Professional Documents
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ADVANCES IN
PARASITOLOGY
Fossil Parasites
SERIES EDITOR
D. ROLLINSON J. R. STOTHARD
Life Sciences Department Department of Parasitology
The Natural History Museum, Liverpool School of Tropical
London, UK Medicine Liverpool, UK
d.rollinson@nhm.ac.uk russell.stothard@lstmed.ac.uk
EDITORIAL BOARD
T. J. C. ANDERSON R. C. OLIVEIRA
Department of Genetics, Texas Centro de Pesquisas Rene Rachou/
Biomedical Research Institute, CPqRR - A FIOCRUZ em Minas
San Antonio, TX, USA Gerais, Rene Rachou Research
Center/CPqRR - The Oswaldo Cruz
M. G. BASÁÑEZ Foundation in the State of Minas
Professor of Neglected Tropical Gerais-Brazil, Brazil
Diseases, Department of Infectious
Disease Epidemiology, Faculty of R. E. SINDEN
Medicine (St Mary’s Campus), Immunology and Infection
Imperial College London, Section, Department of Biological
London, UK Sciences, Sir Alexander Fleming
Building, Imperial College of
Science, Technology and
S. BROOKER Medicine, London, UK
Wellcome Trust Research Fellow
and Professor, London School of D. L. SMITH
Hygiene and Tropical Medicine, Johns Hopkins Malaria Research
Faculty of Infectious and Tropical, Institute & Department of
Diseases, London, UK Epidemiology, Johns Hopkins
Bloomberg School of Public Health,
R. B. GASSER Baltimore, MD, USA
Department of Veterinary Science,
The University of Melbourne, R. C. A. THOMPSON
Parkville, Victoria, Australia Head, WHO Collaborating Centre
for the Molecular Epidemiology
of Parasitic Infections, Principal
N. HALL Investigator, Environmental
School of Biological Sciences, Biotechnology CRC (EBCRC), School
Biosciences Building, University of of Veterinary and Biomedical
Liverpool, Liverpool, UK Sciences, Murdoch University,
Murdoch, WA, Australia
J. KEISER
Head, Helminth Drug X.-N. ZHOU
Development Unit, Department Professor, Director, National
of Medical Parasitology and Institute of Parasitic Diseases,
Infection Biology, Swiss Tropical Chinese Center for Disease Control
and Public Health Institute, Basel, and Prevention, Shanghai, People’s
Switzerland Republic of China
VOLUME NINETY
ADVANCES IN
PARASITOLOGY
Fossil Parasites
Edited by
KENNETH DE BAETS
GeoZentrum Nordbayern,
Friedrich-Alexander-Universit€
at
Erlangen-N€ urnberg, Erlangen, Germany
D. TIMOTHY J. LITTLEWOOD
Department of Life Sciences, Natural History Museum,
London, UK
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Notices
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ISBN: 978-0-12-804001-0
ISSN: 0065-308X
ix j
x Contributors
Paul D. Taylor
Department of Earth Sciences, Natural History Museum, London, UK
Ieva Upeniece
Department of Geology, University of Latvia, Riga, Latvia
Olivier Verneau
CNRS, Centre de Formation et de Recherche sur les Environnements Méditerranéens,
University of Perpignan Via Domitia, Perpignan, France; Unit for Environmental Sciences
and Management, North-West University, Potchefstroom, South Africa
PREFACE
xi j
xii Preface
lifetime of experience Adauto Ara ujo and co-workers illustrate the impor-
tance of ancient parasitic remains and review the methods to study human
parasites. Considering the links between human health, medical practice and
parasites, Piers Mitchell provides the final chapter with a focus specifically on
Medieval European parasite remains. Fascinating personal natural histories of
the rich, famous and simple peasantry provide insights into archaeology as
well as anthropology. The constraints of parasitic infections on lifestyle,
sanitation and medical treatment of humans in early Europe resonates with
much of modern parasitology today and brings into focus our own ongoing
struggles with infection and parasite-mediated disease worldwide.
We take this opportunity to thank all of the authors for their con-
tributions and to the editorial team for their support in making this volume
possible.
Contents
1. Introduction 2
2. Techniques for Ancient Parasite Discovery 4
2.1 Thin sections and computed tomography 5
2.2 Ancient biomolecules 6
2.2.1 Ancient DNA 6
2.2.2 Palaeoproteomics 7
3. The Parasite Fossil Record 8
3.1 Body fossils 14
3.2 Trace fossils and pathologies 18
3.3 Coprolites 22
4. Molecular Perspectives on Parasite Phylogeny and Evolution 26
4.1 Molecular clocks 29
4.2 HGT and ‘parasitic DNA’ 34
5. Future Perspectives 35
Acknowledgements 36
References 36
Abstract
Knowledge concerning the diversity of parasitism and its reach across our current
understanding of the tree of life has benefitted considerably from novel molecular
phylogenetic methods. However, the timing of events and the resolution of the nature
of the intimate relationships between parasites and their hosts in deep time remain
problematic. Despite its vagaries, the fossil record provides the only direct evidence
of parasites and parasitism in the fossil record of extant and extinct lineages. Here,
we demonstrate the potential of the fossil record and other lines of geological evi-
dence to calibrate the origin and evolution of parasitism by combining different kinds
of dating evidence with novel molecular clock methodologies. Other novel methods
promise to provide additional evidence for the presence or the life habit of pathogens
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.07.001 All rights reserved. 1
2 Kenneth De Baets and D. Timothy J. Littlewood
and their vectors, including the discovery and analysis of ancient DNA and other bio-
molecules, as well as computed tomographic methods.
1. INTRODUCTION
Parasitism is one of the most successful modes of life, as evidenced by
its convergent appearance in numerous lineages and its sheer absolute and
relative abundance among extant biodiversity (Poulin and Morand, 2000).
Antagonistic interactions, in the form of arms races between parasites and
their hosts, have been considered important drivers of evolution (Zaman
et al., 2014) and might also have contributed to the origin of sexual repro-
duction (Mostowy and Engelst€adter, 2012). Because parasitism also has an
obvious societal importance with many parasitic taxa being of significant
biomedical, veterinary or economic importance (Bush et al., 2001), it is
here that most of the research effort is focused. This focus is narrow and fails
to provide the wider evolutionary picture or an appreciation of the influence
of parasitism on, and as part of, biodiversity. Indeed, despite their importance
and ubiquity, the evolutionary history of parasites is still poorly known, a
phenomenon not helped by their inadequate, or rather inadequately
explored, fossil record (Littlewood and Donovan, 2003).
Establishing time-calibrated evolutionary frameworks to test the origins
and radiations of parasites in parallel with studies on environmental param-
eters, or the degree of coevolution between parasites and hosts, is a difficult
but as yet a largely unexplored means by which ancient associations may be
revealed. Parasitologists have often resorted to more circular lines of evi-
dence, such as extrapolating from current host associations or distributions
to put time constraints on the origins and evolution of parasites. For instance,
where extant hosteparasite associations appear to be combinations of early
divergent hosts and early divergent parasites, it is tempting and compelling to
assume a long and ancient association; for example, early divergent gyroco-
tylidean cestodes found only parasitizing early divergent ‘primitive’ holoce-
phalan fishes (Xylander, 2001). In these cases, when the timing of a host’s
divergence can be estimated from molecular or preferably fossil evidence,
a calibration point for the parasite’s association also appears tractable, at least
as a working hypothesis. Assumptions of cophylogeny are common but
bring their own suites of problems, not in the least because of the traps set
by multiple assumptions (Page, 2003). To reveal coevolutionary patterns,
phylogenies of hosts and parasites need to be untangled to better understand
The Importance of Fossils in the Evolution of Parasites 3
(e.g. see Scholl et al., 2003), although such events detected among Metazoa
appear to be more common in some groups (e.g. bdelloid rotifers:
Gladyshev et al., 2008) than in others. Whereas palaeontology looks
towards the earth’s fossil and subfossil record for ancient biotic interactions,
it is clear that genomes may also be gleaned for evidence of relictual genetic
elements of nonhost (“parasitic”) origin.
Regardless of approach, time points gathered directly from fossils or
inferred from calibrated phylogenies remain critical in understanding
when, where and to some extent how hosteparasite interactions took place
and how they might respond in the future; for example, the exchange of
genes from parasitic to host plants of the genus Plantago has been shown
to be a result of their direct physical contact with one another (Mower
et al., 2004). Parasitic plants offer a particularly rich resource for understand-
ing HGT (Davis and Xi, 2015).
Morphologically based classifications of parasites have proved chal-
lenging due to frequent apparent simplifications, convergence or specializa-
tions in their morphology that make homology assessment difficult.
However, novel molecular methods, used with caution, may form the basis
for more robust phylogenetic assignments of extant and subfossil parasitic
remains, and thus more comprehensive understanding of the origin and
evolution of parasitism within single lineages (Near, 2002; Lockyer et al.,
2003; Littlewood, 2011; Wood et al., 2013b; Hartikainen et al., 2014; Sum-
mers and Rouse, 2014; Blaxter and Koutsovoulos, 2015; Littlewood and
Waeschenbach, 2015; Okamura and Gruhl, 2015). Here we provide an
updated perspective on the merits, further possibilities and frustrations
associated with using the fossil record in constraining the origins and evolu-
tion of parasitism. We highlight novel methods, which make it possible to
more fully exploit information buried in fossil or genomic sequences of their
hosts.
2.2.2 Palaeoproteomics
DNA is not believed to survive in sufficiently long lengths for sequencing
over longer geological timescales (>1 Ma) (Hebsgaard et al., 2005; Briggs
and Summons, 2014) and is rarely found well preserved. However, the
study of fossilized bone, which has been crudely defined as a composite
of collagen (protein) and hydroxyapatite (mineral) (see Hill et al., 2015),
has shown that, for vertebrates at least, palaeoproteomics can be a
rewarding insight into ancient proteins, providing evidence for phyloge-
netics and an understanding of bone biochemistry (Wadsworth and
Buckley, 2014). Collagen, in particular, has been isolated from vertebrate
fossils of considerable age, including an 80 million year (my)-old Campa-
nian hadrosaur, Brachylophosaurus canadensis (Schweitzer et al., 2009) and a
68-my-old Tyrannosaurus rex (Asara et al., 2007); some of these studies have
attracted some criticism (Pevzner et al., 2008). The characterization of the
constituent peptides of fossil bone proteins, requiring mass spectrometry,
suggests that collagen (the most abundant protein) can survive up to
340 ky at 20 C, and the second most abundant protein, osteocalcin, can
persist for w45 ky; see Ostrom et al. (2000), Hofreiter et al. (2012) and
Collins et al. (2000). There are many other bone proteins that can be iso-
lated and identified depending on the nature of preservation and the age of
the fossil (Cappellini et al., 2012), but recent studies focusing on collagen
have provided opportunities to push timescales back further in the charac-
terization of ancient biomolecules useful for phylogenetics (Welker et al.,
2015). Recently, even putative erythrocyte remains were reported in dino-
saur bones (Bertazzo et al., 2015).
The application of palaeoproteomics more broadly to parasites or to
other fossil remains, in the hope of finding evidence for parasitism, is in its
infancy, but analysis of more resistant biomolecules than DNA might
make it possible to test other hypotheses associated with parasites or host-
related biomolecules. Certainly, the prospect of verifying the presence of
porphyrins in fossilized haematophagous insects (Greenwalt et al., 2013;
Yao et al., 2014) seems a tractable goal.
8 Kenneth De Baets and D. Timothy J. Littlewood
Eukaryota
Metamonada Parabasalia: Indirect: lesions Cretaceous Skeletal Tyrannosaurus rex Wolff et al. (2009) T
Trichomonadida deformation
Amoebozoa? Entamoebites antiquus Direct: cyst Cretaceous Coprolite Archosaur Poinar and Boucot T
(?dinosaur) (2006)
Phylum Apicomplexa
Gregarinasina Primigregarina Direct: in amber CretaceouseMiocene Amber Cockroaches Poinar (2012) T
burmanica
Coccidia Cryptosporidium, Direct: aDNA in Holocene Coprolite Moas Wood et al. (2013b) T
Eimeriorina coprolite
Eimeria lobatoi Indirect: oocysts Holocene Coprolite Deer Ferreira et al. (1992)
Archeococcidia antiquus; Indirect: oocysts Pleistocene Coprolite Ground sloth Schmidt et al. (1992)
A. nothrotheriopsae
Haemospororida Plasmodium dominicana Direct: erythocytes Miocene Amber Culex malariager Poinar (2005b) T
Vetufebrus ovatus Direct: erythocytes Miocene Amber Enischnomyia stegosoma Poinar (2011b) T
Paleohaemoproteus Direct: erythocytes Early Cretaceous Amber Proticulicoides sp. Poinar and Telford T
burmacis (2005)
Phylum Euglenozoa
Trypanosomatida Palaeotrypanosoma Direct: erythocytes Early Cretaceous Amber Leptoconops nosopheris Poinar (2008a) T
burmanicus
Trypanosoma Direct: erythocytes Miocene Amber Triatoma dominicana Poinar (2005b) T
antiquus
(Continued)
Table 1 Ancient history of hosteparasite associationsdcont'd
Higher taxon Taxon Fossil evidence Age Source Host References Environment
Palaeoleishmania Direct: erythocytes Early Cretaceous Amber Palaeomyia burmitis Poinar and Poinar T
proterus (2004a,b)
Paleoleishmania Direct: erythocytes Miocene Amber Lutzomyia adiketis Poinar (2008b) T
neotropicum
Phylum Arthropoda
Copepoda ? Indirect: exocysts Jurassic Skeletal Crinoids, echinoids Mercier (1936),
deformation Radwa nska and
Radwa nska (2005),
Radwanska and
Poirot (2010)
Kabatarina pattersoni Direct: Early Cretaceous Calcareous Fish Cressey and Patterson M
nodules (1973), Cressey and
Boxshall (1989)
Isopoda ?Bopyridae Indirect: swellings ?Early Jurassic; Middle Skeletal Crustacea Klompmaker et al. M
JurassiceRecent deformation (2014),
Klompmaker and
Boxshall (2015)
Pentastomida 5 genera; 10 species Direct: phosphatized Cambrian Calcareous ? early chordates; Waloszek and M€ uller M
remains isolated eOrdovician; nodules ostracod (1994), Waloszek
from host Silurian? et al. (1994),
Waloszek et al.
(2005a,b),
Castellani et al.
(2011), Siveter et al.
