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 THE BIOLOGY AND
IDENTIFICATION OF THE
COCCIDIA (APICOMPLEXA) OF
MARSUPIALS OF THE WORLD

Donald W. Duszynski
Professor Emeritus of Biology, The University of New Mexico
Albuquerque, NM, USA

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 Dedication

This book is dedicated to the Spirit of Inter- Ryan, Division of Veterinary and Biomedical
national Cooperation of my colleagues who work Sciences, Murdoch University, Western Austra-
on marsupials and their protist parasites, both in lia, and Dr Michelle Power, Department of Bio-
Australia and in the Americas. logical Sciences, Macquarie University, Sydney,
Australia. About 20 years ago, when I first NSW. I have known and admired Una for a long
began trying to archive every known reprint on time, and she has helped me in other publica-
the coccidia of vertebrates, Dr Mick O’Callaghan tions to understand the current molecular litera-
(now retired), Central Veterinary Laboratories, ture on Cryptosporidium. I had the great opportu-
Department of Agriculture, Adelaide, South nity, a few years ago, to meet Michelle only once,
Australia, sent me the negatives of many of the when she was visiting Dr Robert Miller’s labora-
Eimeria species that he and his colleagues had tory in Biology at the University of New Mexico.
described from a variety of macropodid hosts. I’m sure I bored her to tears with my diatribe
Many of these had never been published, and about the many, seemingly insoluble, problems
I am fortunate to be able to share these new we face working with the coccidia. I think these
images (photomicrographs) of previously de- two young scientists are doing some of the most
scribed Eimeria species in this book. Professor interesting, insightful, and careful work in mo-
Peter O’Donoghue, Department of Microbiolo- lecular parasitology today. They are developing
gy and Parasitology, University of Queensland, protocols to better help us understand the genet-
Brisbane, offered me access to his professional ic diversity of Cryptosporidium species that have
library and helped me retrieve some of the very so few structural details of their oocysts that
early reprints that were unavailable to me. Pro- they are impossible to distinguish morphologi-
fessor Ian Beveridge, Faculty of Veterinary Sci- cally. Their work has many applications to other
ence, University of Melbourne, NSW, sent me coccidian groups, especially Sarcocystis species,
original reprints of several of his papers that in which the exogenous sporocysts are all nearly
I only had as badly printed copies. It’s much identical, and the protocols to be able to distin-
easier to extract images from the original glossy guish cryptic Eimeria species that may have very
reprint. He also sent me a spread sheet of all the similar-looking sporulated oocysts in sometimes
Klossiella species he had worked on, to ensure I distantly related hosts. I feel truly honored to
didn’t miss any of the descriptions. Dr Ian Barker, know all of these people.
Institute of Medical and Veterinary Science, The Americas. There are three individuals I
Adelaide, South Australia, immediately volun- want to thank and make special reference to.
teered to help me in every way he could when In Brazil, Dr Ralph Lainson, Departamento
he learned that I was writing this book, offering de Parasitologia, Instituto Evandro Chagas,
anything of his that I needed, from plates used Belém, has been a friend and colleague ever
in his previous papers to any negatives he pos- since Steve Upton and I visited him in the
sessed in his files. These guys have been friends Belém hospital (his appendix ruptured a day or
for decades, and they always are eager to help two before we arrived to visit his laboratory!),
colleagues solve problems. I need to mention and he always has been eager to cooperate
two other Australian parasitologists: Dr Una with reprint requests and permission to use his
vi DEDICATION

drawings and photomicrographs in our various cient literature on Sarcocystis species, Dr J.P.
research endeavors. In Costa Rica, Professor Dubey, United States Department of Agricul-
Misael Chinchilla, Research Department, Uni- ture, Agricultural Research Service, Parasite
versidad de Ciencias Médicas (UCIMED), San Biology, Epidemiology, and Systematics Labo-
José, Costa Rica, was kind enough to include ratory, Beltsville, Maryland, was kind enough
me in the work he was doing with Dr Idalia to help locate several older publications for me
Vanlerio, also at UCIMED, involving one of the and, in addition, he sent me a Word.doc copy of
eimerians cited in this book, Eimeria marmoso- his soon-to-be-published revision of Sarcocysto-
pos. Their landmark experimental work with sis of Animals and Man.
this apicomplexan established the first complete If the rest of the world’s humans could be this
endogenous life cycle known for any of the 56 welcoming and willing to understand and coop-
Eimeria and 1 Isospora species described to date erate in helping others to solve their problems,
from marsupials. Finally, in the USA, when I it’d be a better planet on which to live. Everyone
was struggling to locate some of the very an- should be a parasitologist!
 Preface and Acknowledgments

When I was in graduate school at Colorado Monographic research; (2) Training students
State University, working on coccidia in Bill in taxonomic method; and (3) Computer infra-
­Marquardt’s laboratory (1966–1970), the “Bible structure. We had all those pieces in place at
on Coccidia” at that time was László Pellérdy’s University of New Mexico (UNM), so I submitted
Coccidia and Coccidiosis (1965). Our library had only a proposal, and in 1995, I was honored to be
one copy, and there was constant competition in the first cohort of PEET recipients to begin
among Bill’s graduate students to see who could work on “The Coccidia of the World (DBS/
check it out, and keep it for the longest period of DEB-9521687).” Professor Pellédy’s “Bible” had
time. I don’t know why I remember that. an obvious influence on that title. My colleague
Long after being hired (1970) at the Univer- from Kansas State University (and former grad-
sity of New Mexico, progressing through the uate student), Dr Steve Upton, was my co-PI.
ranks, serving a decade as chairman of Biol- Together, Steve and I were able to visit many of
ogy, hiring 18 faculty members, and having the the labs doing research at the time on ­coccidian
good fortune to be surrounded by a cohort of taxonomy and systematics (Australia, Brazil,
my marvelous graduate students, I was rein- France, Hungary, Russia, others), and set up
vigorated (1991) to get back into my research on our network for cooperative interactions for the
the coccidia, and to a make a meaningful contri- future. The Coccidia of the World online data-
bution to coccidian biology, taxonomy, and sys- base, which many who may read this book have
tematics. Fortunately, instead of Murphy (aka used (http://biology.unm.edu/coccidia/hom
Murphy’s Law), Serendipity intervened (my e.html), was one outcome of the PEET award
friend Terry Yates defined serendipity this way: (sadly, without current funding—although still
“Even a blind hog gets an acorn every now useful to many—it is now out of date, and is
and then!”). In 1992–1993, the National Science in desperate need of someone to take over its
Foundation (NSF) announced the first call for upgrade and management). A good number of
its new initiative, Partnerships for Establish- high school, undergraduate, and graduate stu-
ing Expertise in Taxonomy (PEET), to support dents benefited from this PEET initiative that,
research that targeted groups of poorly known in different ways, helped focus their careers in
organisms. The coccidia certainly passed that biology and/or parasitology. And our revision-
test. NSF designed PEET “to encourage the ary monographic work since 1998 resulted from
training of new generations of taxonomists and the foundation of historic reference materials
to translate current expertise into electronic that we acquired and archived over the years,
databases and other formats with broad acces- including marmotine squirrels (Wilber et al.,
sibility to the scientific community.” Three 1998); primates and tree shrews (Duszynski
major elements were required to submit a pro- et al., 1999); insectivores (Duszynski and Upton,
posal in the first PEET Special Competition: (1) 2000); Eimeria and Cryptosporidium in wild

