having obvious selective advantage, so that some early theories are gradually losing support.

The problem of metazoan origins has naturally exercised the imaginations of invertebrate biologists, and many theories have been advanced in the last 150 years. Most of these have been compounded with views on subsequent evolution from the earliest metazoan to the groups of existing lower Metazoa, and on relationships between these various phyla (particularly sponges, cnidarians and platyhelminths). In fact it is difficult to separate these issues, as any theory of the nature of the first multicellular animals inevitably has consequences for conceptions of ‘what happens next’.

Based on the evidence and characters discussed in Parts 1 and 2 of this book, the chapters in Part 3 look at each of the traditional sections of the animal kingdom in turn. The sequence followed is a fairly classical one, so that particular groups can be found in the ‘expected’ places. The origins of the Metazoa, and relationships between the lower groups, are dealt with first (chapter 7); succeeding chapters are then devoted to the acoelomate and spiralian coelomate worms, and to the pseudocoelomates (chapters 8 and 9). The molluscs merit a chapter on their own (10); and then the arthropods are dealt with together (11), though they may not in fact be closely related to each other. Deuterostomes are dealt with collectively, with chordates included briefly (chapter 12). Finally the lophophorates are used in chapter 13 to highlight some problems with the underlying assumptions on which such a sequence of chapters is based.

Introduction

The lophophorates are a group of three phyla, sometimes given taxonomic status collectively as the Lophophorata or Tentaculata, and having in common the presence of a special kind of feeding organ, made up of a ring of ciliated tentacles surrounding the mouth, termed a lophophore. They are not particularly familiar to the layman, and rarely receive attention in introductory zoology courses, but are nevertheless of considerable importance in interpreting the pattern of the animal kingdom, so are justifiably given a chapter to themselves in this book.

The most important of the three phyla nowadays is the moss animals (bryozoans or ectoprocts), individually tiny but with the zooids assembled as often substantial colonies, diverse in form but commonly sheet-like or erect and branching. The bryozoans (reviewed by Ryland 1970; Woollacott & Zimmer 1977) are actually amongst the larger phyla in terms of species number. They are very frequently met with in the lower littoral zone, where they may dominate the filter-feeding community, and they may also be washed up as dried remains on the strandline; most people will therefore have met specimens of these creatures, though they may have misinterpreted them as plant remains. A second group is the lamp shells or brachiopods, reviewed by Rudwick (1970). They resemble molluscan bivalves but have two dissimilar calcareous shell valves that are dorsal and ventral (rather than identical valves that are bilateral), and within which a spiral array of tentacles may be visible. The brachiopods are not abundant now, but have been dominant in previous eras and their fossilised remains are invaluable to geologists for dating purposes.

Introduction

Certain features of basic animal design are critical to all schemes of invertebrate phylogeny and thus underlie, explicitly or otherwise, all zoological textbooks and courses. These are features that contribute to our conventional hierarchical view of animals, giving the sort of schemes summarised in chapter 1: the planes of symmetry that distinguish radiate phyla from ‘higher’ bilateral groups, the diploblastic nature of ‘lower’ animals and the added mesoderm giving triploblasty, the presence of varying types of body cavity, or of serial repetitions of structure, and the use of differing systems of skeletal support. Unless we consider the validity of these characters, we can get nowhere in a review of invertebrate phylogeny – they are the very stuff of which theories have been made, the classic comparative morphology against which all other criteria will be judged. This chapter is therefore devoted to a fairly lengthy examination of these topics, and forms both the starting point and in some sense the core of this book.

Patterns of symmetry

Animals are frequently divided in textbooks into the Radiata and the Bilateria, with the implication that as ‘lower’ animals are radially symmetrical so the earliest animals must have begun with that pattern. For the present this latter point will be left aside, as the symmetry of the first metazoans will form a central issue in chapter 7. But it is important here to decide if there is a fundamental difference between the so-called radiate animals and the rest of the animal kingdom.