(2015)
Acari Cornupalpatum Direct: larva stage Early Cretaceous Amber ? Poinar and Brown T
burmanicum (2003)
(Ixodidae)
Compluriscutula Direct: larva stage Early Cretaceous Amber ? Poinar and Buckley T
vetulum (Ixodidae) (2008)
Thecostraca ?Ascothoracida Indirect: borings Cretaceous Skeletal Echinoidea Madsen and Wolff M
deformation (1965)
?Ascothoracida Indirect: borings Cretaceous Skeletal Octocorallia Voigt (1959), (1967) M
deformation
Insecta
Siphonaptera s.l. Pseudoculidae Direct: isolated from JurassiceCretaceous Lacustrine ?pterosaurs, dinosaurs Gao et al. (2012), T
host deposits and/or small Huang et al. (2012),
mammals Gao et al. (2013),
Huang et al. (2013),
Gao et al. (2014),
Huang (2014)
Siphonaptera s.s. Paleopsylla: 4 species Direct: isolated from Eocene Amber ?mammals Dampf (1911), T
host Beaucournu and
Wunderlich
(2001),
Beaucournu (2003)
Phthiraptera Megamenopon rasnitsyni Direct: isolated from Eocene Lacustrine ?water birds Wappler et al. (2004) F
host deposits
? Indirect: nits Eocene Baltic amber Mammals Voigt (1952) T
Diptera Qiya jurassica Direct: parasitic larvae Jurassic Lacustrine ?salamanders Chen et al. (2014) F
(Athericidae) deposits
Phylum Nematoda
Ascaridida Ascarites rufferi Indirect: eggs Upper Triassic Coprolite Cynodont Da Silva et al. (2014) T
(Ascarididae)
Ascarites gerus Direct: egg with Early Cretaceous Coprolite Archosaur Poinar and Boucot T
(Ascarididae) developing juvenile (2006)
Toxocara canis Direct: eggs Pleistocene Cave deposits Canid Bouchet et al. (2003)
(Ascarididae) (?Crocuta spelaea)
Oxyurida Paleoxyuris cockburni Indirect: eggs Upper Triassic Coprolite Cynodont Hugot et al. (2014) T
(Heteroxyne-
matidae)
(Continued)
Table 1 Ancient history of hosteparasite associationsdcont'd
Higher taxon Taxon Fossil evidence Age Source Host References Environment
Mermithida Cretacimermis libani Direct Early Cretaceous Amber Midge Poinar et al. (1994) T
(Mermithidae) (Chironomidae:
Diptera)
?Enoplida Palaeonema phyticum Direct Early Devonian Silicified plant Early land plant Poinar et al. (2008) T
(Palaeonematidae) material
Phylum Nematomorpha
Chordodidae Cretachordodes burmitis Direct Early Cretaceous Amber Poinar and Buckley T
(2006)
Phylum Platyhelminthes
Cestoda Permian Direct: eggs with Coprolite Sharks Dentzien-Dias et al. M
developing embryo (2013), De Baets
et al. (2015a)
Trematoda Digenites proterus Early Cretaceous Indirect: eggs Coprolite Archosaurs Poinar and Boucot T
(2006)
Dicrocoelidae Pleistocene Indirect: eggs Coprolite ?bear Jouy-Avantin et al. T
(1999)
?Gymnophallidae Early Eocene Indirect: characteristic Skeletal Ruiz and Lindberg M
pits in bivalve shells deformation (1989), Todd and
Harper (2011),
Huntley and De
Baets (2015)
?Monogenea Middle Devonian Direct: attachment Fine-grained Placoderms, Upeniece (2001,
structure sediments acanthodians 2011), De Baets
et al. (2015a)
Phylum Acanthocephala
? ? Holocene Indirect: eggs Coprolite Mammals (canids, Fry and Hall (1969), T
humans) Noronha et al.
(1994)
Phylum Annelida
Myzostomida ? Carboniferous Indirect: skeletal Crinoids Welch (1976), M
eJurassic deformations (galls) Hess (2010)
Clitellata ?Hirudinae Triassic Indirect: cocoons Freshwater ? Manum et al. (1991), F
deposits Bomfleur et al.
(2012), Parry et al.
(2014)
Phylum Mollusca
Eulimidae Eulima Upper Cretaceous Direct: isolated shells Marine deposit ? Sohl (1964) M
? Upper Cretaceous Indirect: trace on Skeletal Echinoids Neumann and M
echinoid hosts deformation Wisshak (2009)
Coriaphyllidae Coralliophila (Timothia) Eocene Direct: isolated shells Marine deposit ? Dockery (1980) M
aldrichi
Leptoconchus: 2 species; OligoceneeMiocene Direct: shells associated Skeletal Corals (Cladocera, Lozouet and Renard M
Coralliophila: with coral host deformation Thegioastraea, (1998)
1 species; Galeropsis: Pocillopora)
1 species
Unionidae Unio, Anodonta Quaternary Direct: glochidium Freshwater ?fish Brodniewicz (1968) F
larvae deposits
14 Kenneth De Baets and D. Timothy J. Littlewood
expected even during different ages. Such fossil Lagerst€atte should therefore
be systematically screened for parasites. Further work needs to be done on
establishing characteristic trace fossils and pathologies, particularly in verte-
brates, back in time.
Diptera
Ceratopogonidae Proticulicoides sp. Indirect Plasmodiidae Burmese amber Poinar and Telford (2005),
Boucot and Poinar (2010)
Leptoconops nosopheris Indirect Trypanosomatidae Burmese amber Poinar (2008a)
Culicidae Culiseta sp. Direct Fe ? Kishenehn Formation Greenwalt et al. (2013)
concentrations,
Hemiptera
Reduviidae Triatoma dominicana Indirect Trypanosomatidae Dominicsssan amber Poinar (2005c)
Torirostratidae Torirostratus pilosus Direct Fe concentrations ? Yixian Formation Yao et al. (2014)
Torirostratidae Flexicorpus acutirostratus Direct Fe concentrations ? Yixian Formation Yao et al. (2014)
The Importance of Fossils in the Evolution of Parasites 17
gymnophallids in extant bivalves (Ituarte et al., 2001, 2005), have also been
reported from the Silurian (Liljedahl, 1985), which is not consistent with
extant parasiteehost associations (De Baets et al., 2015a) as shorebirds (Char-
adriiformes), their present day definitive hosts, are believed to have radiated
sometime between the Cretaceous and Eocene periods (Smith, 2015).
Pathologies, therefore, offer less confident evidence for the presence of
parasitic lineages in the fossil record than in body fossils, when no parasitic
remains are found associated with these traces. Direct evidence for the par-
asites associated with such pathologies is mostly restricted to parasitic organ-
isms with mineralized skeletons such as gastropods (Hayami and Kanie,
1980; Lozouet and Renard, 1998; Baumiller and Gahn, 2002). Such traces
are usually compared with known responses to parasites by extant hosts,
which are sometimes not that well-investigated, and by extrapolation it
has been assumed that the same culprits were responsible in the past. This
can be further complicated by the fact that extant phylogenies indicate
that pathology-inducing lineages might have evolved more than once
(e.g. gall- and cyst-forming myzostomids: Summers and Rouse, 2014).
Parasite-induced pathologies have also been reported from hosts that are
now extinct or no longer affected; although their interpretation becomes
more difficult if no modern analogues are available (Owen, 1985; Babcock,
2007; De Baets et al., 2011; De Baets et al., 2015b). Traces which are
reminiscent of nematode borings in foraminifer tests (Sliter, 1971) have
been reported from Cambrian and Ordovician trilobites (Babcock, 2007),
but no conclusive assignment to nematodes as culprits can be made without
direct fossil evidence for associated nematodes. Furthermore, it is still
debated whether these traces in trilobites were made during life or post-
mortem (Owen, 1985). Various pathological reactions in ammonoids (an
extinct group of externally shelled cephalopods) have been attributed to
parasitic flatworms based on their prevalence and similar pathologies in
extant shelled molluscs (De Baets et al., 2011), but as long as no parasite
remains are found associated with them, their attribution to parasitic flat-
worms remains highly speculative at best (De Baets et al., 2015b).
Many palaeontologists also point out the difficulty of defining an inter-
action as being parasitic, although this might be more a problem concerning
the definition of parasitism rather than its recognition (Tapanila, 2008;
Zapalski, 2011), which is not restricted to fossil associations. Some authors
like Tapanila (2008) have suggested that fossil studies should assume that a
symbiosis is neutral (commensal), unless demonstrated otherwise. Other au-
thors have argued that a neutral interaction is absence of an interaction,
20 Kenneth De Baets and D. Timothy J. Littlewood
which cannot be proven, and is therefore unfit for empirical science. The
detection of commensalism is difficult and rather subjective in recent asso-
ciations (usually it is understood as a weak positive or negative interaction)
and as such it seems impossible to detect in the fossil record. Zapalski (2011)
has, therefore, argued avoiding commensalism as a null hypothesis in palae-
oecology, because the possibility of making a type II error is very high. Pos-
itive or negative effects can be detected or inferred based on comparisons
with extant interactions. Identifying traces or pathologies of fossil parasites
can potentially also be performed by demonstrating a negative influence
or effect on growth, body size and/or morphology of their hosts, while a
certain positive effect for the parasite can be inferred. Of course, such inter-
pretations rely on identifying the traces (e.g. borings) or structures as being
made in vivo. This can be most convincingly demonstrated when a host
response (e.g. growth deformation or pathology) can be shown to be asso-
ciated with these structures, often most readily recognized in specimens with
sparse traces or pathologies (De Baets et al., 2011; Donovan, 2015).
Studies have focused particularly on invertebrate hosts, and especially on
those with external shells or exoskeletons, but such pathologies which could
potentially be tracked in the fossil record are also found in vertebrates
including characteristic limb malformations in amphibians (Johnson et al.,
2001, 2002, 2003; Johnson and Sutherland, 2003) or cavities in the mastoid
bone of humans (Oyediran et al., 1975) caused by digenetic trematodes or
trabecula-like bone lesions in cetacean whales (Littlewood and Donovan,
2003) and enlargement of the frontal sinuses accompanied by bone lesions
in mustelids (Rothschild and Martin, 2006) caused by cestodes. Character-
istic skeletal pathologies in terrestrial vertebrates (e.g. mammals) induced by
helminths with resistant eggs have the potential for comparison of preva-
lence of skeletal deformations directly with parasite load or prevalence in
coprolites effectively linking palaeoparasitology and palaeopathology
(compare Dutour, 2013). Some parasitic unicellular pathogens might leave
characteristic traces or pathologies in their hosts. Wolff et al. (2009) studied
erosive lesions in tyrannosaurs and attributed them to Trichomonas gallinae-
like protozoans, because they are reminiscent of similar pathologies in extant
birds caused by this parasite. Unicellular eukaryotes can also leave character-
istic traces in their hosts; for example, borings by foraminifera in marine
echinoderms and bivalves (Neumann and Wisshak, 2006; Beuck et al.,
2007, 2008). In some cases, the host performs activities or exhibits behaviour
induced by the parasites, which can occasionally also be found in the fossil
record. One spectacular example is the death-grip scars found on Eocene
The Importance of Fossils in the Evolution of Parasites 21
3.3 Coprolites
Coprolites are usually defined as fossilized (permineralized) faeces, although
the term is often also used for desiccated, more recent faeces from archaeo-
logical sites (Ferreira et al., 1991; Reinhard and Bryant, 1992; Hunt et al.,
2012). Coprolites have yielded fossil and archaeological evidence for para-
sitic organisms (Table 3) ranging from coccidia or other protozoans (Ferreira
et al., 1992; Schmidt et al., 1992; Poinar and Boucot, 2006; Frías et al., 2013;
Wood et al., 2013b), to parasitic fungi and plant remains (Sharma et al.,
2005; Wood et al., 2012), to helminths (Gonçalves et al., 2003; Savinetsky
and Khrustalev, 2013), including acanthocephalans (Noronha et al., 1994),
but particularly nematodes (Ferreira et al., 1991, 1993; Poinar and Boucot,
2006; Leles et al., 2010; Da Silva et al., 2014; Hugot et al., 2014) and various
groups of parasitic flatworms (Schmidt et al., 1992; Jouy-Avantin et al.,
1999; Dentzien-Dias et al., 2013). Coprolites can therefore be an important
additional source of ancient parasitism supplementary to amber, where the
record is heavily biased towards arthropods and their terrestrial parasites.
In ideal cases, coprolites are still associated with their producer, which
makes it possible to confidently identify their origin and therefore the
host taxon of the fossil parasites. The coprolite producer may correspond
with the host of the parasite or more rarely as the one who ingested the para-
site and/or host. However, most frequently, coprolites are found in isola-
tion, where the identity of the producer can only be inferred from their
morphology and content (Poinar and Boucot, 2006; Dentzien-Dias et al.,
2013), and, in the case of more recent specimens, by aDNA analysis
(Wood and Wilmshurst, 2014). Invertebrate coprolites might also have
The Importance of Fossils in the Evolution of Parasites
Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organisms
Taxonomic affinity Fossil evidence Age Host References
Protozoa
Coccidia
Eimeriorina Oocyst Holocene Ground sloth Schmidt et al. (1992)
(Nothrotheriops
shastensis)
Eimeridae Oocysts (Eimera) Holocene Deer Ferreira et al. (1992)
Cryptosporidiidae aDNA (Cryptosporidium) Holocene Moas (Dinomis robustus, Wood et al. (2013b)
Pachyornis
elephantopus)
Helminths
Platyhelminthes
Cestoda Egg þ developing Permian ?elasmobranchs Dentzien-Dias et al. (2013)
embryo
Trematoda Eggs Cretaceous Archosaur (?dinosaur) Poinar and Boucot (2006)
Dicrocoelidae Eggs Pleistocene Mammal (?bear) Jouy-Avantin et al. (1999)
Schistosomatidae Schistosome-like eggs Holocene Ground sloth Schmidt et al. (1992)
(Nothrotheriops
shastensis)
Nematoda
? Larvae Pleistocene Hyenid Ferreira et al. (1993)
Ascaridomorpha Eggs Triassic Cynodont Da Silva et al. (2014)
Oxyurida Eggs Triassic Cynodont Hugot et al. (2014)
(Continued)
23
Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organismsdcont'd
24
Taxonomic affinity Fossil evidence Age Host References
Ascaridomorpha Egg þ developing Cretaceous Archosaur (?dinosaur) Poinar and Boucot (2006)
larvae
Heterakoidea aDNA Holocene Archosaur Wood et al. (2013b)
(Anomalopteryx,
Dinornis, Pachyornis,
Megalapteryx)
Trichocephalida Eggs (Trichuris) Pleistocene Hyenid Ferreira et al. (1991)
Acanthocephala
? Eggs Holocene Humans Fry and Hall (1969)
Eggs (Echinopardalis) Holocene Felidae Noronha et al. (1994)
Arthropods
Ticks Body remains Holocene Humans Johnson et al. (2008)
unexpectedly old age estimates of clades (Arcila et al., 2015) and their per-
formance needs to be more extensively tested. Furthermore, such methods
might be difficult to apply to soft-bodied taxa as crucial morphological char-
acters required to confidently place them in extant phylogenies might be ab-
sent or limited in fossil parasite specimens.