xi
xii PREFACE AND ACKNOWLEDGMENTS

mammals (Duszynski and Upton, 2001), bats gave me permission to use, the original koala
(Duszynski, 2002); amphibians (Duszynski et al., photo that adorns the cover of this book. Thus,
2007); snakes (Duszynski and Upton, 2009), two colleagues and friends, whose professional
rabbits (Duszynski and Couch, 2013); turtles careers were in different places, at different
(Duszynski and Morrow, 2014); and this treatise times, and in quite different areas of biology,
on coccidia species known from marsupials. gave me the impetus to start this project. Some
We all stand on the shoulders of others. I am of the many shoulders I stand on are those of
most grateful to the following friends and col- my parasitology colleagues in Australia, and in
leagues, without whose acquaintance, friend- South, Central, and North America, who work
ship, and support this book would not have on the coccidian parasites of marsupials. They
been completed. I thank Lee Couch, friend impressed me so strongly with their willing-
and wife, Department of Biology, The UNM, ness to help me in every way, that I dedicate
for her help scanning, adjusting, and archiving this book to them so they can be individually
all the line drawings and photomicrographs named and thanked.
used in the species descriptions in this book, Finally, and once again, the steadfast profes-
and for proofreading and editorial suggestions. sional staff at Elsevier took my Word.docs and
Special thanks are due to Dr Norman D. Levine translated that ugly caterpillar into this lovely
(deceased) who, many years ago after his retire- book. I am especially grateful to Linda Versteeg-
ment from the University of Illinois, sent me a buschman, Acquisitions Editor; Halima Williams,
preliminary manuscript hand-typed on yellow Editorial Project Manager, Life Sciences; Julia
paper (ca. 1990), of a list of the coccidia then Haynes, Production, Project Manager, Mark Rog-
known from marsupials, and he suggested that ers, Designer, and Janice Audet, Publisher.
if I ever got some free time that this would be
a good project to undertake. To Dr Rob Miller, Donald W. Duszynski
colleague, friend, and current Chair of Biology Professor Emeritus of Biology
at UNM, who said last year, over a few beers, The University of New Mexico
“Why don’t you write your next book on the Albuquerque, NM 87131
coccidia of marsupials?” Rob also took, and February, 2015
 C H A P T E R

1
Introduction

There have been a number of review articles, end (now termed anterior) of certain life stages;
monographs, and books on the coccidian para- these structures, in whatever combination, were
sites of several vertebrate host groups that pre- termed the apical complex. When parasitic pro-
cede this one; they are listed in the Preface. Like tozoologists sought a more unifying and, hope-
the others, this book is intended to be the most fully, more phylogenetically relevant term, Dr
comprehensive discourse, to date, describing Norman D. Levine, from the University of Illi-
the structural and biological knowledge on the nois, came up with “Apicomplexa.” Unfortu-
coccidian parasites (Apicomplexa) that infect nately—and this is only my opinion—the name
marsupials. is incorrect because it means, “complex bee,”
The phylum Apicomplexa Levine, 1970, was having the prefix, Api- (L), a bee. When Levine
created to provide a descriptive name that was created the name he should have coined Apical-
better suited to the organisms contained within complexa, with the prefix Apical- (L), meaning
it than was the long-used Sporozoa Leuckart, “the top,” or “at the top.” No matter; the phylum
1879. The latter name became unsuitable and Apicomplexa is almost universally recognized
unwieldy, because it was a catch-all category for now as a valid taxon.
any protist that was not an amoeba, a ciliate, or Within the Apicomplexa, the class Conoida-
a flagellate; thus, it contained many organisms sida Levine, 1988 (organisms with all organelles
that did not have “spores” in their life cycle, as of the apical complex present), has two princi-
well as many groups, such as the myxo- and pal lineages: the gregarines and the coccidia.
microsporidians, that were not closely related to Within the coccidia, the order Eucoccidiorida
the more traditional sporozoans, such as malaria Léger and Duboscq, 1910, is characterized by
and intestinal coccidia. Two things about this organisms in which merogony, gamogony, and
phylum name bear mentioning. First, it was sporogony are sequential life cycle stages, and
not possible to create the name for, and clas- they are found in both invertebrates and ver-
sify organisms in, the phylum until after the tebrates (Lee et al., 2000; Perkins et al., 2000).
advent of the transmission electron microscope There are two suborders in the Eucoccidia:
(TEM). The widespread use of the TEM in the Adeleorina Léger, 1911 and Eimeriorina Léger,
1950s and 1960s, examining the fine structure 1911. Species within the Eimeriorina differ in
of “zoites” belonging to many different protists, two biologically significant ways from those in
revealed a suite of common, shared structures the Adeleorina: (1) Their macro- and microga-
(e.g., polar ring, conoid, rhoptries, etc.) at one metocytes develop independently (i.e., without

