The Biology and Identification of the Coccidia (Apicomplexa) of Marsupials of the World

Donald W. Duszynski

• Publisher: Academic Press
• Year: 2015
• Print ISBN: 9780128027097
• eBook ISBN: 9780128027127
• Topic: Medicine
• Subtopic: Medical Microbiology & Parasitology

The Biology and Identification of the Coccidia (Apicomplexa) of Marsupials of the World contains the most up-to-date information on the former order marsupial that is now partitioned by mammalogists into seven separate orders that contain 20 families, 86 genera, and 318 species that live on land or in trees in Oceania and the Americas.Marsupials, like other vertebrate animals have many different kinds of parasites (e.g. viruses, protozoa, worms, arthropods, etc.), but there is no definitive text that covers any one of these groups found in all marsupials.Coccidiosis is a serious global problem in most domesticated animals, and under increasing circumstances of loss of habitat and crowding, may also affect some wild animal populations, thus, there is a real need for their identification and control.- Offers line drawings and photomicrograph of each parasite from each hosts species, including methods of identification and treatment- Presents a complete historical rendition of all known publications on coccidia (and their closest relatives) from all marsupials species on Earth, and evaluates the scientific and scholarly merit of each- Provides a complete species analysis of the known biology of every coccidian described from marsupials- Reviews the most current taxonomy of marsupials and their phylogenetic relationships needed to help assess host-specificity and evaluate what little cross-transmission work is available

Chapter 1

Introduction

Abstract

This chapter presents a simple overview of the phylum Apicomplexa and its principal component taxa that are covered in the remaining chapters. Although most of this book deals with the morphology of the most readily available exogenous stage (sporulated oocyst) of these apicomplexan species, morphometrics alone are no longer sufficient to identify many coccidian species such as Cryptosporidium and Sarcocystis, which have very small oocysts and sporocysts, with insignificant structural characters to distinguish them. In addition to morphology, identifications now should be supplemented with detailed biological information (e.g., endogenous developmental stages, cross-transmission studies, etc.), and as much molecular data as can be incorporated from amplification of DNA, sequencing of gene fragments, and phylogenetic analysis of those sequences.

Keywords

Besnoitia; Coccidia; Cryptosporidium; Cystoisospora; Eimeria; Klossiella; Marsupials; Sarcocystis; Species; Systematics; Taxonomy; Toxoplasma

 

There have been a number of review articles, monographs, and books on the coccidian parasites of several vertebrate host groups that precede this one; they are listed in the Preface. Like the others, this book is intended to be the most comprehensive discourse, to date, describing the structural and biological knowledge on the coccidian parasites (Apicomplexa) that infect marsupials.

The phylum Apicomplexa Levine, 1970, was created to provide a descriptive name that was better suited to the organisms contained within it than was the long-used Sporozoa Leuckart, 1879. The latter name became unsuitable and unwieldy, because it was a catch-all category for any protist that was not an amoeba, a ciliate, or a flagellate; thus, it contained many organisms that did not have “spores” in their life cycle, as well as many groups, such as the myxo- and microsporidians, that were not closely related to the more traditional sporozoans, such as malaria and intestinal coccidia. Two things about this phylum name bear mentioning. First, it was not possible to create the name for, and classify organisms in, the phylum until after the advent of the transmission electron microscope (TEM). The widespread use of the TEM in the 1950s and 1960s, examining the fine structure of “zoites” belonging to many different protists, revealed a suite of common, shared structures (e.g., polar ring, conoid, rhoptries, etc.) at one end (now termed anterior) of certain life stages; these structures, in whatever combination, were termed the apical complex. When parasitic protozoologists sought a more unifying and, hopefully, more phylogenetically relevant term, Dr Norman D. Levine, from the University of Illinois, came up with “Apicomplexa.” Unfortunately—and this is only my opinion—the name is incorrect because it means, “complex bee,” having the prefix, Api- (L), a bee. When Levine created the name he should have coined Apicalcomplexa, with the prefix Apical- (L), meaning “the top,” or “at the top.” No matter; the phylum Apicomplexa is almost universally recognized now as a valid taxon.