Computed tomography will be important to reveal additional details of
the morphology and structure of putative body fossils, which will make it
possible to assign them more accurately to extant lineages. In some cases,
the nearest free-living relatives have a good fossil record, which can be
used to put constraints on early nodes in molecular clocks. Interestingly,
this is not always the case. In some soft-bodied helminths, the body fossil
record of parasitic forms is even richer (at least less poor) than that in their
free-living relatives, such as amongst Platyhelminthes (Poinar, 2003; De
Baets et al., 2015a) and Nematoda (Poinar, 2011a, 2015a). Their fossil re-
cord remains are rare in time and space due to their restriction to sites of
exceptional preservation, but can potentially still be valuable to place con-
straints on the evolution of these groups as a whole. In the absence of reliable
body fossils, characteristic traces or pathologies could potentially also be used
to put constraints on certain nodes and computed tomography could also be
possibly used to characterize those (Dittmar et al., 2011). Unfortunately,
skeletal responses to parasitism are still comparatively poorly studied, partic-
ularly in extant taxa (Zibrowius, 1981; Ituarte et al., 2001, 2005; Keupp,
2012; Klompmaker et al., 2014). This makes interpretation of fossil traces
even more open to interpretation as they could also have been made by a
different group of organisms with a similar behaviour, but not necessarily
closely related. It therefore probably makes more sense to avoid using
them to constrain molecular clocks directly. Molecular clocks constrained
by other types of evidence (e.g. body fossils or geological events) could how-
ever be used to test the appearances of these skeletal responses.
Problematically, the fossil record does not yield body fossils or other re-
mains for multiple lineages of unicellular pathogens or soft-bodied metazoan
parasites (e.g. Myxozoa, Argulidae). In these cases, it is therefore necessary to
look for and select suitable alternatives, or supplementary ways, to constrain
the molecular clock (Bensch et al., 2013; De Baets et al., 2015a; Héritier
et al., 2015). Such solutions potentially lie in the host fossil record or biogeo-
graphic events, which have left a footprint of divergence among
evolutionary lineages. Unfortunately, host or biogeographic calibrations
have not received the same scrutiny and refinement as fossil calibrations
(Kodandaramaiah, 2011; De Baets and Donoghue, 2012; Parham et al.,
The Importance of Fossils in the Evolution of Parasites 33
accurate timescale that might lack precision, than a precise timescale that
lacks the necessary accuracy (De Baets et al., 2015a). Even if no suitable cali-
bration points can be found, methods have been developed, which can
compare the relative molecular rates of groups to test the hypotheses of
co-divergences (Loader et al., 2007; Hibbett and Matheny, 2009; Loss-Oli-
veira et al., 2012; Silva et al., 2015).
5. FUTURE PERSPECTIVES
Various new advances in ancient biomolecule detection and charac-
terization (Briggs and Summons, 2014) including aDNA (Dittmar, 2009,
2014; Wood et al., 2013b; Dittmar, 2014; Shapiro and Hofreiter, 2014;
Hofreiter et al., 2015), palaeoproteomics (Hofreiter et al., 2012), novel
development in molecular clock methodologies (Parham et al., 2012; Ho,
2014; W€ orheide et al., 2015) and new possibilities for the critical evaluation
and nondestructive analysis of 3D fossil structures by computed tomography
(Cunningham et al., 2014a,b; Sutton et al., 2014) offer many new prospects
and perspectives in palaeoparasitology.
36 Kenneth De Baets and D. Timothy J. Littlewood
ACKNOWLEDGEMENTS
We are very grateful to Andrea Waeschenbach and Rod Bray for constructive comments on
an earlier draft of the manuscript. The initial research leading to this article was partially
funded by an SNF-grant for Prospective Researchers to KDB (141438).
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CHAPTER TWO
Contents
1. Introduction 54
2. Media for the Study of Fossil Nematodes 54
2.1 Amber 54
2.2 Rock fossils 54
2.3 Coprolites 55
3. Palaeozoic Parasitic Nematodes 55
4. Parasitic Nematode Body Fossils from the Mesozoic 55
5. Nematode Parasites from the Early Cenozoic 60
5.1 Baltic amber 60
6. Nematode Parasites from the OligoceneeMiocene 65
6.1 Dominican amber nematodes 65
6.2 Mexican amber nematodes 75
7. Nematode Parasites from the Pliocene 77
8. Nematode Parasites from the Pleistocene and Holocene 77
8.1 Nematode parasites of humans from the Pleistocene and Holocene 78
9. Stages in the Evolution of Nematode Parasites of Invertebrates 79
10. Origin of Nematode Parasites of Vertebrates 81
11. Origin of Nematode Parasites of Plants 83
12. Summary 83
Acknowledgements 86
References 86
Abstract
This chapter discusses the evolutionary history of nematode parasites of invertebrates,
vertebrates and plants based on fossil remains in amber, stone and coprolites dating
from the Palaeozoic to the Holocene. The earliest parasitic nematode is a primitive plant
parasite from the Devonian. Fossil invertebrate-parasitic nematodes first appeared in
the Early Cretaceous, while the earliest fossil vertebrate-parasitic nematodes are from
Upper Triassic coprolites. Specific examples of fossil nematode parasites over time
are presented, along with views on the origin and evolution of nematodes and their
hosts.
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.03.002 All rights reserved. 53
54 George O. Poinar, Jr.
1. INTRODUCTION
The body fossil record of parasitic nematodes is limited by their small
size and soft bodies (Littlewood and Donovan, 2003). While parasitic forms
can reach up to several metres in length (Yeates and Boag, 2006), decompo-
sition after death is quite rapid, and sclerotized structures that could be fossil-
ized are microscopic, which makes them extremely difficult to locate. While
some nematodes have been preserved in fine-grained cherts dating back to
the Devonian, fossilized resin (amber) and coprolites have been the most use-
ful media for studying the evolution and early hosts of parasitic nematodes.
2.3 Coprolites
Analysis of lithified coprolites dating back millions of years (e.g. Poinar and
Boucot, 2006; Da Silva et al., 2014; Hugot et al., 2014) and desiccated dung
of more recent ages (Poinar, 2014) can reveal the presence of vertebrate-
parasitic nematodes. Ancient dung samples also are one of the best resources
for establishing early records of human nematode parasites (Gonçalves et al.,
2003). However, it can be difficult to distinguish between actual nematode
parasites and microbotrophic nematodes that entered the dung after it was
deposited (Poinar, 1983).
Figure 1 Palaeonema phyticum Poinar et al., 2008 surrounded by cortical cells of Aglao-
phyton major in Devonian Rhynie Chert, Aberdeen, Scotland (Scale bar ¼ 59 mm).
Figure 2 The mermithid, Cretacimermis protus Poinar and Buckley, 2006 emerging from
a biting midge in Early Cretaceous Burmese amber (Ron Buckley amber collection)
(Scale bar ¼ 1 mm).
The Geological Record of Parasitic Nematode Evolution 57
Infection was probably initiated in the larval stage of the midge and the
parasite was carried through the pupal and into the adult stage. Such hoste
parasite associations still occur today (Poinar and Poinar, 2003).
Mid-Cretaceous Burmese amber contains both plant and animal nema-
tode parasites. A small population of the fungal-feeding aphelenchoidid,
Cretaciaphelenchoides burmensis Poinar (2011), together with mycelium, pro-
vides the earliest record of mycetophagous nematodes. Adult males and
females, as well as resistant juvenile stages were present. The nematodes
could have been carried to the site by wood-boring insects, as occurs in
extant members of the family (Hunt, 1993).
A snail in Burmese amber with juveniles of Palaeocosmocerca burmanicum
Poinar (2011) adjacent to its mantle cavity provide early evidence of the
family Cosmocercidae. Features of the fossil nematodes resemble those of
the extant snail parasite, Cosmocercoides dukae (Anderson, 1960). The adults
of C. dukae live in the intestinal tract of the snail, and second stage juveniles
and third stage infectives occur in the mantle cavity. A sibling species of C.
dukae occurs in the rectum of frogs and toads (Harwood, 1930; Vanderburgh
and Anderson, 1987), but it is likely that molluscs were the original host of
Cosmocercoides spp.
Oxyurids may be the first nematodes to form parasitic associations with
terrestrial animals, beginning with invertebrates and then expanding their
host range to vertebrates. While the origin of oxyurids could extend back to
the Silurian based on the earliest fossils of their millipede hosts (Wilson and
Anderson, 2004), when they first invaded insects is unknown. The thelasto-
matid, Paleothelastoma tipulae Poinar (2011) adjacent to a cranefly in Burmese
amber (Figure 3) establishes the earliest fossil record of this group in inverte-
brates. Extant craneflies are common hosts of thelastomatids (Poinar, 1975).
Figure 4 Proheterorhabditis burmanicus Poinar (2011) (arrow) adjacent to its beetle host
in Early Cretaceous Burmese amber (Scale bar ¼ 152 mm).
Figure 5 The mermithid, Cretacimermis protus Poinar and Buckley, 2006 emerging from
a biting midge in Early Cretaceous Burmese amber (Scale bar ¼ 1 mm).
Figure 6 Egg of the early Cretaceous Ascarites priscus Poinar and Boucot, 2006 in a
coprolite of the predatory dinosaur, Megalosaurus from the Bernissant Wealden Iguan-
odon locality in Belgium (Scale bar ¼ 11 mm).
60 George O. Poinar, Jr.
Figure 8 The mermithid, Heydenius formicinus Poinar, 2002 emerging from a male
winged ant (Prenolepis henschei Mayr) in Baltic amber (Scale bar ¼ 640 mm).
62 George O. Poinar, Jr.
Figure 9 The mermithid, Heydenius brownii, Poinar, 2001, emerging from an achiliid
planthopper in Baltic amber (Scale bar ¼ 2.6 mm).
(Rasnitsyn and Quicke, 2002), hemipterans could have been ancient terres-
trial hosts for mermithids.
Several different lineages of parasitic nematodes have been found to
attack sciarid fungus gnats (Diptera: Sciaridae) in Baltic amber. One was a
mermithid, Heydenius sciarophilus Poinar (2011) (Figure 10) and another a
tetradonematid, Palaeotetradonema sciarae Poinar (2011). A third parasite line-
age was represented by Tripius balticus Poinar (2011) of the family Sphaeru-
lariidae. Several nematodes were still inside the body cavity of the adult host
while others had emerged (Figure 11). The life cycle of the fossil was prob-
ably similar to that of the extant species, Tripius sciarae (Bovien).
Other dipterous hosts of mermithids in Baltic amber were gall gnats
(Cecidomyiidae). One specimen of Heydenius cecidomyae Poinar (2011)
had completely emerged from the gall gnat while the second was only partly
Figure 10 Heydenius sciarophilus Poinar (2011) emerging from a sciarid fungus gnat in
Baltic amber (Scale bar ¼ 207 mm).
The Geological Record of Parasitic Nematode Evolution 63
Figure 11 Parasitic juveniles of Tripius balticus Poinar (2011) (arrow) that emerged from
a sciarid fungus gnat in Baltic amber (Scale bar ¼ 322 mm).
emerged (Figure 12). There are no reports of extant gall gnats parasitized by
mermithids.
Another parasite lineage of Diptera was represented by the allantonematid,
Howardula helenoschini Poinar (2003) that parasitized scuttle flies (Phoridae).
Five specimens of H. helenoschini were clustered at the posterior tip of the fly’s
abdomen, obviously having just exited from the host’s body cavity (Figure 13).
The lemon-shaped parasitic female of H. helenoschini could be detected
through the host’s abdomen. Extant phorid flies are parasitized by Howardula
nematodes globally (Richardson et al., 1977; Poinar, 1975; Disney, 1994).
The nematodes normally leave the fly host via the intestine or reproductive
system (Richardson et al., 1977) and that is probably the route used by the
five fossil nematodes.
Another Baltic amber nematode in the allantonematid lineage was Palae-
oallantonema baltica Poinar (2011) that was parasitizing a rove beetle (Staph-
ylinidae). A number of last stage juveniles that had exited the host consisted
of two morphotypes: females of the first generation and pre-adults of the
second generation.
Hematophagous flies in Baltic amber also were associated with vertebrate
nematode parasitic lineages. Blackflies (Simuliidae) and biting midges (Cera-
topogonidae) are the most common biting insects in Baltic amber. A micro-
filaria of Cascofilaria baltica Poinar (2011, 2012) was adjacent to a blackfly with
a swollen abdomen, suggesting that the fly had taken a blood meal shortly
before falling in the resin. The microfilaria falls within the size range of those
of extant Onchocerca spp., a worldwide genus infecting mammals and vectored
by blackflies. This represents the oldest fossil record of a filarial nematode.
Still additional insect hosts of mermithid nematodes in Baltic amber
include a moth (Lepidoptera) parasitized by Heydenius podenasae Poinar
The Geological Record of Parasitic Nematode Evolution 65
Figure 14 Adult caddis fly (Triaenodes balticus Wichard and Barnard, 2005) parasitized
by Heydenius trichorosus Poinar (2012) in Baltic amber (Scale bar ¼ 1.4 mm).
(2012), an adult caddis fly, Triaenodes balticus Wichard and Barnard, 2005
(Trichoptera) parasitized by Heydenius trichorosus Poinar (2012) (Figure 14)
and a phasmatid, Balticophasma sp. (Phasmatodea: Phasmatidae) parasitized
by Heydenius phasmatophilus Poinar (2012) (Figure 15).
Spiders were also parasitized by mermithid nematodes in the Baltic
amber forest, and Heydenius araneus Poinar (2000) from a crab spider (Tho-
misidae) (Figure 16) is the earliest record of nematode parasitism of spiders.
eggs (Figure 17) that had escaped through a hole in the gaster (abdomen) of
a species of Cephalotes Latreille, 1803. The fossil probably had a life cycle
similar to the extant Myrmeconema neotropicum Poinar and Yanoviak
(2008), a parasite of Cephalotes atratus (L.). The life cycle of this group is
especially fascinating and unique. When females of M. neotropicum have
matured and the body cavity of the ant is filled with eggs, the color of
Figure 16 The spider mermithid, Heydenius araneus Poinar (2000) adjacent to its clu-
bionid spider host in Baltic amber (Scale bar ¼ 2 mm).
The Geological Record of Parasitic Nematode Evolution 67
Figure 17 Eggs of Myrmeconema antiqua Poinar (2011) from an ant of the genus Ceph-
alotes Latreille in Dominican amber (Scale bar ¼ 360 mm).
the host’s gaster changes from black to a shiny red. The bright red abdomen
resembles ripe berries that are relished by birds. The infected ants stand on
stems and raise their abdomens high in the air. When a bird ingests an
infected ant, the eggs of M. neotropicum pass thought the bird’s digestive tract
and are deposited in the droppings. Worker ants collect and feed the
infested bird droppings to their brood. The ingested nematode eggs hatch
in the larval guts and the juveniles penetrate into the insect’s body cavity. It
appears that this complicated life cycle was established already some 20e30
million years ago.
Cephalotes ants are also hosts to a third parasite lineage, the Allantonema-
tidae. Mature juveniles of Palaeoallantonema cephalotae Poinar (2011) were
emerging from a worker of Cephalotes serratus in a piece of amber (Figure 18).
