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7 - Acanthocephala: the thorny-headed worms
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
The acanthocephalans (Greek, acanthothorn, cephalahead), or so-called ‘thorny-headed worms,’ are a relatively small group of obligatory intestinal endoparasites comprising approximately 1100 described species. Adult acanthocephalan body lengths are variable, ranging from 1 mm in size to greater than 60 cm. Acanthocephalans were first described in 1684 by Francesco Redi, an Italian physician (Box 1.1), who reported finding white worms (probably Acanthocephalus anguillae) with hooked anterior ends in the intestines of European eels. Since then, adult acanthocephalans have been reported from all classes of vertebrate animals, in marine, freshwater, and terrestrial habitats.
As the phylum name suggests, acanthocephalans have an anterior hooked proboscis that acts as a retractable holdfast, which anchors adults into the intestines of their vertebrate hosts. They are similar in some respects to other intestinal worms; like the tapeworms they have a tegument and lack a mouth or an intestine and are transmitted in food webs by trophic interactions. They also share features with the nematodes and possess a fluid-filled pseudoceolom, and are dioecious and sexually dimorphic, with females generally larger than males. However, acanthocephalans have a number of unique features that demonstrate their independent evolutionary history.
6 - Platyhelminthes: the flatworms
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
The phylum Platyhelminthes (Greek, platyflat, helminthesworm) includes at least 30 000 species. The phylum represents a large and diverse group of organisms, most of which are obligate parasites, living on, or in, most species of vertebrate and invertebrate animal. As the phylum name suggests, these worms are flattened dorsoventrally. They are without segmentation, although cestodes, or tapeworms, superficially appear otherwise. Cestodes are modular iterations, with each segment or proglottid being more like an individual within a colony since each is a complete sexual unit (Hughes, 1989). Moreover, there is no coelom or peritoneum as there are in truly coelomate, segmented animals such as the annelids. Platyhelminths may, or may not, possess an incomplete gut. They are without circulatory, skeletal, and respiratory systems. The functional and structural unit of their excretory/osmoregulatory system is a protonephridium, or flame cell (Fig. 6.1), so named for a tuft of cilia extending away from the cell body that resembles the flame of a burning candle. Most species are monoecious, but a few, such as the medically important schistosomes, are dioecious.
Parasitic platyhelminths are extraordinarily diverse in terms of their morphology, habitats, life cycles, and transmission adaptations. The ectoparasitic monogeneans of primarily fish and amphibians, for example, have direct life cycles, featuring a free-swimming oncomiracidium stage. On the other hand, all endoparasitic digenean trematodes (flukes) have remarkably complex life cycles with molluscs (mostly snails) as first intermediate hosts, in which free-swimming stages known as cercariae are produced by extensive asexual reproduction. Further, most trematodes (and many cestodes) incorporate a resting stage within a second intermediate host. This host is generally a potential prey item of the definitive vertebrate host in which the parasite matures. Thus, most trematodes and cestodes are transmitted via predator–prey interactions. To add to the complexity, and stressing the importance of trophic transmission and food web dynamics, still other trematodes and cestodes have added third intermediate, or often, paratenic hosts to their life cycles. How and why such life cycle complexity evolved in the Platyhelminthes has long been the subject of debate (reviews in Cribb et al., 2003; Parker et al., 2003). As we will see in this, and several subsequent chapters, many species of platyhelminth are utilized as model systems for addressing questions in ecological, evolutionary, and environmental parasitology (see Chapters 12–17).
16 - Evolution of host–parasite interactions
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
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This chapter synthesizes the evolutionary significance of parasites on their hosts. As such, it marks the logical transition from the previous chapter by asking whether parasite-induced effects on host individuals and populations translate to evolutionary-level effects. Our focus is on microevolutionary phenomena. In the first section, we evaluate the empirical evidence that parasites mediate natural selection on specific host traits, and whether this process leads to an evolutionary response. In the next section, we synthesize studies on the population genetic structure of parasites. Here, our focus is on the manner in which genetic variation is distributed within and among parasite populations, and how patterns of genetic structuring can provide insight into the roles that microevolutionary phenomena such as genetic drift and gene flow play in natural host–parasite systems. In the final section, we introduce the phenomenon of host–parasite coevolution. Here, we evaluate the evidence for reciprocal evolution between hosts and parasites within natural host–parasite combinations. We conclude this section by considering how the microevolutionary interplay between hosts and parasites over many generations can help us understand how parasites evolved, and potentially cospeciated with their hosts, over longer time scales.