Within the Apicomplexa, the class Conoidasida Levine, 1988 (organisms with all organelles of the apical complex present), has two principal lineages: the gregarines and the coccidia. Within the coccidia, the order Eucoccidiorida Léger and Duboscq, 1910, is characterized by organisms in which merogony, gamogony, and sporogony are sequential life cycle stages, and they are found in both invertebrates and vertebrates (Lee et al., 2000; Perkins et al., 2000). There are two suborders in the Eucoccidia: Adeleorina Léger, 1911 and Eimeriorina Léger, 1911. Species within the Eimeriorina differ in two biologically significant ways from those in the Adeleorina: (1) Their macro- and microgametocytes develop independently (i.e., without syzygy); and (2) their microgametocytes usually produce many microgametes versus the small number of microgametes produced by microgametocytes of adeleids (Upton, 2000). Coccidians from these two groups are commonly found in the marsupials that have been examined for them, and are represented by about 86 species that fit taxonomically into seven genera in four families. In the Adeleorina: Klossiellidae Smith and Johnson, 1902, 11 Klossiella species; and in the Eimeriorina: Cryptosporidiidae Léger, 1911, 6 Cryptosporidium species; Eimeriidae Minchin, 1903, 56 Eimeria and 1 Isospora species; Sarcocystidae Poche, 1913, 1 Besnoitia, 10 Sarcocystis species, and Toxoplasma gondii.

The taxonomy and identification of coccidian parasites used to be a relatively simple affair based on studying the morphology of oocysts found in the feces. Morphology of sporulated oocysts is still a useful tool, as demonstrated in this book by most of the Eimeria and Isospora species now known from marsupials. My interest here is not just in taxonomy per se, but simply to derive as robust and reasonable a list of all apicomplexan species that occur naturally in marsupials, and use the gastrointestinal or urinary tracts to discharge their resistant propagules.

However, morphology alone is no longer sufficient to identify many coccidian species, especially those in genera such as Cryptosporidium and Sarcocystis, which have species with oocysts and sporocysts, respectively, that are very small in size and have an insignificant suite of structural characters. In addition to morphology, identifications now should be supplemented with as much knowledge as can be gleaned from multiple data sets including, but not limited to, location of sporulation (endogenous vs exogenous), length of time needed for exogenous sporulation at a constant temperature, morphology and timing of some or all of the developmental stages in their endogenous cycle, length of prepatent and patent periods, host-specificity via cross-transmission experiments, observations on histological changes, and pathology due to asexual and sexual endogenous development, and others, to clarify the complex taxonomy of these parasites. Amplification of DNA, sequencing of gene fragments, and phylogenetic analysis of those sequences are now sometimes needed to correctly assign a parasite to a group, genus, or even species (e.g., see Merino et al., 2008, 2009, 2010). Thus, there seems a clear need to use molecular tools to ensure accurate species identifications in groups where it is needed most, if we are to truly understand the host–parasite associations of these species and genera.

It needs to be kept in mind, however, that molecular data alone are insufficient for a species description and name, although their use as a valuable tool can help sort out many taxonomic problems. For example, molecular methods helped differentiate between the Isospora species with and without Stieda bodies; those with Stieda bodies share a phylogenetic origin with the eimeriid coccidia, while those without Stieda bodies may best be placed in the Cystoisospora (Carreno and Barta, 1999). Molecular techniques also have helped resurrect some genera (Modrý et al., 2001), and have allowed proper phylogenetic assignment when only endogenous developmental stages were known (Garner et al., 2006). Tenter et al. (2002) proposed that we need an improved classification system for parasitic protists, and that to build one we need to include molecular data to supplement morphological and biological information. Such combined data sets will enable phylogenetic inferences to be made, which in turn will result in a more stable taxonomy for the coccidia. We seem to slowly be moving in the right direction.