A similar hosteparasite association occurs with an undescribed allantonema-
tid and workers of Cephalotes christopherseni in Peru.
A separate lineage of allantonematids, represented by Palaeoparasitylenchus
dominicana Poinar (2011) parasitized drosophilid fruit flies in the Dominican
amber forest. A female fly was heavily infected and large numbers of juve-
niles and second-generation female nematodes were adjacent to the host
(Figure 19). The life cycle of P. dominicanus was probably similar to that
68 George O. Poinar, Jr.
Figure 20 Two specimens of the mermithid, Heydenius psychodae Poinar (2011), with
their moth fly host in Dominican amber (Scale bar ¼ 800 mm).
alternating between insects and fungi are ancient and provides an evolu-
tionary scenario that insect parasitism by tylenchoid nematodes may have
evolved from mycetophagous lineages.
Strictly mycetophagous nematodes of aphelenchoidid lineages have also
been described from Dominican amber. The stylet-bearing Bursaphelenchus
similus Poinar (2011) probably originated from a gallery belonging to an
adjacent platypodid beetle. Some 60 specimens of the aphelenchoidid Crypt-
aphelenchus dominicus Poinar (2011) were associated with an adult platypodid
beetle. Many of them were dauer (resistant) juveniles, which is a phoretic
stage. A third lineage was represented by numerous individuals of Oligaphe-
lenchoides dominicanus Poinar (2011) feeding on a large mat of adjacent fungal
hyphae.
Also in Dominican amber are nematode parasites of herbivorous insects.
The allantonematid, Palaeoallantonema apionae Poinar (2011) was parasitizing
an apionid weevil, and numerous individuals of the diplogastrid, Synconema
dominicana Poinar (2011) were adjacent to a fig wasp (Hymenoptera: Agao-
nidae) (Figure 22), thus providing indirect evidence of fig trees in the ancient
forest. Based on their attenuated head, lack of a stylet, rounded lip region
and elongate tail, S. dominicana was placed in the Parasitodiplogaster clade,
an extant genus that parasitizes figs wasps in Africa and Mesoamerica (Poinar,
1979; Poinar and Herre, 1991).
Fossil-parasitic nematodes of higher plants are extremely rare; however,
numerous specimens of Oligaphelenchoides maximus Poinar (2011) in all
developmental stages were found in a section of a monocot rootlet in
Dominican amber (Figure 23). The long, slender, stylet-bearing adults
The Geological Record of Parasitic Nematode Evolution 71
and males with a C-shaped terminus align the species with members of the
Aphelenchoididae.
Another species of stylet-bearing plant-parasitic nematode in Dominican
amber was the anguinid, Palaeoanguina dominicana Poinar (2011) (Figure 24).
It apparently had been feeding within and then attempted to escape from a
seed that fell in the resin. Extant anguinids can withstand desiccation and
survive for years in dried seeds.
One interesting lineage of aphelenchoidids in Dominican amber is the
Acugutturidae Hunt (1993). Extant representatives are ectoparasites on
the external surface of insects, especially moths. Several specimens of Seto-
nema protera Poinar (2011) belong to this family. One large specimen is adja-
cent to its moth host (Figure 25), while another is some distance away.
Figure 25 The ectoparasitic nematode Setonema protera Poinar (2011) (arrow) adja-
cent to its moth host in Dominican amber (Scale bar ¼ 245 mm).
The Geological Record of Parasitic Nematode Evolution 73
Figure 26 A specimen of Heydenius dominicus Poinar, 1984 inside the body cavity of a
Culex mosquito in Dominican amber (Scale bar ¼ 348 mm).
Figure 27 Parasitic juvenile of Heydenius saprophilus Poinar (2011) adjacent to its wood
gnat host (Diptera: Anisopodidae) in Dominican amber (Scale bar ¼ 971 mm).
Since the wasp larvae develop as internal insect parasites, it is possible that the
nematodes were also parasitizing the same host and entered the wasp larva.
that served as their food source (Figure 31). Also present were nematopha-
gous fungi that had parasitized several individuals of O. atrebora (Jansson and
Poinar, 1986) (Figure 32).
Few parasitic nematodes have been recovered from Mexican amber;
however, one interesting species was the tetratonematid, Palaeotetradonema
dating from 3553 to 3550 BC, include treatments for ascarids (Ascaris lumbri-
coides L.), hookworms (Ancyclostoma duodenale Dubini) and Guinea worms
(Dracunculus medinensis L.) (Bryan, 1931; Ebbell, 1937).
Additional nematodes found in Egyptian mummies, but not mentioned
in the Papyrus Ebers, were whipworms (Trichuris trichiura L.), filarial nema-
todes (probably Wuchereria Silvo Araujo or Brugia spp.), and Trichinella spiralis
Owen and Stronglyoides stercoralis Bavay. Mummies show that Egyptians
were parasitized by ascarids some 2200 years ago (Cockburn et al., 1975),
infections of D. medinensis 3991e3786 years ago (Tapp and Wildsmith,
1993) and scrotal filarial nematodes (Tapp and Wildsmith, 1993).
It is curious that pinworms (Enterobius vermicularis L.) have only been
rarely recovered from ancient Egyptian mummies (Horne, 2002) and are
not mentioned in the Papyrus Ebers. Since the earliest record of pinworms
is from the New World, perhaps this species originated in the Americas,
although this might be a sampling bias.
The oldest records of human hookworms are 7230-year-old eggs recov-
ered from coprolites in Brazil (Montenegro et al., 2006; Ferreira et al.,
1987), showing that the parasites were present in South America well before
the Spanish invasion.
The whipworm, T. trichiura, infects slightly over 1000 million humans
worldwide today (Crompton, 1999). The oldest record of human parasitism
by this species dates back between 7000 and 8000 BP based on eggs from
human remains in a pre-Colombian bog in Chile, suggesting that this species
is endemic to the New World although Klicks (1990) concluded that both
T. trichiura and E. vermicularis were introduced to the New World by people
migrating across the Bering strait from Siberia.
When parasitic nematodes were originally acquired by humans is
unknown. Recent studies on nematode parasites of nonhuman primates
suggest that at least all human intestinal nematodes could have been acquired
from other primates (Dupain et al., 2009; Kaur and Singh, 2009). In fact, it is
likely that most, if not all, nematode parasites that plague humans today were
obtained through their distant ancestors and domesticated animals.
Precambrian, even earlier than has been proposed using relaxed molecular
clock methodologies (Rota-Stabelli et al., 2013), and were parasitizing marine
invertebrates by the Cambrian and terrestrial invertebrates by the Ordovician
based on extrapolations from extant parasiteehost relationships and the fossil
record of the hosts of nematode parasites (Poinar, 2011).
Early hosts of nematode parasites of invertebrates were probably repre-
sentatives of Tetradonematidae, Marimermithidae, Echinomermellidae,
Benthimermithidae, Monhysteridae and Leptolaimidae (see Poinar (2011)
for the systematic placement of these groups) that today parasitize marine
ostracods, copepods, shrimp, amphipods and isopods (Petter, 1980; Poinar
et al., 2002, 2009), starfish (Asteroidea) (Rubtsov and Platonova, 1974;
Rubtsov, 1977), brittle stars (Ophiuroidea) (Ward, 1933), sea urchins
(Echinoidea) (Gemmill and Von Linstow, 1902; Jones and Hagen, 1987),
priapulids (Rubtsov, 1980), polychaetes (Petter, 1983), tubicifid oligo-
chaetes (Hallett et al., 2001), foraminifera (Hope and Tchesunov, 1999)
and marine nematodes (Chesunov, 1988; Tchesunov and Spiridonov,
1993). Some of these host groups, such as polychaetes, ostracods and fora-
minifera, have fossil records extending back to the Cambrian (Lehmann and
Hillmer, 1983).
Today, members of the Mermithidae parasitize invertebrates in the
marine and terrestrial habitat. When mermithids shifted towards land,
marine amphipods and intertidal chironomid midges could have served as
hosts (Poinar, 1975; Schlinger, 1975; Poinar et al., 2002). Chironomid
midges have a fossil record extending back to the Late Triassic (Rasnitsyn
and Quick, 2002) and Cretacimermis and Heydenius show that mermithid
parasitism of these flies was present in the Early Cretaceous.
Later, mermithids selected freshwater aquatic or semiaquatic Diptera as
hosts, such as biting midges (Ceratopogonidae), scavenger flies (Scatopsi-
dae), gall gnats (Cecidiomyiidae), moth flies (Psychodidae), wood gnats
(Anisopodidae), scuttle flies (Phoridae), fruit flies (Drosophilidae) and
fungus gnats (Sciaridae and Mycetophilidae). These insect families all
have fossil records dating back to the Jurassic (Rasnitsyn and Quicke,
2002).
Three terrestrial groups of invertebrate-parasitic nematodes, the oxy-
urids, drilonematids and cosmocercoids, are particularly primitive and
were the possible first terrestrial parasites of invertebrates (Osche, 1963;
Inglis, 1965). Oxyurids probably parasitized invertebrates before verte-
brates and while P. tipulae) establishes the oxyurids as parasites of Diptera
in the Early Cretaceous, pinworms could have potentially already occurred
The Geological Record of Parasitic Nematode Evolution 81
in earliest known (Silurian) millipedes. Other early hosts for oxyurids could
have been isopods (Schwenk, 1927) and annelids (Poinar, 1978b; Yeates
et al., 1998). The drilonematids represent a primitive, but highly special-
ized lineage now confined to the coelom of earthworms. The discovery
of Mesidionema praecomasculatis Poinar (1978a), an earthworm parasite that
has morphological and biological features of both oxyurids and drilonema-
tids, suggests that drilonematids could have evolved as a specialized clade
from oxyurids.
The Cosmocercoids may have evolved in gastropods Anderson, 2000;
McClelland, 2005), and P. burmanicum shows that a snail-infecting lineage
was already in existence by the Early Cretaceous (Poinar, 2011). Infected
snails eaten by amphibians could have initiated the vertebrate-parasitic
taxa, although it has been suggested that amphibians may have been the
original hosts (Vanderburgh and Anderson, 1987).
The first fossil record of parasitic rhabditids is the Early Cretaceous Pro-
heterorhabdites burmanicus parasitizing a rove beetle. Heterorhabditids are
thought to have evolved from free-living, intertidal rhabditids (Poinar,
1993) and their early hosts could have been beach dwelling crustaceans (iso-
pods, amphipods, etc.) and intertidial insects.
Insect-parasitic tylenchs and aphelenchs probably evolved from myce-
tophagous lineages like Cryptaphylenchus dominicus that were associated
with platypodid beetles. This could lead to dual fungal and insect parasitism
as seen in the Dominican amber Paleoiotonchium dominicanum that probably
had a life cycle alternating between mushrooms and fungus gnats. While
there is no evidence of fungal fruiting bodies in the amber piece with Pale-
oiotonchium, mushrooms and other fungi occur in Dominican amber (Poinar
and Poinar, 1999; Boucot and Poinar, 2010). The fossil representatives of
Howardula, Palaeoallantonema, Palaeoparasitylenchus and Tripius show that the
typical allantonematidesphaerularid life cycle involving only insect hosts
existed by the beginning of the Cenozoic.
12. SUMMARY
Since nematodes most likely evolved in the sea (Poinar, 2011), it is
highly likely that the earliest animal parasites already lived in trilobites,
eurypterids and other marine invertebrates, although so far no direct fossil
evidence has become known. The first vertebrate parasites might have used
84 George O. Poinar, Jr.
85
86 George O. Poinar, Jr.
ACKNOWLEDGEMENTS
The author would like to acknowledge E. J. Brill and ‘Nematology’ for previously having
published many of the figures used in the present work.
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CHAPTER THREE
Contents
1. Introduction 94
2. Assessment of the Flatworm Fossil Record 96
2.1 Devonian fossil hook circlets 97
2.2 Silurian blister pearls and calcareous concretions in bivalve shells 101
2.3 Permo-Carboniferous egg remains in shark coprolites 103
2.4 Cretaceous egg remains in terrestrial archosaur coprolites 105
2.5 Eocene shell pits in intermediate bivalve hosts 106
2.6 Eggs remains in a Pleistocene mammal coprolite 107
2.7 Holocene evidence for parasitic flatworms from ancient remains 107
2.8 Free-living flatworms 108
3. Interpolating or Extrapolating Extant ParasiteeHost Relationships and the 110
Assumption of ParasiteeHost Coevolution
4. Molecular Clock Studies 113
5. Conclusions and Future Prospects 119
Acknowledgements 121
References 122
Abstract
Novel fossil discoveries have contributed to our understanding of the evolutionary
appearance of parasitism in flatworms. Furthermore, genetic analyses with greater
coverage have shifted our views on the coevolution of parasitic flatworms and their
hosts. The putative record of parasitic flatworms is consistent with extant host
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.06.002 All rights reserved. 93
94 Kenneth De Baets et al.
associations and so can be used to put constraints on the evolutionary origin of the par-
asites themselves. The future lies in new molecular clock analyses combined with addi-
tional discoveries of exceptionally preserved flatworms associated with hosts and
coprolites. Besides direct evidence, the host fossil record and biogeography have the
potential to constrain their evolutionary history, albeit with caution needed to avoid
circularity, and a need for calibrations to be implemented in the most conservative
way. This might result in imprecise, but accurate divergence estimates for the evolution
of parasitic flatworms.
1. INTRODUCTION
Parasitic flatworms (Platyhelminthes: Neodermata) are a highly
diverse group containing many parasites of biomedical, veterinary and eco-
nomic importance (Olson and Tkach, 2005; Littlewood, 2006). Time con-
straints on the origin and evolution of parasitism in this group are still poorly
resolved due to their patchy and largely overlooked fossil record (Littlewood
and Donovan, 2003; Littlewood, 2006). The fossil record of parasitic
flatworms is often disregarded by parasitologists (Combes, 2001; Littlewood,
2006; Verneau et al., 2009a; Badets et al., 2011) and evolutionary (paleo)bi-
ologists (Labandeira, 2002; Erwin et al., 2011; Wey-Fabrizius et al., 2013)
alike. Most parasitologists have therefore focused on extrapolating or inter-
polating extant parasiteehost associations to infer information on the
evolution history of parasitic flatworms (Llewellyn, 1987; Brooks, 1989;
Brooks and McLennan, 1993; Boeger and Kritsky, 1997; Hoberg, 1999;
Hoberg et al., 1999; Littlewood et al., 1999a). Nevertheless, the last two
decades have seen several new fossil discoveries, which have extended the
record from certain lineages of parasitic flatworms deeper into the Cenozoic
( Jouy-Avantin et al., 1999; Todd and Harper, 2011) or from the Cenozoic
to the Mesozoic (Poinar and Boucot, 2006) or even the Paleozoic
(Upeniece, 2001, 2011; Dentzien-Dias et al., 2013).