The Biology and Identification of the Coccidia (Apicomplexa) of Marsupials of the World Copyright © 2016 Donald W. Duszynski. Published by Elsevier Inc.
http://dx.doi.org/10.1016/B978-0-12-802709-7.00001-1 1 All rights reserved.
2 1. INTRODUCTION

syzygy); and (2) their microgametocytes usu- on histological changes, and pathology due to
ally produce many microgametes versus the asexual and sexual endogenous development,
small number of microgametes produced by and others, to clarify the complex taxonomy of
microgametocytes of adeleids (Upton, 2000). these parasites. Amplification of DNA, sequenc-
Coccidians from these two groups are com- ing of gene fragments, and phylogenetic analysis
monly found in the marsupials that have been of those sequences are now sometimes needed
examined for them, and are represented by to correctly assign a parasite to a group, genus,
about 86 species that fit taxonomically into or even species (e.g., see Merino et al., 2008,
seven genera in four families. In the Adeleo- 2009, 2010). Thus, there seems a clear need to use
rina: Klossiellidae Smith and Johnson, 1902, 11 molecular tools to ensure accurate species iden-
Klossiella species; and in the Eimeriorina: Cryp- tifications in groups where it is needed most,
tosporidiidae Léger, 1911, 6 Cryptosporidium if we are to truly understand the host–parasite
species; Eimeriidae Minchin, 1903, 56 Eimeria associations of these species and genera.
and 1 Isospora species; Sarcocystidae Poche, It needs to be kept in mind, however, that
1913, 1 Besnoitia, 10 Sarcocystis species, and molecular data alone are insufficient for a spe-
Toxoplasma gondii. cies description and name, although their use
The taxonomy and identification of coccid- as a valuable tool can help sort out many taxo-
ian parasites used to be a relatively simple affair nomic problems. For example, molecular meth-
based on studying the morphology of oocysts ods helped differentiate between the Isospora
found in the feces. Morphology of sporulated species with and without Stieda bodies; those
oocysts is still a useful tool, as demonstrated in with Stieda bodies share a phylogenetic origin
this book by most of the Eimeria and Isospora spe- with the eimeriid coccidia, while those without
cies now known from marsupials. My interest Stieda bodies may best be placed in the Cys-
here is not just in taxonomy per se, but simply to toisospora (Carreno and Barta, 1999). Molecu-
derive as robust and reasonable a list of all api- lar techniques also have helped resurrect some
complexan species that occur naturally in mar- genera (Modrý et al., 2001), and have allowed
supials, and use the gastrointestinal or urinary proper phylogenetic assignment when only
tracts to discharge their resistant propagules. endogenous developmental stages were known
However, morphology alone is no longer suf- (Garner et al., 2006). Tenter et al. (2002) proposed
ficient to identify many coccidian species, espe- that we need an improved classification system
cially those in genera such as Cryptosporidium for parasitic protists, and that to build one we
and Sarcocystis, which have species with oocysts need to include molecular data to supplement
and sporocysts, respectively, that are very small morphological and biological information. Such
in size and have an insignificant suite of struc- combined data sets will enable phylogenetic
tural characters. In addition to morphology, inferences to be made, which in turn will result
identifications now should be supplemented in a more stable taxonomy for the coccidia. We
with as much knowledge as can be gleaned from seem to slowly be moving in the right direction.
multiple data sets including, but not limited to, As a quick overview, Chapter 2 presents some
location of sporulation (endogenous vs exoge- basic information about the physical characteris-
nous), length of time needed for exogenous spor- tics of marsupials, and recent thoughts on how
ulation at a constant temperature, morphology and when they evolved. Chapters 3, 4, and 5
and timing of some or all of the developmental cover the 56 Eimeria and 1 Isospora species in the
stages in their endogenous cycle, length of pre- Eimeriidae (Eimeriorina) that have been reported
patent and patent periods, host-specificity via from the three marsupial orders (Didelphimor-
cross-transmission experiments, observations phia, Diprotodontia, and Peramelemorphia) in
 INTRODUCTION 3
which they were found. In Chapter 6, I outline apicomplexans. The formal chapters are followed,
what we know about the 11 Klossiella species in in order, by three Tables (11.1. parasite–host; 11.2.
the Klossiellidae (Adeleorina) known from mar- host–parasite; 11.3. eimeriid oocyst/sporocyst
supials. Along with the Eimeriidae, the other features), a Glossary and a List of Abbreviations,
important apicomplexan family is the Sarcocysti- a complete list of all references cited, and an
dae; it has two subfamilies, Sarcocystinae Poche, Index.
1913 (Sarcocystis) and Toxoplasmatinae Biocca, Throughout the chapters of this book, I use
1957 (Besnoitia, Toxoplasma, others). These are cov- the standardized abbreviations of Wilber et al.
ered separately in Chapters 7 and 8, respectively. (1998) to describe various oocyst structures:
Chapter 9 documents the six Cryptosporidium length (L), width (W), and their ratio (L/W),
species known to date from marsupials. Chap- micropyle (M), oocyst residuum (OR), polar
ter 10 entitled Species Inquirendae, details all of granule (PG), sporocyst (SP) L and W and their
the apicomplexans that have been mentioned to L/W ratio, Stieda body (SB), substieda body
occur in marsupials, but from which there is not (SSB), parastieda body (PSB), sporocyst residuum
enough clear documentation to label them “spe- (SR), sporozoite (SZ), refractile body (RB), and
cies” that really exist in nature. Chapter 11 offers nucleus (N). Other abbreviations used, as well
a brief summary of the salient data and ideas as definitions of some terms that may be unfa-
presented in the previous chapters, and reiterates miliar, are bolded in the text and are found in
some of those topics/issues discussed in previous the Glossary. All measurements in the chapters
works, including an overview of where we stand are in micrometers (μm) unless indicated other-
now regarding examining vertebrate hosts for wise (usually in mm).
 C H A P T E R

2
Review: Marsupials and Marsupial
Evolution
O U T L I N E

What Are Marsupials? 5 Creating Zoonoses 8

Marsupial Evolution 6

WHAT ARE MARSUPIALS? abdominal pouch; in some it is well developed,

in some it consists only of folds of skin around
Ever since the first Europeans reached the mammae, while in others, the pouch only
Australia, people—especially biologists— develops during the female’s reproductive sea-
became fascinated by the curious animals they son, and a few, small marsupials have no pouch
found there called marsupials. Immediately at all. All marsupials lack a complete placenta,
intriguing to many was the question of the evo- and the female reproductive tract is bifid; that
lutionary relationships between the living Aus- is, both the vagina and the uterus are double.
tralian and South American marsupials. In males, the scrotum is in front of the penis
Before I discuss the apicomplexan parasites (except in one order, the Notoryctemorphia),
of marsupials, I think it is useful to have a basic many have a bifid penis, but they do not pos-
sense of what marsupials are and of how they fit sess a baculum. There also are skull, jaw, and
into the web of living things, particularly other tooth characteristics (∼five upper, four lower
mammals. There are three subclasses of extant incisors, a canine, three premolars, and four
mammals: the most primitive are the mono- molars) to help set marsupials apart from pla-
tremes or egg-laying mammals (e.g., echidnas cental mammals (Nowak, 1991). In Australia,
(spiny anteaters), duck-billed playtpus), the and as a group, marsupials exploit many types
metatheria or marsupials, and the eutherians of habitats; some of them climb (didelphids),
or placental mammals. Marsupials can be dis- hop (kangaroos), dig (bandicoots, wombats),
tinguished from all other mammals by some or even swim (the yapok) (Nowak, 1991). Most
unique anatomical and physiological charac- are herbivores, some are insectivores, but only
ters of reproduction. Most females possess an a few are predators.