11 - Arthropoda: the joint-legged animals
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
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The phylum Arthropoda (Greek, arthrojointed, podafoot) comprises the most abundant and diverse of all animals, with more species than all other animal groups combined. One group alone, the insects, likely includes well over 5 000 000 species, although ‘only’ about 1 000 000 have been described (Gullan & Cranston, 2010). Arthropods have an extraordinarily rich fossil record that extends back to the Cambrian period. Since then, arthropods have undergone a phenomenal adaptive radiation and exploit virtually every conceivable habitat on earth. Within these habitats, arthopods are of ecological significance, playing many integral ecosystem functions. As free-living animals, as micropredators, and as mutualists and parasites, they are of massive evolutionary importance, driving the evolution of countless other organisms. Arthropods are also of economic importance to humans. Many are sources of food, while others are direct competitors for our food or destroy valuable products, and can be devastating pests. Life on earth would not exist as we know it, were it not for arthropods.
Arthopods feature prominently in parasitology. Thus, we have learned in previous chapters that arthropods can act as intermediate hosts for a variety of parasites, demonstrating their importance in food web relationships and predator–prey interactions. We have also discovered that many arthropods are micropredators and act as vectors for many species of protist and nematode parasites infecting vertebrates. Given their diversity, it should come as no surprise that a substantial number of arthropods have also evolved a parasitic life style. Most are ectoparasitic, with exquisite morphological adaptations for attachment to a host. Others are endoparasitic and live within a host. Our focus in this chapter is to present an overview of the biology of ectoparasitic and endoparasitic arthropods, especially the crustaceans, arachnids, and insects. These three groups include over 95% of all arthropod species (Pechenik, 2010). While some of these parasites resemble their free-living ancestors, we will encounter others that rival the most bizarre and highly specialized of any of the parasitic animals that we have discussed up to now.
5 - Myxozoa: the spore-forming cnidarians
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
The myxozoans are highly specialized, multicellular, spore-forming parasites primarily of marine and freshwater fishes. In vertebrate hosts, they are mostly site-specific and found in cavities such as the gall bladder, urinary bladder, and ureters, or in tissues such as cartilage, muscle, gills, and skin. For this reason, myxozoans are often classified as being either coelozoic (inhabiting cavities) or histozoic (within tissues). Approximately 2200 species in 62 genera have been described; many more await discovery. A tremendous amount of research has been, and is currently, devoted to these enigmatic parasites. As such, our understanding of the biodiversity, ecology, evolution, and systematics of the Myxozoa has been greatly enhanced (Okamura & Canning, 2003; Canning & Okamura, 2004; Fiala & Bartošová, 2010).
One of the reasons for the wealth of scientific interest is that several myxozoans are serious fish pathogens. Myxobolus cerebralis, the causative agent of whirling disease in salmonid fishes (see Box 5.1), and Kudoa thyrsites, the cause of post-mortem myoliquefaction in various marine fishes, are two examples of well-studied myxozoans having significant economic impacts in sports fisheries and/or the aquaculture industry (reviews in Kent et al., 2001; Yokoyama, 2003; Fiest & Longshaw, 2006). Although many fish myxozoans can be pathogenic, several others are valuable as biological tags in fish stock discrimination and in determining fish migration routes.
Plate section
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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15 - Effects of parasites on their hosts: from individuals to ecosystems
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
Parasitologists have long been interested in the extent to which parasites affect their hosts. While the historical focus has been at the scale of host individuals and host populations, enquiries that span the range from genome-level effects to ecosystem-level effects are increasingly common. The early focus on host individuals and populations likely arose from the need for clinical parasitologists to characterize and control important human and veterinary pathogens. Indeed, a key direction of modern studies, aided by the explosion in molecular methodologies, is to determine the mechanisms of pathology that occur at the host–parasite interface and to assess their consequences on host individuals and populations. We included this perspective in our coverage of the general biology of human parasites such as Plasmodium spp., Trypanosoma spp., Schistosoma spp., and Trichinella spiralis in earlier chapters.