Furthermore, molecular analyses have considerably shifted our views on
flatworm phylogeny (Lockyer et al., 2003a; Olson and Tkach, 2005;
Littlewood, 2008; Perkins et al., 2010; Laumer and Giribet, 2014) with
implications for older hypotheses of parasiteehost coevolution. Due to
the patchy fossil record, establishing the phylogeny of flatworms is particu-
larly important for establishing a timeline for the group. Traditionally, Mon-
ogenea (ectoparasitic with simple life cycles) and Cestoda (endoparasitic with
complex, trophically transmitted, life cycles) were often grouped based on
morphological similarities of their larval stages (Bychowsky, 1937; Brooks,
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 95
free-living flatworms has proven even more problematic (but see Littlewood
and Waeschenbach, 2015 for a review of recent advances) and has been
further complicated by the fact that some extant forms traditionally included
in Platyhelminthes have been excluded from the phylum based on molec-
ular analyses (Jondelius et al., 2002; Telford et al., 2003; Willems et al.,
2006; Wallberg et al., 2007; Hejnol et al., 2009) such as the Acoela
(Ruiz-Trillo et al., 1999; Mwinyi et al., 2010; Philippe et al., 2011) and Xen-
oturbella (Bourlat et al., 2003). Furthermore, platyhelminths have often been
grouped in the Platyzoa (Cavalier-Smith, 1998) together with various other
taxa including Acanthocephala, which have convergently evolved a parasitic
lifestyle with larval stages and have been shown to be closely related with
free-living Rotifera (Near, 2002; Weber et al., 2013). It remains unclear
whether Platyzoa is a clade or an artificial grouping generated by systematic
error and long-branch attraction artefacts (Edgecombe et al., 2011; Wey-
Fabrizius et al., 2013; Struck et al., 2014), since subsequent studies have
not only disagreed on the membership of the phyla, but also on the relation-
ships within this grouping. This makes new fossil discoveries of parasitic flat-
worms not only relevant in constraining the evolutionary origin of
flatworms, but also that of the Platyzoa as a whole.
Here we review the potential of fossil flatworm evidence with a view to
using these data to constrain the timescale for the evolutionary history of this
group and outline how they can be used to improve our understanding of
the evolutionary radiation of the Neodermata. We consider whether these
rare fossil finds are at least consistent with coevolution of parasitic flatworms
and their hosts, as well as how fossil finds and other geological evidence in
combination with molecular clock methodology can be best used to
constrain the temporal framework for the evolution of parasitic flatworms.
Such a temporal framework is a key to test evolutionary hypotheses
regarding the origin and diversification of parasitism and its coincidence
with certain biogeographic events, major environmental changes or key
ecological or evolutionary events in the evolution of their hosts.
(d)
(e)
(f) (g)
Figure 1 Fossil helminth remains in Middle Devonian gnathostomes (Upeniece, 2001,
2011) (Modified from Upeniece (2011) unless otherwise stated.): (a) Locations where hel-
minth remains were found on juveniles of the placoderm Asterolepis ornata. (b) Multiple
fossil circlets of parasitic helminth hooks (marked with ellipses in (a)) found inside the
acanthodian Lodeacanthus gaujicus, LDM 270/18c (Upeniece, 2001, Pl. 3, Figure 2); (c)
Close-up on the hook circlet found associated with L. gaujicus, specimen LDM 270/
33; (d) Locations where helminth remains were found in juvenile and adults of the
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 99
=
acanthodian L. gaujicus; (e) Schematic drawing of circlets of fossil hooks (Modified from
Upeniece (1999).) found in juveniles of placoderm fish A. ornata (No 1e11), in juveniles
and adults of acanthodian L. gaujicus (No 12e23), and in/on crustacean Mysidacea (No
24); (f) Fossil hooks found in juvenile acanthodian body near the scapula (see also
Figure 1(e), No. 17), LDM 270/4a; (g) fossil hooks found near a clam shrimp. All speci-
mens derive from the Middle Devonian, Liepa (Lode) pit. Dark grey circles, squares e
possible endoparasites; Light grey circles, squares e possible ectoparasites.
100 Kenneth De Baets et al.
(a) (b)
(c)
(d) (e)
Figure 2 Shell structures (igloo-shaped concretions, shell pits) which have been linked
with gymnophallid trematodes (Digenea) in extant and fossil bivalves. (a) Metacercaria
lodged in live position into an igloo-shaped calcareous covering of Gaimardia trapesina
(MLP 5659) from Beagle Channel in Ushuaia; note the noncalcified area around the
anterior end of the larva (photo: Cristian Ituarte; refigured from Ituarte et al. (2005).);
(b) Scanning electron micrograph of a left valve of Cyamiomactra sp. from a Holocene
sample of Río Varela (Tierra del Fuego) showing a single igloo-shaped covering just
below the anterodorsal margin (Photo: Cristia n Ituarte; refigured from Ituarte et al.
(2005).); (c) Upper view of an igloo-shaped covering in G. trapesina (MLP 5659) from
Beagle Channel in Ushuaia showing the non-calcified area in front of the igloo opening
(Photo: Cristian Ituarte; refigured from Ituarte et al. (2005).); (d) Igloo-shaped concretion
found close to posterior adductor muscle scar in the Silurian bivalve Nuculodonta got-
landica (SGU Type 1030) from the Halla Formation of Gotland (Modified from Liljedahl
(1994).); (e) Interior of right valve of Venericor clarendonensis (NHMUK PI TB 14236)
from the Eocene (subdivision B2 of the London Clay) with irregular shell deformations
and shell pits interpreted to have been produced in response to digenean trematode
infestation. Photo courtesy of Jon Todd; compare Todd and Harper (2011).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 103
placement of fossil taxa (Dyke and Van Tuinen, 2004; Thomas et al., 2004;
Mayr, 2011) and/or other methodological artefacts (cf. Ksepka et al., 2014).
The appearance of shorebirds in the Cretaceous or Early Paleogene suggests
that the Paleozoic structures were probably caused by a different group of
parasites or even epizoa (Liljedahl, 1985, 1994) with similar behaviour,
although we cannot rule out the possibility that gymnophallids, or closely
related (now potentially extinct) taxa or their ancestors, had different life cy-
cles and host associations in the past. Shell pits have so far been traced back
only to the Eocene (Ruiz and Lindberg, 1989; Todd and Harper, 2011;
Huntley and De Baets, 2015), which is more or less consistent with the pres-
ence of gymnophallideshorebird associations (Figure 2).
Age: The Silurian occurrence of an igloo-shaped concretion was found
in the silicified M€ollboss 1 fauna from the Halla Formation (previously Halla
Beds) of Gotland (Liljedahl, 1985, 1994). Jeppsson et al. (2006) correlated
M€ ollboss 1 with the parvus graptolite biozone and the Ozarkodina bohemica
longa conodont subzone 2 as defined by Calner and Jeppsson (2003). The
top of the Pristiograptus dubius parvus e Gothographus nassa graptolite biozone
has been dated to 428.18 0.4796 Myr, yielded an minimum age of
427.7 Ma (Melchin et al., 2012). This is consistent with UePb age of
428.45 0.35 Myr obtained by Cramer et al. (2012) for the Gr€ otlingbo
bentonite at the nearby locality H€ orsne 3, which has been correlated with
M€ ollboss 1 (Jeppsson et al., 2006) and probably accounts for some of the sil-
ification of the strata there (Mikael Calner, personal communication 2014).
(a) (b)
(c) (d)
Figure 3 Fossil evidence for the presence of derived parasitic flatworms (Cestoda) in
the Middle Permian (Modified from Dentzien-Dias et al. (2013).): (a) Picture of the spiral
heteropolar coprolite from the Rio do Rasto Formation, which has yielded the cestode
eggs, before destructive thin section analysis; (b) Thin section of the coprolite part con-
taining parasite eggs clustered in; (c) Cestode egg with a developing embryophore.
(d) Partial reconstruction of egg in (c) with interpretations of the observed structures.
Abbreviations: C ¼ capsule or shell; E ¼ embryophore (ochosphere); H ¼ putative
developing hooklets; I ¼ inner envelope; M ¼ oncospheral membrane; O ¼ outer
envelope; P ¼ putative polar thickening; Op ¼ operculum; S ¼ somatic cells.
of these eggs (operculum, egg shape and size: Figure 3(c) and (d)) as well as
their deposition together in an elongate arrangement (Figure 3(b)), which is
typical of modern tapeworm eggs deposited in mature segments or proglot-
tids, corroborates their cestode affinity.
Age: The coprolite derives from the upper member of the Rio do Rasto
Formation, which has also yielded a variety of vertebrate faunas (Dentzien-
Dias et al., 2012). The locality is located near Posto Queimado, where verte-
brate faunas indicate a Guadalupian (Late WordianeCapitanian) age (Cisneros
et al., 2012; Dias-Da-Silva, 2012). The coprolite should therefore be older
than the Guadalupian (Capitanian)eLopingian (Wuchiapingian) boundary
dated to at least 259.4 Ma (259.8 0.4 Myr: Henderson et al., 2012).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 105
Older reports of potential cestode eggs (Zangerl and Case, 1976; Combes,
2001) within a Carboniferous coprolite are still controversial (Boucot, 1990;
Poinar, 2003; Dentzien-Dias et al., 2013). Strictly speaking, this coprolite
should be called a cololite as the fossilized faecal remains were found lodged
within its producer (Hunt et al., 2012). Boucot (1990) considered the report
as fairly speculative as the urea-rich environment of the dead shark would
probably lead to the rapid decomposition of such eggs, but the latest discovery
of cestode eggs in a Permian shark coprolite (Dentzien-Dias et al., 2013) illus-
trate that their interpretation as helminth eggs cannot be excluded. However,
further analyses of the morphology and the arrangement of these spherical
bodies are necessary to confirm their assignment to cestodes (Zangerl and
Case, 1976; Combes, 2001) or other parasitic helminths.
Age: The Cobelodus aculeatus specimen with the putative cestode eggs
derives from the Stark Shale, the core black shale member of the Dennis
Formation of the Missouri Series, near Fort Calhoun, Nebraska. It was
assigned to the Westphalian D by Zangerl and Case (1976) without any in-
formation corroborating this assignment. The Missouri series form part of
the local Missourian stage, which largely corresponds with the Kasimovian
(Falcon-Lang et al., 2011), which also includes the Stark Shale (Rosscoe,
2008; Rosscoe and Barrick, 2013). An age older than the Kasimoviane
Gzhelian boundary (303.6 Ma according to the 2012 Geological Timescale:
Davydov et al., 2012) can therefore be used as minimum constraint.
Pending reinvestigation of this fossil, it could extend range of cestode
eggs in shark coprolites by an additional 40 Myr.
Eocene Baltic amber (Poinar, 2003) and calcareous nodules of Miocene age
(Pierce, 1960; Poinar, 2003), and those of flatworm egg capsules from Qua-
ternary lake sediments (Frey, 1964; Harmsworth, 1968; Gray, 1988). These
fossils considerably post-dated divergence time estimates for free-living flat-
worms derived from molecular clock studies. Older molecular clock studies
place the origin of (free-living) Platyhelminthes deep in the Precambrian
(Hausdorf, 2000; Otsuka and Sugaya, 2003), but more recent relaxed molec-
ular clock studies place their origins between the latest Precambrian (Edia-
caran) and the early Cambrian (Douzery et al., 2004; Peterson et al., 2004,
2008; Erwin et al., 2011). Some Ediacaran fossils have occasionally been
related to free-living flatworms (Allison, 1975; Palij et al., 1979; Fedonkin,
1985), although they cannot be confidently assigned to the phylum (Conway
Morris, 1981; Labandeira, 2002; Erwin et al., 2011). Even Dickinsonia was
assigned to flatworms at one point (Palij et al., 1979; Conway Morris,
1981). The taxonomic position of Dickinsonia has been heavily debated
(Retallack, 2007; Brasier and Antcliffe, 2008) and this taxon is often inter-
preted as one of the earliest divergent metazoans (Xingliang and Reitner,
2006; Sperling and Vinther, 2010). Various Permian to Triassic trace fossils
have also been attributed to turbellarians including Polycladida and Tricladida
(Alessandrello et al., 1988; Knaust, 2010). The assignment of trace fossils to
this phylum is also problematic as various worm-like groups with similar ecol-
ogy and mode of locomotion could also have produced these traces (Sei-
lacher, 2007). Curvolithus has also been attributed to flatworms (Seilacher,
2007), but could also have been produced by other taxa with similar behav-
iour (Buatois et al., 1998). Further studies of traces produced by extant forms
as well as fossil traces associated with body fossils are therefore important to
confidently assign them to the phylum (Collins et al., 2000; Knaust, 2010).
The oldest parasitic flatworm fossils are therefore not only important for
putting constraints on free-living flatworms, but also on the presence of
Platyzoa in the fossil record, a group currently containing both parasites
(Platyhelminthes, Acanthocephala) and free-living taxa (Wey-Fabrizius
et al., 2013). The assignment of Cambrian fossils (cambroclaves) to the Acan-
thocephala as suggested by some authors (Qian and Yin, 1984), which has also
been followed in some recent classifications (Amin, 2013), is highly question-
able and widely rejected (Conway Morris et al., 1997; Elicki and Wotte,
2003; Kouchinsky et al., 2012). These problematic Cambrian organisms
can be classified as Lophotrochozoa at best (Kouchinsky et al., 2012);
Compare Conway Morris and Crompton (1982) and Near (2002) for further
speculations and hypotheses on the origin and evolution of parasitism towards
110 Kenneth De Baets et al.
Figure 4 Fossil finds of putative flatworm fossils discussed in the text mapped on their
host phylogeny, which was modified from Donoghue and Smith (2003) and Rowe
(2004) taking into account new phylogenetic hypotheses summarized in Donoghue
and Keating (2014).
Figure 5 Comparisons of the consistency between extant and fossil host ranges of
parasitic flatworms and pentastomids. Host phylogeny was modified from
Goudemand et al. (2011). Note that the host gap would be considerably greater if
the position of conodonts would be more basal as postulated by some authors (Blieck
et al., 2010; Turner et al., 2010). Recent discoveries of Silurian pentastomids associated
with ostracods even further extend the host gap between fossil and extant pentasto-
mids (Siveter et al., 2015).
112 Kenneth De Baets et al.
exact host of these marine forms is still unknown as they were not found
directly associated with their hosts. Some have suggested their hosts might
have been conodonts (Walossek and M€ uller, 1994), of which tooth-like
remains have been commonly found in these deposits. Interestingly, the
CambrianeOrdovician fossil pentastomids resemble larvae of modern forms
that can infest fish, making it conceivable that these small pentastomids
represent adults that spent their entire life cycle on small fish-like vertebrates
(Sanders and Lee, 2010). The range of the host gap between Cambrian and
extant pentastomids (Figure 5) might therefore depend on the systematic
position of conodonts, which is still debated. Most authors agree that con-
odonts are chordates, probably either stem- or crown-vertebrates (Blieck
et al., 2010; Turner et al., 2010; Goudemand et al., 2011; Murdock et al.,
2013; Donoghue and Keating, 2014). Interestingly, putative pentastomid
remains were recently also reported from ostracods within the Silurian
Herefordshire Lagerst€atte (Siveter et al., 2015), which further increases the
host gap between extant and fossil pentastomids. This might suggest that in-
vertebrates might have been the initial hosts in the marine realm, if ostracods
are the final hosts as suggested by these authors and if no host switching
occurred between the Cambrian and the Silurian. However, pentasto-
midehost associations from the Cambrian and Ordovician lagerst€atten
would be necessary to further test this hypothesis.