The Biology and Identification of the Coccidia (Apicomplexa) of Marsupials of the World Copyright © 2016 Donald W. Duszynski. Published by Elsevier Inc.
http://dx.doi.org/10.1016/B978-0-12-802709-7.00002-3 5 All rights reserved.
6 2. MARSUPIALS AND MARSUPIAL EVOLUTION

In previous classifications of mammals (e.g., genomes. Only by sequencing multiple genomes,

Nowak, 1991), all marsupials were placed in a and then analyzing and comparing them, can
single order, Marsupialia, but molecular and biologists make use of these sequence differ-
genetic research within the last decade or two ences to understand the evolutionary process
has allowed mammalogists to partition them from any hypothesized clades that emerge; this
into seven orders within two superorders: progression is called comparative genomics.
Ameridelphia (Didelphimorphia, Microbiothe- Early in the first decade of this century (2000s),
ria, Paucituberculata), the American marsupials, once molecular analyses of various mamma-
and Australidelphia (Dasyuromorphia, Dipro- lian evolutionary trees began to gain traction,
todontia, Notoryctemorphia, Peramelemor- there were many reconstructions and diverse
phia), the Australian marsupials (Wilson and revisions, the aspects of which were sometimes
Reeder, 2005). However, the key to marsupial hotly debated (Kriegs et al., 2006). One of the
evolutionary history and relationships falls to confounding issues was molecular homopla-
the monotypic South American order Micro- sies; that is, shared similar characteristics due
biotheria. Recent molecular work suggests that to such things as directional mutation pressure,
this primitive “Monito del Monte,” Dromiciops but lacking common ancestry. Then retroposed
gliroides Thomas, 1894, from Chile, is the link elements were discovered to be useful.
to a complex, ancient, biogeographic history of Retroposed elements, or retroposons, are
marsupials (see below). repetitive fragments of DNA that are inserted
The marsupials are not a stagnant lineage, randomly into chromosomes after they have
because we know that their number of spe- been reverse-transcribed from any RNA. This
cies continues to increase; some because newer means there is negligible probability of the same
molecular techniques have allowed more criti- element integrating independently into ortholo-
cal and detailed comparisons of species limits, gous positions in different species (Kriegs et al.,
allowing cryptic species to be delineated, but 2006; Nilsson et al., 2010). Thus, the presence or
most by the discovery of new species, previ- absence of these elements provides a source of
ously undocumented to science. For example, information on rare genomic changes that can be
Walker et al. (1975) said that the order Marsu- an incomparable strategy for molecular system-
pialia contained 9 families, 81 genera, and about atists to use. Kriegs et al. (2006) emphasized that
244 species; Nowak (1991) listed 16 families, retroposons are, “…a virtually ambiguity-free
78 genera, and 280 species; Wilson and Reeder approximation of evolutionary history.”
(1993) recorded 7 orders, 19 families, 83 genera, Mikkelsen et al. (2007) reported on their
and 272 species; and Wilson and Reeder (2005) genome sequences of Monodelphis domestica (Wag-
updated their records in 7 orders to 21 families, ner, 1842), the gray, short-tailed opossum, which
92 genera, and 331 species. was the first marsupial species to be completely
sequenced. This important research milestone
allowed opossum (i.e., marsupial) and eutherian
MARSUPIAL EVOLUTION (placental) genomes to be compared for the first
time. Their comparison of these genomes revealed
In this section, I want to briefly review some a sharp difference in evolutionary innovation
of the most recent and, I believe, pertinent litera- between protein-coding and noncoding elements,
ture on who begat whom—as best I can under- and allowed them to conclude that metatherian
stand it—within the marsupials. Waddell et al. (marsupial) and eutherian lineages diverged from
(2001) pointed out that a major effort is being each other sometime between 130 and 180 million
undertaken to sequence an array of mammalian years ago (MYA), long before the radiation of the
 Marsupial Evolution 7
extant eutherian clades (∼100 MYA) (Mikkelsen with the identification and use of retroposed ele-
et al., 2007). Interestingly, although marsupials ments, allow systematists the unique opportunity
seem to have originated in, and then radiated to help resolve marsupial and eutherian mammal
from, North America, only one extant species, relationships. The presence of one retroposed ele-
Didelphis virginiana Kerr, 1792, the Virginia opos- ment in the orthologous genomic loci of two spe-
sum, is now found in North America. All other cies signals a common ancestry, while its absence
American marsupial species (93 species) are in another species signals a prior divergence
found in Central and South America, while the (Shedlock and Okada, 2004). No other sequenced
majority of marsupials (72%), about 237 spe- mammalian genome has shown as high a per-
cies that include the familiar kangaroos, bandi- centage of discernible retroposed elements as
coots, wallabies, koalas, and others, are found in marsupials (52%) (Mikkelsen et al., 2007). Nilsson
Australia. et al. (2010) screened the genomes of M. domestica
Nilsson et al. (2010) pointed out that the evo- and M. eugenii for retroposons, and from analysis
lutionary/phylogenetic relationship between of ∼217,000 retroposon-containing loci, they
the three Ameridelphia and the four Australi- identified 53 that helped resolve most branches
delphia marsupial orders was unclear and of the marsupial evolutionary tree. They found
debated intensively ever since the small species, that D. gliroides is only distantly related to Austra-
D. gliroides, was taxonomically moved from the lian marsupials, supporting a single Gondwanan
Didelphimorphia into a new order, Microbioth- migration of marsupials from South America to
eria, and into the cohort Australidelphia, which Australia. They also found that 10 of the 53 phy-
was originally based on ankle joint morphol- logenetically informative markers accumulated
ogy (Szalay, 1982). The Australidelphia now in the marsupial genome since they split from
comprises the four Australian marsupial orders the placental mammals ∼130 MYA (Lou et al.,
and the South American order Microbiotheria. 2003; Kullberg et al., 2008), and before the earliest
Nilsson et al. (2010) expanded upon the work of divergence of the modern marsupial mammals,
Mikkelsen et al. (2007) using retroposon inser- 70–80 MYA (Nilsson et al., 2004; Beck, 2008). All 10
tion markers to explore the basal relationships were absent in other mammals, significantly con-
among marsupial orders. Nilsson et al. (2010) firming the monophyly of marsupials (Waddell
found that Australidelphia orders share a single et al., 2001). Using the 43 other retroposon mark-
origin with Microbiotheria, as their closest sister ers, they established the first molecular support
group, supporting a clear divergence between for the earliest branching of Didelphimorphia,
South American and Australian marsupials. confirming it as the sister group to the remaining
Their data place the American opossums (Didel- six marsupial orders; skull and postcranium mor-
phimorphia) as the first branch of the marsu- phological data also support Didelphimorphia as
pial tree, and placed into a paleobiogeographic the sister group to all marsupials (Horovitz and
context, indicated a single marsupial migra- Sánchez-Villagra, 2003). Another of Nilsson et al.
tion from South America to Australia, which is (2010) observations was that 13/53 (25%) of the
remarkable, given that South America, Antarc- original markers were present in the Microbio-
tica, and Australia were connected in the South theria (South America) and in the four Austra-
Gondwanan continent for many millennia (Nils- lian orders, but not in either Didelphimorphia
son et al., 2010). or Paucituberculata from the Americas, signifi-
The two recently sequenced marsupial cantly supporting the monophyly of the Australi-
genomes, the South American opossum (M. domes- delphia (Szalay, 1982). The original 53 markers
tica) (Mikkelsen et al., 2007), and the tammar wal- also significantly supported the monophyly of
laby, Macropus eugenii (Desmarest, 1817), along each of the five multispecies marsupial orders:
8 2. MARSUPIALS AND MARSUPIAL EVOLUTION