Beginning in the 1970s, interest in the influence of parasites on their hosts was extended to include wildlife and other animals. An important milestone was the theoretical treatments initiated by Crofton (1971) and later by Anderson & May (1978) and May & Anderson (1978) that included alpha (the rate of parasite-induced host mortality) as a key epidemiological parameter (see Chapter 12). Although difficult to do, research focused on estimating alpha for a range of host–parasite interactions and evaluating how ecological conditions could affect its magnitude. This emphasis had a powerful impact on the integration of parasitology and wildlife disease ecology into mainstream ecology, conservation biology, and wildlife management. But perhaps most importantly, these theoretical treatments shifted the emphasis away from medical and host-centered views of parasite-induced effects to more parasite-centered views that placed variation in alpha into the context of variation in the ways in which parasites exploit their hosts (Poulin, 2007). In so doing, the question of ‘effects’ has developed into one of the leading questions in our field, requiring integration among parasitologists and researchers from every conceivable subdiscipline in biology, particularly ecology and evolutionary biology.
Dedication
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Contents
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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2 - Immunological aspects of parasitism
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
One unifying characteristic of most organisms is their ability to distinguish entities of their own bodies from entities that are genetically different. This ability to distinguish ‘self’ from ‘non-self’ originated in the deepest roots of the Tree of Life, when natural selection favored individual prokaryotes that could phagocytize potential food and not kin or potential mating partners. Likewise, sexual reproduction, another unifying characteristic on almost all branches of the Tree of Life, requires the recognition of appropriate gametes. The processes underlying recognition of self/non-self are undoubtedly complex, as we will see, but they fundamentally require intimate, molecular-level interactions at the interface (usually on cell surfaces) between two unrelated partners. Herein lies the foundation of one of the key processes that defines biological systems: cell–cell communication, and the ability for all organisms to protect themselves from potential invaders, both abiotic and biotic, via immunity.
In the introductory chapter, we alluded to the phenomenal success of the parasitic way of life. In a sense, this success should not surprise us. Individuals that adopt a life style that avoids predators and diseases, that provides access to potentially limitless resources, that provides access to mates, and so on, should be favored by natural selection. Yet, all organisms that adopt this life style confront the constraint of avoiding (or limiting) immunological defenses (and other host defenses, see Chapter 16), many of which can drive parasite reproductive success to zero. Thus, the host immune response represents a critical selective force on individual parasites. As we will see later in this chapter, and throughout this book, the manner in which parasites evade the sophisticated host immune response has major consequences to human health and to the development of parasite control strategies.
Parasitism
- The Diversity and Ecology of Animal Parasites
- 2nd edition
- Timothy M. Goater, Cameron P. Goater, Gerald W. Esch
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Reflecting the enormous advances made in the field over the past ten years, this text synthesizes the latest developments in the ecology and evolution of animal parasites against a backdrop of parallel advances in parasite systematics, biodiversity and life cycles. This second edition has been thoroughly revised to meet the needs of a new generation of parasitology students. Balancing traditional approaches in parasitology with modern studies in parasite ecology and evolution, the authors present basic ecological principles as a unifying framework to help students understand the complex phenomenon of parasitism. Richly illustrated with over 250 figures, the text is accompanied by case study boxes designed to help students appreciate the complexity and diversity of parasites and the scientists who study them. This unique approach, presented clearly and with a minimum of jargon and mathematical detail, encourages students from diverse backgrounds to think generally and conceptually about parasites and parasitism.
3 - Protista: the unicellular eukaryotes
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
The protists (Greek, the very first), also referred to as the protozoans (Greek, protofirst, zoaanimals), comprise a spectacular diversity of unicellular, eukaryotic organisms possessing organelles such as a membrane-bound nucleus, mitochondria, chloroplasts, Golgi, etc., found in the metazoan plants and animals. There is considerable evidence that eukaryotic protists evolved by a process of sequential endosymbiosis of prokaryotes (see Box 3.1, as well as Margulis (1981) for a discussion of the theory). The Kingdom Protista was erected almost 150 years ago by the famous German zoologist Ernst Haeckel in an attempt to accommodate this diversity. Today, with considerable ultrastructural, genetic, and biochemical research and the molecular phylogenetic revolution, it is now known that unicellular animals are distributed among all kingdoms. There is no longer a formal taxonomic category called the Protista. However, ‘protist’ is still widely used as a general term (as is ‘protozoan’) when referring to this diversity of unicellular eukaryotes, even though neither of these terms implies monophyletic origins.