Thus, it is not always possible to precisely constrain parasiteehost asso-
ciations in the fossil record. This is not only the case for isolated remains
of parasites not directly attached to their hosts (Castellani et al., 2011), but
also for parasite remains found in isolated coprolites not confidently assign-
able to precise host taxa (Jouy-Avantin et al., 1999; Poinar and Boucot,
2006; Dentzien-Dias et al., 2013).
Fossils of potential hosts might be common or present in the same layers,
although without direct evidence for a parasitic relationship (attached or
found within well-preserved body fossils of their hosts), appointing a poten-
tial host remains within the realm of speculation. In the case of intermediate
hosts, where the fossil evidence is often pathologies or traces, it is hard to be
certain of the identity of the culprits since various organisms with similar
behaviour can produce similar traces. Furthermore, it might also be hard
to identify the final host without finding remains of the putative parasite
associated with them. Predatoreprey relationships might provide a clue
(Ruiz and Lindberg, 1989; De Baets et al., 2011), but direct evidence for
predation from one taxon on another is rare in the fossil record too (Brett
and Walker, 2002; Walker and Brett, 2002). Nevertheless, age in itself might
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 113
be sufficient to rule out certain hosts if they had not yet evolved, they must
have had different intermediate and/or final hosts at that time. Although the
hosts of CambrianeOrdovician pentastomids remain speculative, hosts
assignable to taxa they currently parasitize were not around yet, so they
must have had additional parasiteehost associations in the past which are
now extinct.
fossil calibrations are well justified if the following criteria are fulfilled:
(1) listing of museum numbers of specimen(s) that demonstrate all the rele-
vant characters and provenance data, (2) availability of apomorphy-based
diagnoses of the specimen(s) or an explicit, up-to-data, phylogenetic analysis
that includes the specimen(s), (3) explicit statements on the reconciliation of
morphological and molecular data sets, (4) specification of the locality and
stratigraphic level (to the best current knowledge) from which the calibrat-
ing fossils are derived, (5) reference to a published radioisotopic age and/or
numeric timescale with details on its selection. Divergence time estimation is
not possible with minimum constraints alone, as the substitution rate is var-
iable and unknown; therefore, at least one point calibration or maximum
constraint is required to calculate the substitution rate and absolute diver-
gence times (Warnock et al., 2012).
It would therefore be more appropriate to use the oldest estimate (95%
confidence maximum) for the origin of the total group from a robust
molecular clock analysis as the maximum, and the oldest fossil assignable
with confidence to the crown group (as the minimum), to constrain the
evolutionary history of the host (and the parasite). For example, if the origin
of parasitic flatworms occurred during the early evolution of gnathostomes
as suggested by Littlewood (2006), this would mean they originated bet-
ween the Cambrian (643 Ma: oldest confidence intervals of Erwin et al.,
2011 for this node) and the earliest well-dated fossils that can be confidently
assigned to crown-group gnathostomes deriving from Ordovician
(w421.8 Ma: Benton et al., 2009; Donoghue and Keating, 2014). Alterna-
tively, the entire 95% confidence posterior interval (from robust molecular
clock studies) for diverging host clades could be used as priors on the clade
ages in the parasites.
A more conservative and less circular approach would be to use the lat-
est robust relaxed molecular clock estimates for the origin of their free-
living ancestors (744 Ma: oldest confidence of Erwin et al., 2011 for this
node) and the earliest certain appearance of parasitic flatworms in the fossil
record, which would be only Permian (>259.4 Ma as discussed above).
This would yield quite large confidence intervals (cf. Warnock et al.,
2012 for Parasitiformes), but such estimates would be more honest and
accurate (closer to reality) than seemingly precise estimates which are argu-
ably inaccurate, since the origin of parasitism falls outside the calibration
interval a priori (Warnock et al., 2011). Furthermore, reinvestigation of
putative flatworm trace or body fossils from Upper Silurian (>427.7 Ma)
or Middle Devonian (>381.9 Ma) deposits might further narrow this
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 115
time interval in the future. The fossil record also provides constraints on the
origin of Cestoda in shark hosts (Dentzien-Dias et al., 2013) and Trema-
toda in archosaur hosts (Poinar and Boucot, 2006). Furthermore, the fossil
record provides upper constraints on the origin of Gymnophallidae in the
form of characteristic pathologies, dicrocoelid flatworms derived from eggs
in coprolites as well as several genera and even species from archeological
sites (e.g. Dicrocoelium, Diphyllobothrium, Fasciola, Monoecocestus, Schistosoma,
Taenia).
The oldest fossil evidence for schistosomes are antigens deriving from a
3200 BC Egyptian mummy, but the origin of this group is believed to be
considerably older based on the evolutionary history of their intermediate
or final hosts (Lawton et al., 2011). Davis (1993) suggested that the genus
Schistosoma arose before the breakup of the supercontinent Gondwana
over 150 Ma based on the distribution of their snail hosts and that ancestors
of Asian schistosomes were carried to Asia via India after it separated from
Africa. More recent studies (Snyder and Loker, 2000) have suggested a
younger, ancestral Asian origin somewhere in the Miocene, which might
indicate that schistosomes only colonized Africa around 15e20 Ma (Lawton
et al., 2011). Performing a robust molecular clock analysis using dates of fos-
sil Schistosoma and their hosts might be a more formal way to test these
hypotheses. In some cases, additional historical dates might become avail-
able to constrain certain nodes such as the possible slave transport of Schis-
tosoma mansoni to South America (Lockyer et al., 2003b), which is so far not
contradicted by finds of older remains of S. mansoni in archeological sites of
South America (Gonçalves et al., 2003). Direct dating of samples yielding
ancient DNA (Wood et al., 2013) might also provide additional constraints
in such studies. However, a recent study by Mello et al. (2014) has demon-
strated that the assignment of calibration information to deeper phyloge-
netic nodes is more effective in obtaining more precise and accurate
divergence time estimates compared to analyses involving calibration at the
shallowest node.
Most authors agree that multiple, well-justified calibrations are the best
approach to obtain the most robust and accurate molecular clock estimates
(Warnock et al., 2011; Parham et al., 2012). Note that careful a priori selec-
tion of suitable calibration points cannot be replaced by using as a posteriori
cross-validation procedures (Near et al., 2005; And ujar et al., 2014) as these
only verify consistency (Clarke et al., 2011). In some cases, multiple inaccu-
rate calibrations might be consistent, which can result in erroneous rejection
of more reasonable calibrations. Furthermore, consistent calibrations may be
116 Kenneth De Baets et al.
redundant by definition, since they fail to correct for changes in rate varia-
tion (Clarke et al., 2011; Warnock et al., 2015). Furthermore, calibration
should be implemented in the most conservative way, which might result
in less precise, but ultimately more accurate divergence estimates (Warnock
et al., 2012).
In the absence of a suitable fossil record, one could resort to the use of
biogeographic events or calibrations related only to the host fossil record.
Nevertheless, both methods also have their problems and add an additional
component of circularity to calibration procedures depending on the
hypotheses being tested (Hipsley and M€ uller, 2014). Biogeographic calibra-
tions as they are currently implemented are problematic (Goswami and
Upchurch, 2010; Kodandaramaiah, 2011; De Baets and Donoghue, 2012;
Hipsley and M€ uller, 2014), and they should be implemented more con-
servatively. It should be established when a certain barrier, causal to a given
speciation event, actually occurred (De Baets and Donoghue, 2012;
Warnock, 2014).
Most importantly, there remains an assumption that biogeographic distri-
butions have not changed significantly in geological time, making it harder to
establish whether biogeographic barriers were coincident with speciation
events, and introduce an aspects of circularity (Crisp et al., 2011). Having
taxon-area relationships consistent or inconsistent with biogeographic
events, does not necessarily mean that these clades diversified at the same
time as these events, because older events might have led to similar distribu-
tions (pseudo-congruence) or younger events might have altered their dis-
tributions (pseudo-incongruence; see Donoghue and Moore, 2003). Even
for some of the classical examples of groups with current distributions
congruent with vicariance, such as onychophorans and cichlids, studies
have demonstrated that divergence might predate (Murienne et al., 2014)
or postdate (Friedman et al., 2013) the continental break-up of superconti-
nents, respectively.
Using the fossil record of hosts also introduces an aspect of circularity in
addition to other considerations related with fossil calibrations (Donoghue
and Benton, 2007; Parham et al., 2012) as discussed above. It assumes that
the current parasiteehost associations did not markedly change through
geological time, which is not necessarily true, particularly in groups which
are estimated to range several hundred million years into the past (e.g. the
pentastomid example we discussed above). Using hosts also leads to circular
reasoning when employing them to investigate hypotheses of parasiteehost
coevolution. In highly host-specific lineages with simple life cycles like the
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 117
Polystomatidae (Figure 6), it might work well, but for groups with common
host switches and/or complex life cycles this approach might be less suitable.
The most conservative way to implement them would be to use the oldest
reliable estimate for the origin of this group as a maximum and the oldest
from well-attributable fossil to this lineage as a minimum. Polystomatid flat-
worms are one of the most host-specific groups of parasitic flatworms and
their direct life cycle that involves a short free-living aquatic larval stage
(which means they are probably only passively disseminated by their hosts),
have made them an ideal model to test the use of constraints from biogeog-
raphy and the host fossil record (Bentz et al., 2001, 2006; Verneau et al.,
2002, 2009a,b; Badets et al., 2011). Verneau et al. (2002) used 425 Ma to
calibrate the split between Actinopterygii and Sarcopterygii (Figure 6),
although this event must have happened at the latest by about 419 Ma
(Zhu et al., 2009). However, it would be more conservative to use the oldest
robust estimate from relaxed molecular clock studies for the separation of
actinopterygian from sarcopterygians and the earliest fossil confidently
assigned to either tetrapods or lungfishes to constrain this node (Badets
et al., 2011). The oldest stem-group lungfish is generally considered to be
Diabolepis (Friedman, 2007; Qiao and Zhu, 2009), while one of the oldest
ingroup lungfishes might be Westollrhynchus (Qiao and Zhu, 2009). Badets
et al. (2011) also suggested that some dates might be consistent with the
break-up of the supercontinent Gondwana, although this needs to be
further tested with additional sampling.
Taxon sampling can play a large role in tree reconstruction and interpre-
tation with respect to biogeography (Trewick and Gibb, 2010) or host
switching (Hafner and Page, 1995). In the case of lineages or parasitee
host associations, which have been around for many hundreds of millions
of years, host range changes and extinction might contribute significantly
to missing taxa, making it hard to infer past biogeographical distribution
or parasiteehost associations, from extant data alone. There is at least
some evidence that extinction might also have played a role in parasitic flat-
worms and other helminths over longer timescales as several parasiteehost
associations documented in the (sub)fossil record are now evidently extinct
(Upeniece, 2001, 2011; Poinar and Boucot, 2006; Wood et al., 2013).
Furthermore, molecular studies with greater taxonomic coverage have
particularly focused on biomedically or economically important taxa such
as Schistosomatidae (Lockyer et al., 2003b; Orélis-Ribeiro et al., 2014) or
particular lineages with a high host specificity such as Polystomatidae (Bentz
et al., 2001, 2006; Badets et al., 2011, 2013; Héritier et al., 2015). To better
118 Kenneth De Baets et al.
=
hypothesized ages of dispersal routes between Eurasia and Africa (Rage, 1988; Bentz
et al., 2001). Finally, the root prior was set at 160 Ma (sd 5 Myr), corresponding to an
initial divergence separating Asian and Australian polystomes from all other neobatra-
chian polystomes (Badets et al., 2011), hypothetically corresponding to a separation of
the western and eastern components of Gondwanaland. Divergence time estimates
(see Verneau et al., 2009b) are reported for two nodes that are relevant for understand-
ing the origin of the new Malagasy genus, i.e. Madapolystoma (see Du Preez et al.,
2010). According to Verneau et al. (2009b), Madapolystoma would have diverged
from Eupolystoma about 116 Ma (node A) and the first crown divergence in Madapo-
lystoma (node B) would have occurred about 63 Ma.
120 Kenneth De Baets et al.
Fossil evidence can only provide minimum time constraints and is not avail-
able for all lineages of parasitic flatworms. Interpolations based on parasiteehost
associations or biogeographic events can potentially be used to supplement fos-
sil constraints. However, circularity in testing hypotheses should be avoided
and caution should be taken when multiple host-switching events are sus-
pected. Before using such calibrations it should be at least verified if this hypoth-
esis is robust to a wider sampling of extant and extinct taxa as well as the
evolutionary history of their hosts, where the sampling and fossil record might
be comparatively better. We therefore advise implementing such calibrations in
the most conservative way. For calibrations based on the evolutionary history of
parasites or their hosts, this would correspond with using the oldest estimate
based on relaxed molecular clock estimates as maximum and the oldest well-
attributable fossils of the parasite or its host as a minimum; for calibrations based
on biogeographic events, this would correspond to the using the oldest age of
the oldest geological event that could have influenced the distribution of the
parasites and their hosts as a maximum and the youngest age of the geological
events that could have influenced their distribution as a minimum.
Several recent discoveries indicate that exceptionally preserved gnathos-
tomes or their coprolites might yield additional finds of parasitic flatworm
fossils, particularly their attachment organs or their eggs (Littlewood and
Donovan, 2003; Poinar and Boucot, 2006; Dentzien-Dias et al., 2013),
which can be characteristic for certain lineages. Novel methods like exper-
imental decay studies or computer tomography might provide additional
insights into the phylogeny, 3D-morphology and ecology of such fossils.
The future of constraining the evolutionary history of Platyzoa and parasitic
flatworms lies in molecular clock methodology by combining information
from the geological record (particularly body fossils or eggs) and molecular
sequences with the fewest assumptions. Characteristic pathologies might also
put constraints on the evolutionary history of parasitic flatworm, although
this still needs to be further studied in extant and fossil hosts to establish a
robust relationship with a particular lineage of parasites (Campbell, 1985;
Ituarte et al., 2001, 2005).