Dasyuromorphia, Didelphimorphia, Diprotodon- human settlements, such as opossums in urban

tia, Paucituberculata, and Peramelemorphia. areas throughout the Americas and Australia,
and kangaroos in agricultural areas of Australia.
The dispersal of marsupial wildlife species into
CREATING ZOONOSES areas dominated by human activities increases
the chance for their interactions with humans
Although Australian marsupials have been and introduced placental mammal species such
geographically isolated from their American as cattle, sheep, dogs, and cats. Such interactions
cousins for millennia, Power (2010) correctly at the wildlife, domestic animal, and human
and importantly pointed out that human influ- interface can and do present risks for patho-
ence has seen Australian and American species gen transfer and zoonoses that are conducive
dispersed to different continents for zoological to emerging disease (Daszak et al., 2000). These
displays and for the pet trade, particularly in the interactions also predispose wildlife to parasite
USA. In Australia, marsupials represent normal species that are atypical in their natural habitats.
and abundant wildlife species and, hence, are As we will see in the chapters that follow, this
naturally present in water catchments across the certainly is true of apicomplexan parasites that
country. Many marsupials also have adapted to infect marsupials along with other animals.
 C H A P T E R

3
Order Didelphimorphia—Eimeriidae
O U T L I N E

Order Didelphimorphia Gill, 1872 10 Eimeria cochabambensis Heckscher,

Wickesberg, Duszynski, and Gardner,
Introduction10
199921
Species Descriptions 13
Eimeria marmosopos Heckscher, Wickesberg,
Family Didelphidae Gray, 1821 13 Duszynski, and Gardner, 1999 23
Subfamily Caluromyinae Kirsch, 1977 13 Genus Micoureus Lesson, 1842 26
Genus Caluromys J.A. Allen, 1900 13 Eimeria micouri Heckscher, Wickesberg,
Duszynski, and Gardner, 1999 26
Eimeria caluromydis Lainson
and Shaw, 1989 13 Genus Monodelphis Burnett, 1830 27
Eimeria haberfeldi Carini, 1937 14 Eimeria cochabambensis Heckscher,
Wickesberg, Duszynski, and Gardner,
Genus Didelphis L., 1758  15
199927
Eimeria auritanensis Teixeira, Rauta,
Genus Philander Brisson, 1762 27
Albuquerque, and Lopes, 2007 15
Eimeria philanderi Lainson and Shaw,
Eimeria didelphidis Carini, 1936 emend.
198927
Pellérdy, 1974 16
Genus Thylamys Gray, 1843 28
Eimeria gambai Carini, 1938 17
Eimeria cochabambensis Heckscher,
Eimeria indianensis Joseph, 1974 18
Wickesberg, Duszynski, and Gardner,
Eimeria marmosopos Heckscher, Wickesberg, 199928
Duszynski, and Gardner, 1999 19
Discussion and Summary 29
Isospora arctopitheci (Rodhain, 1933) 19
Genus Marmosops Matschie, 1916 21

The Biology and Identification of the Coccidia (Apicomplexa) of Marsupials of the World Copyright © 2016 Donald W. Duszynski. Published by Elsevier Inc.
http://dx.doi.org/10.1016/B978-0-12-802709-7.00003-5 9 All rights reserved.
10 3. ORDER DIDELPHIMORPHIA—EIMERIIDAE