Introduction

The phylum Mollusca is structurally and ecologically enormously diverse, and highly speciose. Inevitably this makes the search for ancestral forms and possible origins more difficult, and there have been endless controversies over the nature of the molluscan ‘archetype’, and over relations between the various sub-phyla or classes that it gave rise to. However, there is perhaps a stronger current consensus over the status of the molluscs, and their position relative to other phyla, than there has been for many decades; consequently this chapter presents reasonably uncontroversial material, with which most modern treatments would concur.

Nevertheless many text-books and the simplified phylogenetic trees commonly presented therein still treat the molluscs in a rather outdated manner and insist on their close affinities to annelids and arthropods, endowing them with coeloms (and sometimes even segmentation) of a homologous if reduced nature. Such traditional views usually combine these three groups as the major spiralian or protostome invertebrates, at the apex of the left-hand ‘branch’ of a neatly dichotomous ‘tree’. It is therefore necessary to consider the evidence that gave them this position for the best part of a century, before turning to the insights from morphology and embryology that have, within the last two decades, led to their relocation as derivatives of a turbellarian-like form (a view actually initiated in the 1890s).

The traditional ‘annelid theory’ for the origins of molluscs is fast losing ground to the newer views, but there remains some dispute over the relative affinities of the annelids, molluscs and flatworms.

In the first part of this book, some of the principles and problems of phylogenetic study are considered. Many of the classical morphological characters that have been used to classify invertebrates are critically examined, and the schemes of invertebrate relationships traditionally derived from interpretation of these characters are compared.

Introduction

The way in which genes and proteins evolve and can reveal phylogenies has been dealt with, as far as possible; this chapter moves on to the later stages of the processes and interrelationships shown on page 51. Development and morphogenesis require a complex series of cellular behaviours and interactions, all ultimately dependent on cellular proteins. These include cell division, cell determination, cell shape changes, and cell sorting and movement (Gerhart et al. 1982; Wessells 1982; Maynard Smith 1983). Increase in morphological complexity thus arises by epigenetic effects, in an apparently hierarchical fashion. Though biologists are still far from understanding the relations between genetics and developmental morphology, an enormous investment of research effort is being expended in these fields and good reviews of the underlying principles and problems, set in an evolutionary context, are fortunately available (see Bonner 1982; Goodwin et al. 1983; Raff & Kaufmann 1983), though again much of the work is purely vertebrate- and insect-orientated. Nevertheless from such work it is increasingly apparent that the developing organism is itself a ‘target’ for evolutionary change and that developmental processes may directly affect the expression of mutational genomic changes (Lewin 1981). This is clearly not the place to consider such issues in any detail, but it should be borne in mind that new insights in genetics are beginning to have profound effects on our appreciation of the role of embryology in evolution and hence in phylogeny, and that further shifts of view are very likely over the next few years.

Introduction

Phylogenetic study is important, and is possible. There is a right answer to the question of how all the familiar living animals are related to each other; they do, at some point in the past, share common ancestral forms. And looking for that right answer, though it is surrounded by much theoretical debate, is not purely a matter of academic speculation. The search in itself is feasible, for there are many clues and possible sources of evidence; furthermore, the search is informative and, above all, interesting. This book is written to try to convince both students and teachers of these views, and to introduce new insights and sources of evidence that bear on the problem, particularly from the application of technological innovations.

However, there are several other related reasons for a book of this kind. Firstly, phylogenetic study is in itself a serious and stimulating challenge for any zoology student seeking to understand the patterns and principles of animal evolution. Very few courses in vertebrate zoology are conducted without a sound phylogenetic framework, yet it seems that when the other 99% of animals – the invertebrates – are at issue we are only too often quite happy to leave phylogeny aside. Many courses now consider the invertebrates independently of their evolutionary framework, or with such a meagre (and quite probably incorrect) treatment of the degrees of relationship that little or no underlying pattern can be perceived.