ACKNOWLEDGEMENTS
Michael Calner (Lund University), Ervıns Luksevics (University of Latvia, Riga), Steve Ross-
coe (Hardin-Simmons University), Pascal Godefroit (Royal Belgian Institute of Natural Sci-
ences, Brussels) and Jon Todd (Natural History Museum, London) are thanked for pointing
us to literature with the latest stratigraphic assignment of the Silurian, Upper Devonian,
Carboniferous, Cretaceous and Eocene flatworm fossils, respectively. Jon Todd (Natural
122 Kenneth De Baets et al.
History Museum, London) and Cristian Ituarte (Museo Argentino de Ciencias Naturales,
Buenos Aires) kindly put pictures of bivalve pathologies linked to trematode parasites at
our disposal. This research was partially funded by an SNF grant (2012e141438) to Kenneth
De Baets. Rodney Bray (Natural History Museum, London, retired), John Huntley (Univer-
sity of Missouri, Columbia), Tim Littlewood (Natural History Museum, London) and Rachel
Warnock (Smithsonian National Museum of Natural History, Washington) kindly read and
commented on previous versions of this manuscript.
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CHAPTER FOUR
Contents
1. Introduction 139
1.1 Insects as parasites and hosts 139
1.2 Insects in the fossil record 140
2. Insect Parasitism sensu stricto (s. str.) e Paraneoptera 142
2.1 Phthiraptera 142
2.1.1 General aspects 142
2.1.2 Phylogenetic inference of appearance and molecular estimations of early 143
evolution
2.1.3 Fossil representatives 145
2.2 Hemiptera 146
2.2.1 General aspects 146
2.2.2 Phylogenetic inference of appearance and molecular estimations of early 146
evolution
2.2.3 Fossil representatives 146
3. Insect Parasitism s.str. e Antliophora 147
3.1 Siphonaptera 148
3.1.1 General aspects 148
3.1.2 Phylogenetic inference of appearance and molecular estimations of early 148
evolution
3.1.3 Fossil representatives 149
3.2 Diptera 152
3.2.1 General aspects 152
3.2.2 Phylogenetic inference of appearance and molecular estimations of early 153
evolution
3.2.3 Fossil representatives 154
4. Insect Parasitism s.str. e Neuropteroida 159
4.1 Neuroptera (Mantispidae) 159
4.1.1 General aspects 159
4.1.2 Phylogenetic inference of appearance and molecular estimations of early 160
evolution
4.1.3 Fossil representatives 160
Abstract
Within Metazoa, it has been proposed that as many as two-thirds of all species are para-
sitic. This propensity towards parasitism is also reflected within insects, where several
lineages independently evolved a parasitic lifestyle. Parasitic behaviour ranges from
parasitic habits in the strict sense, but also includes parasitoid, phoretic or kleptopara-
sitic behaviour. Numerous insects are also the host for other parasitic insects or meta-
zoans. Insects can also serve as vectors for numerous metazoan, protistan, bacterial and
viral diseases. The fossil record can report this behaviour with direct (parasite associated
with its host) or indirect evidence (insect with parasitic larva, isolated parasitic insect,
pathological changes of host). The high abundance of parasitism in the fossil record
of insects can reveal important aspects of parasitic lifestyles in various evolutionary lin-
eages. For a comprehensive view on fossil parasitic insects, we discuss here different
aspects, including phylogenetic systematics, functional morphology and a direct com-
parison of fossil and extant species.
1. INTRODUCTION
1.1 Insects as parasites and hosts
Insecta is often considered to be the largest animal group comprising
over half of all metazoan species (Mayhew, 2007). Also, it has been estimated
that only about 20% of all existing insect species have been described so far
(Grimaldi and Engel, 2005). Considering that over 60% of all insect species
have been proposed to be parasites (Price 1980), we could estimate that
there should be at least 600,000 parasitic insect species in the modern fauna
(although one could ask how reliable these estimations are).
Ectoparasitism has been suggested to have evolved not less than 30 times
in different insect groups (Grimaldi and Engel, 2005). Ectoparasitism and
especially haematophagy occurs, for example, in fleas (Siphonaptera), lice
(Phthiraptera), midges (Diptera), some beetles (Coleoptera) and bugs (Hem-
iptera) (Pe~
nalver and Pérez-de la Fuente 2014, Lukashevich and Mostovki,
2003). Other insects, such as mantid lacewings (Mantispidae) and blister bee-
tles (Meloidae) are endoparasites or kleptoparasites.
While parasites (in the strict sense) do not kill their host, parasitoids do
(Kathirithamby, 2009). Parasitoidism is an important feeding strategy for
different wasps and relatives (Hymenoptera), at least in their larval stages,
140 Christina Nagler and Joachim T. Haug
but also for twisted-wing ‘parasites’ (Strepsiptera) and occasionally also for
other insects. In contrast to most parasites, the size relation of host and para-
sitoid is oddly skewed. While parasites are usually significantly smaller than
their hosts, parasitoids reach about the same size as their host. Often we
also see parasitoids that have parasitoids as host, a phenomenon known as
hyperparasitoidism (Kathirithamby, 2009). Besides parasitoidism, another
important parasitic mode (in the widest sense) is plant parasitism, which
occurs in several insect groups, e.g., hemipterans, coleopterans, dipterans
or hymenopterans.
Finally, insects do not only act as parasites themselves, but many serve as
hosts also for other insects, nematode and nematomorph worms and mites.
They also are hosts to a plethora of bacteria, viruses and protists. Many
notable pathogens, including Trypanosoma, Plasmodium and Dengue virus
use insects as vectors, to become widely distributed (e.g. Poinar, 2014a).
2.1 Phthiraptera
2.1.1 General aspects
The group Phthiraptera, or true lice, currently comprises 4900 extant species.
They are traditionally split into two subgroups, ‘Mallophaga’, the chewing
lice, and Anoplura, the sucking lice (Grimaldi and Engel, 2005). The chewing
lice are named for their chewing mouthparts and include Amblycera, Ischno-
cera and Rhynchophthirina (Johnson and Clayton, 2003).
All phthirapterans are obligate ectoparasites of birds or mammals. They
are extremely modified for their parasitic lifestyle and behaviourally adapted
for particular microhabitats on the hosts (Johnson and Clayton, 2003). All
stages (including the adults) are wingless and dorsoventrally flattened.
They posses claws for clinging to hair or feathers and have modified
mouthparts for feeding (Light et al., 2010). The true lice are highly host-
and site-specific and spend their entire life on the host (as the only group
of ectoparasitic arthropods except mites). The females lay large eggs and atta-
ch them to the hair or feathers of their host with a special secretion (Martill
and Davis, 1998). Due to the dependence of their life cycle to the host and
their host specificity, Phthiraptera is a candidate for being the most special-
ized group of parasites among insects. They are a model system for phyloge-
netic studies including co-speciation and coevolution (Wappler et al., 2004;
Johnson and Clayton, 2003).
Insects as Parasites and Hosts 143
congruent with the fossil record. Yet, also even earlier origins have been
suggested (e.g. Martill and Davis, 1998).
Molecular data support an evolutionary scenario from free-living detri-
tivorous generalistic psocodeans over liposcelid-like forms to highly special-
ized obligate ectoparasitic phthirapterans (Yoshizawa and Johnson, 2003).
Representatives of Liposcelidae have been found in nests of birds, mammals
or in the plumage of birds and fur of mammals, feeding on faeces, shed fur
and feathers (Grimaldi and Engel, 2006). This association may have given
the input to a permanent parasitism in lice (Yoshizawa and Lienhard, 2010).
Based on molecular data, Anoplura supposedly appeared in the Late
Cretaceous (77 ma) and soon after the CretaceousePalaeogene boundary
(before 65 ma), they radiated and adapted to different mammalian in-groups
(Smith et al., 2011; Light et al., 2010).
2.2 Hemiptera
2.2.1 General aspects
Hemiptera includes Fulgoromorpha, Cicadomorpha (together forming
Auchenorrhyncha), Coleorrhyncha, Sternorrhyncha (all four groups
together formerly referred to as ‘Homoptera’) and Heteroptera (Beutel
et al., 2014). A prominent haematophagous group within Hemiptera is
Reduviidae; some species are commonly known as kissing bugs (Grimaldi
and Engel, 2005). Two other groups, Cimicidae and Polyctenidae, contain
also several haematophagous species (Yao et al., 2014). The exact relation-
ship of the hemipteran subgroups is still under discussion (Beutel et al., 2014;
Li et al., 2012).
(Poinar, 2012b). Certain scorpionflies from the Early Cretaceous (100 ma)
have long pointed mouthparts with fine serrations, this indicates that these
early mecopterans fed on blood (Boucot and Poinar, 2010).
Some fossils of the Late Jurassic (150e140 ma) indicate a Mesozoic age
for the sister group to the fleas (Grimaldi and Engel, 2005) and that this
type of fossil scorpionflies may have led to Siphonaptera (Huang et al.,
2012; Poinar, 2012b). It has also been suggested that Siphonaptera is either
an in-group (Friedrich and Beutel 2010) or the sister group (Whiting et al.,
2008) to the mecopteran in-group Boreidae. Despite the fact the exact
origin and relationships of fleas and other scorpionflies remains partly un-
clear, we can still state that with the radiation of mammals in the Palaeocene
and the obligate ectoparasitism of fleas, Siphonaptera radiated far more
recently than other mecopteran groups (Grimaldi and Engel, 2005).
3.1 Siphonaptera
3.1.1 General aspects
Siphonaptera, the true fleas, are laterally compressed, wingless obligate ecto-
parasites. They feed exclusively on the blood of mammals (94%) and birds
(6%) (Poinar, 2012b). About 2500 living species are known and they are
evolutionarily successful as they are a long-lived lineage that has radiated suc-
cessfully across multiple hosts (Poulin and Morand, 2000). Like many other
insect parasites, fleas have reduced eyes, reduced antennae, no wings, large
claws and modified mouthparts to pierce the skin of the host and suck blood
(Lukashevich and Mostovki, 2003; Rasnitsyn and Quicke, 2002). Interest-
ingly all insect ectoparasites have a dorsoventrally flattened body, except
fleas, where it is laterally compressed. In contrast to lice, fleas do not generally
spend their whole life on the host. Larvae often live in or near the nest of the
host and feed on host faeces, exfoliated skin; others are predators or even can-
nibals (Grimaldi and Engel, 2005; Rasnitsyn and Quicke, 2002).
• Mesozoic giant fleas: two species (Figure 2(d)) from the Middle Jurassic
(165 ma) and one species from the Early Cretaceous (125 ma) in China.
These specimens share morphological characters with extant fleas, but
retain plesiomorphic features like nonjumping hind legs. Also they
have similar mouthparts in siphonate mecopterids. These giant fleas
might document an early diversification towards haematophagy (Huang
et al., 2012), assuming this is not a plesiomorphic feature. All three spe-
cies were ascribed subsequently to Pseudopulicidae (see below; Huang
et al., 2013)
• Pseudopulex jurassicus from the Middle Jurassic and Pseudopulex magnus from
the Early Cretaceous (Gao et al., 2012). These specimens share some
morphological characters with extant fleas, but could represent an extinct
lineage in early flea evolution (Gao et al., 2012). The morphological data
indicate that Pseudopulicidae (including these two) represent an early
offshoot of the siphonapteran lineage (Gao et al., 2012). Subsequently
Gao et al. (2013a) suggested Tarwinia þ Pseudopulicidae as sister group
to Saurophthirus þ the modern fleas based on morphological characters.
• Saurophthiridae. With Saurophthirus exquisitus from the Lower Creta-
ceous Yixian Formation in China et al. (Gao et al., 2013a). This species
has short and slender piercingesucking stylet mouthparts. Hence Sau-
rophthiridae (including another species S. longipes see above) resembles
the true fleas more than any other Mesozoic flea or flea-like fossil.
This indicates a divergence of Saurophthiridae and true fleas in the
Late Jurassic (Gao et al., 2013a). However, Grimaldi and Engel (2005)
saw no features that indicate special relationships to true fleas, but may
be because at the point of their review the only known Saurophthirus
was S. longipes, where the mouthparts were not preserved.
All flea-like Mesozoic fossils are definitely not true fleas in the strict sense
(Poinar, 2012b), but are more likely early offshoots of the evolutionary line-
age towards them (some may also represent other groups, see above). One
could simply consider modern fleas (including most amber fossils) as Siphon-
aptera sensu stricto, while using Siphonaptera sensu lato for the Mesozoic flea-
like fossils plus Siphonaptera s.str., instead of discussing at which point the
term ‘flea’ should be applied. Hence, we can state that early representatives
of Siphonaptera sensu lato (before the node of Siphonapetra sensu stricto) were
likely parasitizing feathered dinosaurs, pterosaurs or early mammals as ecto-
parasites grasping with their long legs (Gao et al., 2013a; Rasnitsyn, 1992;
Ponomarenko, 1976; Jell and Duncan, 1986). Their habitus indicates a strict
ectoparasitic lifestyle, adapted more for attachment than jumping (as in
152 Christina Nagler and Joachim T. Haug
3.2 Diptera
3.2.1 General aspects
The superdiverse insect group Diptera is cosmopolitan and with 154,000
described species represents 10e12% of all described animal species
(Lambkin et al., 2013). Dipterans are easily recognizable as their hind wings
are reduced to halteres.
The ancestral feeding mode for Diptera is blood-sucking. Females of
groups which retain this mode have mandibles, which function as lancets
(Grimaldi and Engel, 2005). Haematophagy is obligate for females (of
blood-sucking species) to complete each gonadotrophic cycle and produce
fertile eggs (Greenwalt et al., 2013). Early divergent representatives of
Diptera, like midges and craneflies, resemble mecopterans in basic
morphology, with their long wings and long, dangling legs. Haematophagous
groups within the Diptera are numerous: Phlebotominae, Sycorinae, Culici-
dae, Corethrellidae, Ceratopogonidae, Simuliidae, Rhagionidae, Tabanidae,
Carnidae, Muscidae and Glossinidae (Grimaldi and Engel, 2005).
Extant adults of Chironomidae feed on nectar and honeydew, but early
representatives of Chironomidae from the Triassic and Jurassic were still
haematophagous. Such forms had biting mandibles, like Aenne triassica
from the Late Triassic of England (210 ma; Azar and Nel, 2012).
Extant representatives of Culicidae are blood suckers of almost all verte-
brates. Hence, likely fossil hosts could have been early mammals, lizards,
snakes, turtles, crocodilians, but also nonavian dinosaurs (Poinar et al., 2000).
Species of Corethrellidae are known as frog-biting midges. These tiny
midges are host-specific and parasitize frogs. 105 extant and 7 fossil species
are known (Borkent, 2014). Female frog-biting midges find their hosts
by listening to the mating calls of the host frogs (De Silva and Bernal, 2013).
Representatives of Ceratopogonidae or biting midges are small, but have
well-developed wings. Representatives of older lineages feed on vertebrates,
while more derived species feed on insects as ectoparasites (Borkent et al.,
2013; Pérez-de la Fuente et al., 2011). Ceratopogonidae is very species
rich, with 6180 extant species (Borkent, 2014; Greenwalt et al., 2013).
Insects as Parasites and Hosts 153
Simuliidae or blackflies are a group with 2100 extant species (Craig et al.,
2012). The claws of fossil forms indicate that early representatives of
Simuliidae fed on feathered nonavian dinosaurs or early birds (Currie and
Grimaldi, 2000).