ORDER DIDELPHIMORPHIA 500 mm at the other, and in weight from about

GILL, 1872 10 g to more than 3000 g. Most didelphids,
however, range in head-and-body length from
INTRODUCTION about 100 to 300 mm and weigh between 20 and
500 g (Voss and Jansa, 2009).
The Didelphimorphia is the only substan- All didelphids have nonspinous fur, which
tially intact radiation of New World mar- is soft to the touch. A few taxa (e.g., Caluromys)
supials; it is represented by a single family, have somewhat woolly fur that does not lie flat
Didelphidae, commonly known as opossums. or exhibit the glossy highlights typically seen
According to Voss and Jansa (2009), didelphids in the pelts of many other taxa, but textural dif-
were the first metatherians to be encountered ferences are hard to define by objective criteria.
by European explorers (Eden, 1555), the first The only superficial feature of didelphid body
to be described scientifically (Tyson, 1698), and pelage that is taxonomically useful is the pres-
the first to be classified by taxonomists (Lin- ence of long, coarse, nonpigmented guard hairs
naeus, 1758). In this chapter, and throughout that project conspicuously from under the fur
this book, I use the taxonomic presentation and (e.g., in Didelphis spp.). Dorsal body pelage of
arrangement provided by Wilson and Reeder most didelphids is uniformly colored in some
(2005) for each of the seven marsupial orders. shade of brown or gray, but other taxa can be
I have chosen to use their organizational scheme distinctively marked (e.g., Chironectes, black
so I can be internally consistent in presenting transverse scapular stripes/bars on a gray
the apicomplexan parasites known from each background; Monodelphis, with three longitudi-
marsupial taxon. Wilson and Reeder (2005) rec- nal stripes).
ognize 87 extant species in 17 genera within Many females that are in the process of,
the Didelphidae. Although steady advances in or have produced offspring (parous adults),
didelphid taxonomy were made from the sev- have pouchlike enclosures (marsupium, sin-
enteenth through the twentieth centuries, most gular; marsupia, plural) for nursing young,
involved the description of new species. Thus, but these are absent in some didelphids.
the arrangement I use for marsupial taxa in this When present, there seems to be no intra-
book does not necessarily reflect the evolution- specific variation in this female reproductive
ary or phylogenetic relationship of, or within, structure, although distinctly different pouch
any marsupial order. configurations can be recognized among
Most didelphids (opossums) have pointed different opossum species. Genera of par-
muzzles, well-developed vibrissae, prominent ous adult females that, apparently, do not
eyes, membranous ears, nonspinous pelage, have marsupia include Glironia, Gracilinanus,
and other morphological, cranial, and dental Hyladelphys, Lestodelphys, Marmosa, Marmos-
features that unite them. In many respects, ops, Metachirus, Monodelphis, Thylamys, and
they resemble some ancestral marsupials (e.g., Tlacuatzin, while well-developed pouches
Dromiciops), as well as certain unspecialized are found in Caluromys, Chironectes, Didel-
placental mammals (e.g., tree shrews). Closer phis, Lutreolina, and Philander. The presence or
inspection, however, reveals numerous distinc- absence of a pouch remains undocumented for
tive and some phylogenetically informative many opossums (e.g., Caluromysiops). While
details. These are small- to medium-sized mam- intraspecifically consistent, the marsupium of
mals. They can vary in head-and-body length some species may consist of deep lateral skin
from as small as 68 mm at one extreme to about folds that enclose the nursing young and open
 Introduction 11
in the midline; in others, the lateral pockets length. This does not, however, imply that
are joined posteriorly, forming a more exten- arboreal taxa are always longer-tailed than
sive enclosure that opens anteriorly (Enders, terrestrial forms.
1937; Voss and Jansa, 2009), yet in others, Linnaeus (1758) described five species of
the lateral pockets are connected anteriorly, didelphid marsupials, all of which he placed
forming a marsupium that opens posteriorly in the genus Didelphis (Voss and Jansa, 2009);
(Krieg, 1924; Oliver, 1976). In all marsupials four of those species are still recognized as
that possess marsupia, the mammae are con- valid, but three now reside in different genera
tained within it, but the mammae of pouch- (Philander, Opossum, Murina). As time advanced
less taxa are variously distributed (Voss and and knowledge of new forms increased, new
Jansa, 2009). In most pouchless didelphids, generic names for opossums proliferated, espe-
the mammae are confined to a somewhat cir- cially during the eighteenth and nineteenth
cular inguinal/abdominal array that occupies centuries, but without a consistent binomial
the same anatomical position as the pouch in usage. It was not until Thomas’s (1888) cata-
taxa that possess a marsupium. However, a log of the marsupials in the British Museum
few other pouchless opossums have bilater- of Natural History (Voss and Jansa, 2009) that
ally paired mammae that extend anteriorly, some context began to take place. He recog-
well beyond the pouch region. Although most nized only Didelphis and Chironectes as genera,
of these anterior teats are not actually located while including other taxa as subgenera of
on the upper chest, many mammalogists still Didelphis, including Metachirus, Micoureus, and
refer to them as pectoral or thoracic mammae Philander. As knowledge of didelphid diversity
(e.g., Reig et al., 1987). In addition to bilater- increased in the years following Thomas’s clas-
ally paired mammae, most didelphids have an sification, Matschie (1916) persisted in refer-
unpaired median teat that occupies the ven- ring all nonaquatic opossums to the genus
tral midline, approximately in the center of Didelphis; he also recognized more subgenera
the abdominal-inguinal array (Voss and Jansa, of Didelphis than Thomas did, resurrecting old
2009). Mammary counts for didelphids are, names or describing new ones to suit his needs
therefore, usually odd-numbered, but there (according to Voss and Jansa, 2009). Although
are exceptions. Cabrera’s (1919) classification, among others,
All male opossum species examined to date rejected Linnaeus’s inclusive concept of Didel-
have a bifid penis, although the male genita- phis, it was influential in establishing modern
lia exhibit conspicuous variations in length, binomial usage, but he made no use of subfam-
shape, urethral grooves, and other details. ilies, tribes, or other suprageneric categories to
Unfortunately, these characters of male geni- indicate relationships among living opossums.
talia have been unstudied in many opossum Cabrera’s (1958) checklist of South American
species. mammals was one of the last attempts to clas-
Although most didelphids have a tail sify extant opossum diversity by traditional
substantially longer than their combined (prephylogenetic) criteria, and it remained
head-and-body length, some taxa are much more-or-less unchallenged until the advent of
shorter-tailed. For example, some arboreal molecular systematics in the mid-1970s (Voss
species have a tail that may be almost twice and Jansa, 2009).
as long as their head-and-body length, while The first classifications of opossum-like
some terrestrial forms have a tail that, gener- marsupials based on an explicitly phyloge-
ally, is less than half of their head-and-body netic analysis were by Reig et al. (1985, 1987),
12 3. ORDER DIDELPHIMORPHIA—EIMERIIDAE

and their classification also was the first to subfamilies (-inae), 4 tribes (-ini), 18 genera,
incorporate results from molecular and cyto- and 97 species:
  