Within the confines of a single cell membrane (= plasmolemma), these organisms have undergone an enormous adaptive radiation. This single cell functions as a complete organism. Protists are not simple; they feed, move, behave, and reproduce, and, thus, can be considered more complex and versatile than our own cells! Complexity arises from the specialization of organelles. Protists have evolved a bewildering array of morphologies, physiologies, behaviors, reproductive strategies, life histories, and nutritional and locomotory modes. In short, the diversity of protist form and function rivals that encountered among all other animals combined.
10 - Pentastomida: the tongue worms
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
The pentastomids (Greek, pentafive, stomamouth), or tongue worms, are a small group of obligatory parasites that includes about 130 species. The taxonomic name was erroneously coined in the belief that each of the hooked appendages that flank the true mouth had a mouth. Some species supposedly resemble a miniature vertebrate tongue. Adult pentastomids are found primarily in the respiratory passages of terrestrial vertebrates, mostly reptiles. They range in size from a few millimeters to 15 cm in length. Approximately 70% of the definitive hosts for pentastomes are snakes; several pentastome species have also been described from lizards and freshwater turtles and crocodilians. Relatively few adult pentastomes have been described from amphibians, birds, or mammals, although some species are reported from such unusual sites and hosts as the air sacs of marine birds, the trachea of vultures, and the nasopharynx and sinuses of canines and felines. Raillietiella is the most speciose pentastome genus and is the only one known to mature in amphibian hosts. The unique site specificity of pentastomes, coupled with their hematophagus feeding habit, large body size, and long-lived nature have inspired fascinating studies in parasite ecology and evolution (review in Riley, 1986). Particular focus has been on examining the mechanisms by which these large parasites evade their vertebrate host’s immune response (reviews in Riley, 1992; Riley and Henderson, 1999; see Box 10.1).
17 - Environmental parasitology: parasites as bioindicators of ecosystem health
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
Parasites comprise the most significant component of our planet’s biodiversity, and are integral components of all ecosystems, often playing pivotal ecological and evolutionary roles. We hope you have been convinced by previous chapters that, for example, parasites may influence the biology of their hosts in a myriad of ways. Many parasites manipulate the phenotypes of their hosts dramatically. Some parasites have been shown to also regulate host populations. Others can impact the evolution of their hosts and act as powerful agents of natural selection. Parasites can mediate the competitive interactions between free-living animals and act as ‘cryptic determinants of animal community structure’ (Minchella & Scott, 1991). It is not surprising that concepts such as ‘keystone parasite’ and ‘ecosystem engineer’ have been applied to parasitic animals, alluding to their significant ecological roles in nature (e.g., Thomas et al., 1999; see Chapter 15). Indeed, there is increasing evidence that, paradoxically, the ‘healthiest’ ecosystems are those which are rich in parasites, due to their influence on a range of ecosystem functions, their important roles in food web structure and function, and as ‘drivers’ of biodiversity (reviews in Marcogliese, 2005; Hudson et al., 2006).
In addition to these diverse ecological and evolutionary roles, recall that parasites are also widely studied from an applied perspective, e.g., as biological tags in fisheries stock management (see Chapter 14), and as indicators of complex food web interactions (e.g., Marcogliese & Cone, 1997a). This chapter reviews yet another contribution of parasites, as posed by Lafferty (1997), “What can parasites tell us about human impacts on the environment?”