As a quick overview, Chapter 2 presents some basic information about the physical characteristics of marsupials, and recent thoughts on how and when they evolved. Chapters 3, 4, and 5 cover the 56 Eimeria and 1 Isospora species in the Eimeriidae (Eimeriorina) that have been reported from the three marsupial orders (Didelphimorphia, Diprotodontia, and Peramelemorphia) in which they were found. In Chapter 6, I outline what we know about the 11 Klossiella species in the Klossiellidae (Adeleorina) known from marsupials. Along with the Eimeriidae, the other important apicomplexan family is the Sarcocystidae; it has two subfamilies, Sarcocystinae Poche, 1913 (Sarcocystis) and Toxoplasmatinae Biocca, 1957 (Besnoitia, Toxoplasma, others). These are covered separately in Chapters 7 and 8, respectively. Chapter 9 documents the six Cryptosporidium species known to date from marsupials. Chapter 10 entitled Species Inquirendae, details all of the apicomplexans that have been mentioned to occur in marsupials, but from which there is not enough clear documentation to label them “species” that really exist in nature. Chapter 11 offers a brief summary of the salient data and ideas presented in the previous chapters, and reiterates some of those topics/issues discussed in previous works, including an overview of where we stand now regarding examining vertebrate hosts for apicomplexans. The formal chapters are followed, in order, by three Tables (11.1. parasite–host; 11.2. host–parasite; 11.3. eimeriid oocyst/sporocyst features), a Glossary and a List of Abbreviations, a complete list of all references cited, and an Index.

Throughout the chapters of this book, I use the standardized abbreviations of Wilber et al. (1998) to describe various oocyst structures: length (L), width (W), and their ratio (L/W), micropyle (M), oocyst residuum (OR), polar granule (PG), sporocyst (SP) L and W and their L/W ratio, Stieda body (SB), substieda body (SSB), parastieda body (PSB), sporocyst residuum (SR), sporozoite (SZ), refractile body (RB), and nucleus (N). Other abbreviations used, as well as definitions of some terms that may be unfamiliar, are bolded in the text and are found in the Glossary. All measurements in the chapters are in micrometers (μm) unless indicated otherwise (usually in mm).

Chapter 2

Review

Marsupials and Marsupial Evolution

Abstract

This chapter introduces marsupials and distinguishes them from placental mammals by pointing out some of their unique anatomical and physiological characters of reproduction (marsupium, bifid reproductive tracts, etc.). It also points out that we have not yet identified all marsupials, as their numbers of species continue to increase the more we study them. Recent discoveries in molecular studies, especially the discovery of repetitive fragments of DNA called retroposons, have given molecular systematists virtually an ambiguity-free tool to approximate evolutionary history. Additionally, two recently sequenced marsupial genomes, a South American opossum and an Australian wallaby, along with the use of retroposed elements, allow systematists the unique opportunity to help resolve marsupial and eutherian mammal relationships. Finally, Australian marsupials have been isolated geographically from their American counterparts for millennia. However, human fascination with zoos and the pet trade allows the movement of marsupials and many other animals across oceans and continents, creating an interface where humans, domesticated animals, marsupials, and all of their parasites can come in contact, creating new zoonoses.

Keywords

American marsupials; Ameridelphia; Australian marsupials; Australidelphia; Comparative genomics; Evolution; Metatheria; Retroposons; Unique reproductive characters; Zoonoses

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Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Dedication
• Preface and Acknowledgments
• Chapter 1. Introduction
• Chapter 2. Review: Marsupials and Marsupial Evolution
• Chapter 3. Order Didelphimorphia—Eimeriidae
• Chapter 4. Order Diprotodontia—Eimeriidae
• Chapter 5. Order Peramelemorphia—Eimeriidae
• Chapter 6. Adeleidae in Marsupials
• Chapter 7. Sarcocystidae: Sarcocystinae (Sarcocystis) in Marsupials
• Chapter 8. Sarcocystidae: Toxoplasmatinae (Besnoitia, Toxoplasma) in Marsupials
• Chapter 9. Cryptosporidiidae: Cryptosporidium in Marsupials
• Chapter 10. Species Inquirendae in Marsupials
• Chapter 11. Discussion, Summary, and Conclusions
• References
• Glossary and Abbreviations
• Index