genetic research. Kirsch and Palma (1995)
Didelphidae:
were among the first to incorporate the results
Glironiinae: Glironia (1)
of DNA–DNA hybridization experiments
Caluromyinae: Caluromys (3),
into a classification, and McKenna and Bell’s
Caluromysiops (1)
(1997) classification followed that of Reig et al.
Hyladelphinae: Hyladelphys (1)
(1985) to some extent. However, no compre-
Didelphinae:
hensive phylogenetic synthesis was attempted
Marmosini: Marmosa (15), Monodelphis
until Voss and Jansa (2009) summarized more
(22), Tlacuatzin (1)
than a decade of morphological and molecu-
Metachirini: Metachirus (1)
lar research on the phylogenetic relationships
Didelphini: Chironectes (1), Didelphis (6),
of didelphid marsupials. Their observations,
Lutreolina (1), Philander (7)
representing diverse functional, morphologi-
Thylamyini: Chacodelphys (1), Cryptonanus
cal, karyotypic, and molecular data (some
(5), Gracilinanus (6), Lestodelphys (1),
gleaned from the literature, some original
Marmosops (15), Thylamys (9)
sequencing data), provided the basis for a   

new phylogenetic inference on the didelphids. Gardner (2005, in Wilson and Reeder, 2005)
Using separate parsimony, likelihood, and lists the Didelphidae with only 2 subfamilies, 17
Bayesian analyses of six data partitions (mor- genera, and 87 species; this is the order in which
phology + karyotypes, five genes), they found their apicomplexan parasites will be presented
highly congruent estimates of didelphid phy- below, in those genera from which one or more
logeny, with few examples of conflict among have been described:
  
strongly supported nodes.
Didelphidae:
Of the many genes that have been sequenced
Caluromyinae: Caluromys (3),
to date from one or more didelphid marsupials—
Caluromysiops (1), Glironia (1)
including the entire genome of Monodelphis
Didelphinae: Chironectes (1), Didelphis
domestica (Mikkelsen et al., 2007)—only a few
(6), Gracilinanus (9), Hyladelphys (1),
had been sequenced from enough taxa to be
Lestodelphys (1), Lutreolina (1), Marmosa (9),
useful to Voss and Jansa (2009) for phylogenetic
Marmosops (14), Metachirus (1), Micoureus
inference; these included: Breast Cancer Activat-
(6), Monodelphis (18), Philander (4),
ing 1 Gene; Dentin Matrix Protein 1 Gene; Inter-
Thylamys (10), Tlacuatzin (1).
photoreceptor Retinoid Binding Protein Gene;   

Recombination Activating 1 Gene; and the von Reiterating what was stated in Chapter 1,
Willebrand Factor. These five protein-coding in the descriptions of coccidian exogenous
nuclear loci were obtained from many species stages given below, and throughout the other
representing almost all the currently recognized chapters, I use the standardized abbreviations of
genera. Wilber et al. (1998): oocyst length (L), width (W),
The classification scheme resulting from the and their ratio (L/W), micropyle (M), oocyst
analysis of Voss and Jansa (2009) differs some- residuum (OR), polar granule (PG), sporocyst
what from the one I use in this chapter (Gard- (SP) L and W and their L/W ratio, Stieda body
ner, 2005, in Wilson and Reeder, 2005), but (SB), substieda body (SSB), parastieda body.
theirs is more phylogenetically accurate. Voss (PSB), sporocyst residuum (SR), sporozoite
and Jansa (2009) list the Didelphidae with 4 (SZ), refractile body (RB), and nucleus (N). All
 EIMERIA CALUROMYDIS LAINSON AND SHAW, 1989 13
measurements are in micrometers (μm) unless that appears striated in optical section, brown-
otherwise stated. ish-yellow, ∼3.2 (2.5–4) thick; L × W (n = 50):
31.8 × 31.2 (26–36 × 25–35); L/W ratio: 1.0; M,
OR, PG: all absent. Distinctive features of oocyst:
SPECIES DESCRIPTIONS rough, thick, yellow-brown outer wall surface
that appears striated and lack of M, OR, and PG.
FAMILY DIDELPHIDAE GRAY, Description of sporocyst and sporozoites: Spo-
1821 (17 GENERA, 87 SPECIES) rocyst shape: ovoidal; L × W (n = 20): 14.8 × 9.7
(12.5–16 × 9–10); L/W ratio: 1.5; SB: inconspicu-
SUBFAMILY CALUROMYINAE ous at pointed end of sporocyst; SSB: prominent
KIRSCH, 1977 and large; PSB: absent; SR: present; SR charac-
teristics: “bulky,” composed of granules and
GENUS CALUROMYS J.A. ALLEN, spherules; SZ: sausage-shaped, longer than, and
1900 (3 SPECIES) lying lengthwise in, the sporocysts so they are
recurved back on themselves (line drawing);
EIMERIA CALUROMYDIS LAINSON RB: not visible. Distinctive features of sporocyst:
AND SHAW, 1989 long SZ with SR that almost completely fills the
SP and obscures the SZs.
Type host: Caluromys philander philander (L., Prevalence: Found in 2/13 (15%) of the type host.
1758), Bare-tailed Woolly Opossum. Sporulation: “Not determined, but within
Type locality: SOUTH AMERICA: Brazil: Pará 14 days” (Lainson and Shaw, 1989).
State, Island of Tocantins. Prepatent and patent periods: Unknown, oocysts
Other hosts: None to date. were collected from the feces.
Geographic distribution: SOUTH AMERICA: Site of infection: Unknown.
Brazil. Endogenous stages: Unknown.
Description of sporulated oocyst: Oocyst shape: Cross-transmission: None to date.
spheroidal to subspheroidal; number of walls: Pathology: Unknown.
seemingly of a single layer (?); wall character- Materials deposited: A specimen of the “woolly
istics: prominently mammillated outer surface opossum is lodged with the Smithsonian

FIGURES 3.1–3.3 3.1. Line drawing of the sporulated oocyst of Eimeria caluromydis. 3.2. Photomicrograph of a sporulated
oocyst of E. caluromydis. 3.3. Photomicrograph of sporocysts of E. caluromydis. All figures slightly modified from Lainson and
Shaw, 1989, the Bulletin du Museum National d’Histoire Naturalle (Paris), and with permission from the senior author.
14 3. ORDER DIDELPHIMORPHIA—EIMERIIDAE