1 - Introduction
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
Encounters with parasites
On a fateful spring day in a small northern Canadian town in the 1970s, two of the authors (the two that are related) of this text came upon a sickly red fox. Following some foolhardy thinking, they handled the fox and carried it home. A few days later, health officials diagnosed the fox with rabies. To avoid the fatal consequences of the disease, the brothers required daily intramuscular injections of the prophylactic drug that was used at the time. We recall the episode with memories of pain, dismay from parents, and ruthless teasing from our friends. And so goes our introduction to the world of parasites. So too goes our introduction to the phenomenon of parasitism. Readers might envision two teenagers discussing how their predicament arose: How did that fox get infected? Why was the fox population, but not the racoon population, so heavily infected that year? How does the virus migrate from the site of a wound, to the brain, to saliva? How, and why, does it transform a normally secretive and nocturnal animal into one that is aggressive and diurnal? There are obvious parallels between these early queries and modern questions associated with host specificity, parasite site selection, the geographical mosaic of coevolution, and mechanisms of alterations in host behavior.
9 - Nematomorpha: the hairworms
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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The common name of the nematomorphs, ‘horsehair worm’ or ‘hairworm,’ arises from their long filariform, cylindrical morphology. Adult body size among the approximately 350 described species varies considerably, ranging from a few centimeters in length to over 2 m. Nematomorphs are dioecious and the large adults (Fig. 9.1) are free-living in aquatic habitats, mostly permanent freshwater lakes, ephemeral ponds, and streams. In contrast, juvenile nematomorphs are obligate parasites within the hemocoel of arthropods, a characteristic they share with the mermithid nematodes (see Chapter 8). The juveniles of almost all described nematomorphs are parasitic in terrestrial arthropods (the gordiids), whereas the remainder (the nectonematids) are parasites of marine invertebrates, especially crustaceans. Nematomorphs are often referred to as gordiids or Gordian worms on account of the tangled mass of swarming adults (Gordian knots) that are frequently observed in shallow aquatic habitats. Compared to the mermithids and their potential for biological control of insect pests and vectors, the nematomorphs are a poorly studied group. Following the first completion of a nematomorph life cycle under laboratory conditions (Hanelt & Janovy, 2004b), significant advances have been made in our understanding of the ecology, systematics, and life cycles of this enigmatic taxon (review in Hanelt et al., 2005). The facilitation of nematomorph transmission between its parasitic larval stage and its free-living adult stage in water is now a well-known case of parasite-induced alteration in host behavior (see Chapter 15, Color plate Fig. 8.3).
List of boxes
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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4 - Microsporida: the intracellular, spore-forming fungi
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Summary
General considerations
Following decades of taxonomic upheaval, strong molecular phylogenetic evidence now indicates that the phylum Microspora is a monophyletic lineage within the Kingdom Fungi (review in Corradi & Keeling, 2009). Members of this clade are obligate, intracellular, spore-forming parasites. The unique and distinctive spores of these unicellular eukaryotes are minute, ranging from 2 to 20 µm in length. Although they are eukaryotic, microsporidian cells have several unusual characteristics, including a lack of organelles such as flagella, peroxisomes, mitochondria, and Golgi apparatus. Microsporidians also have 16S rather than 18S ribosomes. However, despite their relative simplicity, they can also be considered as marvels of structural and functional complexity, possessing adaptations for survival while outside their host, and also for intracellular parasitism. Within the spore is a diagnostic, exquisite extrusion apparatus, adapted for the penetration of host cells.
Louis Pasteur described the first microsporidian in the mid nineteenth century. He showed that Nosema bombycis caused ‘pebrine disease’ in silk-moth larvae, and provided recommendations to European silkworm farmers regarding control. Currently, a total of approximately 1300 species of microsporidians in 160 genera have been described. Following from modern advances in molecular diagnostics, it is likely that many more species await discovery. While most microsporidians are parasites of insects, they infect a wide range of other invertebrates, including nematodes, molluscs, annelids, and crustaceans. Microsporidians are present within all five classes of vertebrates, with 14 genera described from teleost fishes alone. Research involving microsporidians has traditionally focused on economically important species of insects (e.g., Nosema spp., review in Wittner & Weiss, 1999) and fish (e.g., Loma spp., review in Dyková, 2006). In recent years, this focus has expanded to include microsporidians that have been implicated as causative agents of opportunistic infections and emergent diseases in humans (review in Weiss, 2001).
Index
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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Glossary
- Timothy M. Goater, Cameron P. Goater, University of Lethbridge, Alberta, Gerald W. Esch, Wake Forest University, North Carolina
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