Institution, Washington, D.C., USA.” Photo- OR, PG: all absent. Distinctive features of oocyst:
types are deposited with the Department of Par- scabrous brown outer wall that appears radially
asitology, the Instituto Evandro Chagas, Belém, striated in optical section and lack of M, OR,
Pará, Brazil, and with the Muséum National and PG.
d’Histoire Naturelle (Laboratoire des Vers), Description of sporocyst and sporozoites: Sporo-
Paris, P-6555. cyst shape: ovoidal; L × W: 13 × 8; L/W ratio: 1.6;
Remarks: Lainson and Shaw (1989) felt that SB: prominent, at pointed end of sporocyst; SSB,
the remarkably thick, dense, and mammillated PSB: both absent; SR: present; SR characteristics:
wall of this species “effectively distinguished “copious” mass of granules and spherules that
the parasite from the four other Eimeria species fill the space between the SZ and sometimes
described from American marsupials, and in almost fill the SP (line drawing); SZ: sausage- or
addition, the oocysts of E. gambai and E. haber- banana-shaped (line drawing) lying lengthwise
feldi are ovoid.” in the sporocysts, usually without RB. Distinc-
tive features of sporocyst: massive SR filling
much of the space in the SP.
EIMERIA HABERFELDI CARINI, Prevalence: Found in 1/1 of the type host.
1937 Sporulation: In about 6 days (according to
Pellérdy, 1974).
Prepatent and patent periods: Unknown, oocysts
were collected from the feces.
Site of infection: Carini (1937) said that propa-
gating forms of this eimerian were found “in the
first part of the intestine,” but Pellérdy (1974)
mistranslated that to say the site of infection was
the posterior third of the small intestine.
Endogenous stages: Meronts were extremely
rare, but Carini (1937) found a few that were
spheroidal, 12–15 wide, beneath the host cell
nucleus (HCN) in the epithelial cells of the villi
of the anterior small intestine; each meront con-
tained 9–13 fusiform, slightly curved merozo-
FIGURE 3.4 Line drawing of the sporulated oocyst of ites. Carini (1937) said that the sexual forms in
Eimeria haberfeldi modified from Carini, 1937.
the tissue sections he examined were numerous.
Type host: Caluromys philander (L., 1758), Bare- Microgamonts were spheroidal, 20–22 wide,
tailed Woolly Opossum. beneath the HCN, each with about 100 micro-
Type locality: SOUTH AMERICA: Brazil: near gametes that resemble slightly curved small
São Paulo. rods. Macrogametes were found apparently
Other hosts: None to date. above or below the HCN and were spheroidal
Geographic distribution: SOUTH AMERICA: with alveolar protoplasm. Carini (1937) said that
Brazil. after fertilization, numerous granules appeared
Description of sporulated oocyst: Oocyst shape: (wall-forming bodies) “which later take part in
ovoidal or ellipsoidal; number of walls: 1 (line the formation of the capsule.”
drawing); wall characteristics: rough scabrous Cross-transmission: Carini (1937) was unable
outer surface, with radial striations, brownish- to infect two opossums, Didelphis aurita, with
yellow, ∼2.0 thick; L × W: 30 × 20; L/W ratio: 1.5; M, this species by feeding them drops of slurry
 EIMERIA AURITANENSIS TEIXEIRA, RAUTA, ALBUQUERQUE, AND LOPES, 2007 15
containing oocysts. He examined the feces daily Description of sporulated oocyst: Oocyst shape:
for 20 days postinoculation (PI) and never saw spheroidal to subspheroidal; number of walls:
oocysts. 2; wall characteristics: ∼2.1 thick; outer mem-
Pathology: Unknown. brane yellow and strongly ornamented with a
Materials deposited: None. prominently mammillated surface; inner layer is
Etymology: This species was named as a trib- brown and smooth; L × W: 31.6 × 29.6 (ranges not
ute to Professor Walter Haberfeld. given); L/W ratio: 1.1; M, OR: both absent, PG:
Remarks: This was the first eimerian ever present (?), as one or two granules according
found in a Caluromys species (at that time) so to Teixeira et al. (2007), but not visible in either
Carini (1937) did not see the need to compare it their line drawing or in their photomicrograph.
to other forms. Distinctive features of oocyst: thick, mammil-
lated oocyst wall.
Description of sporocyst and sporozoites: Spo-
GENUS DIDELPHIS L., 1758 rocyst shape: ovoidal; L × W: 13.2 × 10.4 (ranges
(6 SPECIES) not given); L/W ratio: 1.7; SB: present, small and
faint; SSB, PSB: both absent; SR: present; SR char-
EIMERIA AURITANENSIS acteristics: composed of granules and spherules
TEIXEIRA, RAUTA, that fill the majority of the sporocyst obscuring
ALBUQUERQUE, AND LOPES, 2007 the SZs; SZ, RB, and N not visible. Distinctive
features of sporocyst: small, almost indistinct
SB, and the SP has an SR that obscures the SZs.
Prevalence: Unknown.
Sporulation: Oocysts sporulated in 8–9 days in
2.5% potassium dichromate solution (K2Cr2O7)
(Teixeira et al., 2007).
Prepatent and patent periods: Unknown.
Site of infection: Unknown, oocysts were
recovered from the feces.
Endogenous stages: Unknown.
Cross-transmission: None to date.
Pathology: Unknown.
Materials deposited: Oocysts in 10% formal-
FIGURES 3.5, 3.6 3.5. Line drawing of the sporulated dehyde–saline solution, phototypes, and line
oocyst of Eimeria auritanensis. 3.6. Photomicrograph of a
drawing are deposited in the Parasitology Col-
sporulated oocyst of E. auritanensis. Both figures from Teix-
eira et al., 2007, with permission from the Editor-in-chief, lection, Department of Animal Parasitology,
Revista Brasileira de Parasitologia Veterinária. UFRRJ, Seropédica, Rio de Janeiro, Brazil, repos-
itory number P-012/2006.
Etymology: The specific epithet is derived
Type host: Didelphis aurita (Wied-Neuwied, from the specific epithet of the host.
1826), Big-eared Opossum. Remarks: The oocysts described by Teixeira
Type locality: SOUTH AMERICA: Brazil: Man- et al. (2007) were said to be different from all
garatiba, Rio de Janeiro and Sereopedica. other eimerians previously described from the
Other hosts: None to date. Didelphidae when they published their paper
Geographic distribution: SOUTH AMERICA: (see their Table 1). However, there are several dis-
Brazil. crepancies in their paper that make me question
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