Psychodidae with about 3000 extant species has received special scienti-
fic attention due to their medical significance. Within Psychodidae,
representatives of Sycorinae and Phlebotominae are parasitic blood feeders
(Grimaldi and Engel, 2005).
The parasitic groups Tabanidae and Rhagionidae are in-groups of
Tabanomorpha (Kerr, 2010). Species of Rhagionidae are known as water
snipe flies and are a relatively small group with about 500 extant species
(Zhang, 2012). About 50 extant species are parasitic on birds, mammals or
amphibians, mainly species of Symphoromyia (Zhang, 2012). In other groups,
plesiomorphic are parasitic while derived forms have abandoned this strat-
egy. An exception might be Rhagionidae, which is thought to have evolved
a predatory lifestyle, while parasitic forms evolved de novo from this strategy
(Grimaldi and Engel, 2005).
The elongate mouthparts of the 4500 species of Tabanidae (Zhang,
2012) are well suited for blood- and nectar-feeding at the same time (Karoyli
et al., 2014) and they have been considered to be the first pollinators of early
angiosperms (Labandeira, 2010).
5. PARASITOIDS
5.1 Hymenoptera
5.1.1 General aspects
Hymenoptera is one of the most diverse groups among insects. Currently
there are 125,000 extant described species, traditionally divided in two
groups: ‘Symphyta’ (‘plant wasps’) and Apocrita (‘waisted wasps’) (Delcl os
et al., 2007). Parasitoidism, hyperparasitoidism and kleptoparasitism occur
in numerous in-groups: Orussidae (a group of ‘plant wasps’), Stephanoidea,
Ephialtioidea, Megalyroidea, Trigonalyoidea, Evanoidea, Proctotrupo-
morpha, Ichneumonoidea (all of these Apocrita, formerly also together
called Parasitica) and some groups of Aculeata (Grimaldi and Engel,
2005). Surprisingly the hosts of most extant species appear to be unknown
(Engel and Perrichot, 2014).
The only symphytan parasitoid group is Orussidae, which is the likely sis-
ter group to Apocrita (Grimaldi et al., 2002). Given this pattern of character
distribution, parasitoidism appears to have evolved in or slightly before the
stem species of Orussidae þ Apocrita (and was lost in apocritan in-groups).
Orussidans were diverse and abundant in the Jurassic and Cretaceous and
were associated with trees due to their ectoparasitoidism of wood-boring
beetles and wood wasps. The wasp waist is restricted to Apocrita. This
morphological character appears to provide them a better mobility of the
abdomen and hence the ovipositor. This appears to have been an essential
novelty for effective parasitoidism.
Like species of Orussidae, species of apocritan groups branching off early,
Stephanoidea and Megalyroidea, are ectoparasitoids of wood-boring beetles
and symphytan wasps (Grimaldi and Engel, 2005). Stephanoideans have a
very similar biology to species of Orussidae. The females use their elongated
ovipositor to pierce through wood into the host that is later eaten by the
parasitoid larvae (Engel et al., 2013a). This type of biology is also retained
the next group branching of the lineage towards the more derived apocri-
tans, Ephialtioidea (Figure 4(a)).
Representatives of Megalyroidea parasitize not only wood-boring bee-
tles (as the groups before) but also spheciform wasps. Their close relatives,
trigonalyoideans, are hyperparasitoids, hence are parasitoids on parasitoid
larvae (Perrichot, 2013).
Representatives of Evanoidea are diverse. The supposedly ancestral
appearing representatives of Aulacidae (Figure 4(b)) are parasitoids, but the
164 Christina Nagler and Joachim T. Haug
more derived forms such as evaniids and gasterupiids are larval predators of
cockroach oothecae (Grimaldi and Engel, 2005). Their inferred oldest rela-
tives are species of the extinct group Praeaulacidae; species of this group
were abundant in the Jurassic and Early Cretaceous of Australia and Asia
(Li et al., 2014).
Proctotrupomorpha is a group of usually very small and tiny parasitoids
(except the giant Pelicinidae). In-groups are Stigmaphronidae, Ceraphroni-
dea, Platygastroidea (Grimaldi and Engel, 2005). These wasps are
Insects as Parasites and Hosts 165
groups, such as bees, wasps, flies, moths, beetles, but also cockroaches. Spe-
cies of Rhopalosomatidae are ectoparasitoids of crickets. Lastly species of
Scoliidae are ectoparasitoids of ground-burrowing beetles (Grimaldi and
Engel, 2005).
Also in the lineages that diverged from the ancestral type of parasitoidism
and switched to other strategies, parasitoidism (or parasitism?) has (re-)
evolved. For example, some ants are secondarily ectoparasitoids or klepto-
parasitic, but no fossil forms of these have been found so far (Grimaldi
and Engel, 2005). Within eusocial bees, different types of kleptoparasitism
are known (Litmann et al., 2014). Also species of spheciform wasps, Ampu-
licidae, Sphecidae and Crabronidae are parasitoids. Their larvae feed on the
living host for several larval stages, entering the host’s body and live as endo-
parasitoid. After the host is dead, the larvae spin a cocoon and pupate within
the host (Grimaldi and Engel, 2005). Spheciform wasps are evolutionarily
important as they are the sister group to bees (e.g. Johnson et al., 2013).
5.2 Strepsiptera
5.2.1 General aspects
Strepsipterans are obligate endoparasitoids; Strepsiptera comprises ca. 600
extant species. These parasitize numerous different types of insects, mainly
representatives of Auchenorrhyncha (like Cicadellidae, Membracidae),
Hymenoptera, Hemiptera and Zygentoma (Rasnitsyn and Quicke, 2002).
Part of their success has been attributed to their pronounced sexual
dimorphism and life cycle. Strepsipteran males bare halteres and hind wings.
They are agile fliers, but live only a few hours, to find a female
(Kathithiramy, 2009; Grimaldi and Engel, 2005). Most females are wingless
and sack-like, lack functional eyes and antennae. In some groups which
retain some more ancestral features, females bear short antennae, reduced
(but still present) eyes and legs. They live their entire life within the host.
The hosts’ life span can last until all strepsipteran larvae emerge from the
host (Kathithiramby, 2009).
The larvae hatch immediately when the egg is laid (ovovivipary). The
first larva, is called a triungulin (cf. Meloidae). This larva actively searches
for a host. Most of them search for larvae or nymphs, some go for eggs
(Kathithiramby, 2009). After finding a potential host, the strepsipteran larva
attaches to the host; special enzymes allow the larva to enter the host.
To avoid the host’s immune defence, the larvae mimic the host at a mo-
lecular level. This mechanism is unique among insect parasitoids and
170 Christina Nagler and Joachim T. Haug
Figure 5 Fossil parasitoid strepsipterans (Figure 5a and b); plant parasitic gall wasp
(Figure 5(c)). (a) Bahiaxenos relictus (Bahiaxenidae, Strepsiptera) (modified with permis-
sion from John Wiley & Sons from Bravo et al. (2009, Figure 2)). (b) Bohartilla kinzelbachi
(Bohartillidae, Strepsiptera) (modified from Grimaldi and Engel (2005, Figure 10.88) with
kind permission of Cambridge University Press and David Grimaldi). (c) Gall-forming cyn-
ipidan (Cynipidae, Hymenoptera) (modified from Grimaldi and Engel (2005, Figure 11.17)
with kind permission of Cambridge University Press and David Grimaldi).
amber. In Baltic and Dominican amber, more modern (Figure 5(b)) and
less-derived strepsipterans occur together.
• Some fossils provide quite direct evidence for the extraordinary life cycle
of strepsipterans and direct evidence for their parasitoid lifestyle: (1) two
puparia on an ant specimen in Middle Eocene oil slate of Messel (Lutz,
1990), (2) an ant with an emerging parasite preserved in amber (Pohl and
Kinzelbach, 2001), (3) an empty male puparium associated with a hyme-
nopteran preserved in amber, (4) two parasitized planthoppers, from one
of these planthoppers emerge larvae (Poinar, 2004b) and preserved in
amber, (5) a female specimen ascribed to Myrmecolacidae parasitizing
an ant in Baltic amber (Pohl and Kinzelbach, 2001).
the possible parent could have been a dragonfly, due to the elongated
ovipositor, that is needed to pierce through the robust leaves of bennet-
titalean plants. Yet also other insect groups possess long ovipositors.
• There are some leaf-mining fossils that appear extremely similar to their
modern counterparts: moths on oaks (for 20 million years), moths on
poplars (for 20 million years), moths on mahogany (for 40 million years)
and beetles on Heliconia (for 70 million years) (Grimaldi and Engel,
2005).
7. INSECTS AS HOSTS
7.1 Nematoida
7.1.1 General aspects
The monophyletic group Nematoidea consists of the two sister groups
Nematomorpha (hairworms) and Nematoda (roundworms) (Bleidorn
et al., 2002; Schmidt-Rhaesa, 2013).
Within the hairworms, 350 extant species are known which fall into two
groups: Gordiida with freshwater and terrestrial forms and Nectoma with
marine forms (Schmidt-Rhaesa, 2013). Gordiids have a free-living aquatic
phase and an obligate parasitic phase on terrestrial invertebrates. The parasite
goes through two hosts; the final host (insect) has to eat the intermediate
host (freshwater snail, small aquatic insects; Poinar, 2011a; Labandeira,
2002; Schmidt-Rhaesa and Ehrmann, 2001). Extant species parasitize
carabid beetles, grasshoppers, cockroaches and praying mantids (Schmidt-
Rhaesa and Ehrmann, 2001).
Nematoda includes about 10,500 species that are endoparasites of arthro-
pods and vertebrates (Poinar and Thomas, 2014; Poulin, 2006). Although
there are about 20,000 described extant nematode species, several million
species have been estimated (Schierenberg and Sommer, 2011; Poinar,
2012a). Fossil nematode parasites are treated in detail elsewhere in this
volume (Poinar, 2015).
7.2 Mites
7.2.1 General aspects
Acari comprises about 55,000 described extant species, known as mites.
They can be free-living herbivorous and scavenging, as well as predatory,
or parasites of insects and vertebrates (Dunlop and Penney, 2012; Pereira
et al., 2012). They are also important vectors of several viruses and bacteria,
for example Borrelia burgdorferi that causes Lyme disease and might have
already been so in the past (Poinar 2014a,b, 2015). Mites use insects, partic-
ularly termites, ants and other arthropods for transport in a phoretic way also
(Dunlop and Penney, 2012).
176 Christina Nagler and Joachim T. Haug
Figure 6 Vectors and hosts. (a) Pheidole dentata (Myrmicinae, Formicidae) parasitized by
nematodes (modified after Poinar (2012a, Figure 6(c))). (b) Lutzomyia adiketis
(Phlebotominae, Diptera) (modified after Poinar (2008b, Figure 1)). (c) Myrmozercon sp.
(Mesostigmata, Acari) attached to Ctenobethylus goepperti (Dolichoderinae, Formicidae)
(modified from Dunlop et al. (2014, Figure 1(b)) with kind permission of the Royal Society).
(d) Erythraeid mite (Erythraeidae, Acari) on a chironomid midge (Chironomidae, Diptera)
(modified from Poinar and Krantz 1997, Figure 2 with kind permission from Springer Science
and Business Media). (e) Cheliferidae indet (Cheliferoidea, Pseudoscorpionida) (modified
from Judson (2009, Figure 5(b)) with kind permission of Geodiversitas and Mark Judson).
7.3 Pseudoscorpions
7.3.1 General aspects
There are currently 3533 described extant species and 41 fossil species of
pseudoscorpions (Harvey, 2013). Pseudoscorpions distantly resemble
scorpions, yet their posterior segments are not differentiated as a tail. Also
pseudoscorpions possess a characteristic cheliceral spinning apparatus
178 Christina Nagler and Joachim T. Haug
8. INSECTS AS VECTORS
8.1 General aspects
Extant insects are important vectors for numerous viruses, bacteria and
protist, but it is difficult to give fossil evidence for it (Poinar, 2014b). The
most important arthropods that serve as vectors are haematophagous insects
and arachnids (ticks).
180 Christina Nagler and Joachim T. Haug
virus (CPV) and nuclear polyhedrosis virus (NPV), infect only insects and
are distributed among their populations, whereas some attack mammals
and birds also. These viruses are always fatal to the population of the
infected insects.
9. CONCLUSION
Given the shear vastness of examples of parasitism in and by insects, it
is hard to draw any major conclusions. However, a few overriding patterns
can be mentioned.
Two of the four hyperdiverse lineages appear to have their early radia-
tions coupled to parasitism sensu lato, namely Hymenoptera and Diptera.
So we can indeed ask what made these two lineages so successful. In both
cases, the parasitic act is directly linked to the provision of nutrition to
offspring, in early hymenopterans by injecting the egg into a host, and in
dipterans by haematophagy of the female to have enough nutrients to be
stored in the eggs. Compared to other lineages the parasitic act is therefore
less of an ‘everyday business’, which mainly means that in both lineages the
mobility of the adult is retained. This is quite different, for example, in fleas
or lice, where developing successful dispersal mechanisms are likely one of
the important factors in the early diversification of these two lineages.
Another similarity is that in both Hymenoptera and Diptera, there were in-
dependent switches to feeding on flower products, which likely triggered a
Insects as Parasites and Hosts 183
Figure 7 Timescale of the discussed groups. Dashed lines indicate the ghost range of
the respective groups. Solid lines are based on actual findings of the respective
groups.
10. OUTLOOK
With the given examples, we provide direct and indirect evidence for
palaeoparasitology concerning insects. Regrettably most fossil examples for
palaeoparasitism only provide indirect evidence for parasitism (pathological
changes of the host, functional morphology of the isolated parasite, phylo-
genetic inference) and these are more difficult to compare to their extant
counterparts. Nevertheless, these fossils have the potential to reveal impor-
tant aspects of the origins and diversification of parasitic lifestyles in various
evolutionary lineages. But even with all these fossil examples, for which
there is a much better record than in many other metazoan groups, we
184 Christina Nagler and Joachim T. Haug
ACKNOWLEDGEMENTS
Foremost we thank the editors for the invitation to contribute to this volume. CN is funded
by the Studienstiftung des deutschen Volkes with a PhD fellowship. JTH is kindly funded by
the German Research Foundation (DFG) under Ha 6300/3-1. Both authors thank J. M.
Starck, Munich, for his support. We thank all people involved in providing free and low-
cost software, such as OpenOffice, CombineZM, CombineZP, Image Analyzer.
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CHAPTER FIVE
Contents
1. Introduction 202
2. Trematode-Induced Shell Malformations in Living Bivalve Molluscs 206
3. Occurrences of Trematode-Induced Pits in Fossil and Subfossil Bivalves 211
3.1 Taxonomic, temporal and ecological occurrences 211
3.2 Taphonomy and the origin of the trematodeebivalve parasiteehost 217
interaction
3.3 Trematode-induced malformations as palaeoenvironmental indicators 220
4. Detrimental Effects of Trematodes on Living Bivalves and Their Potential 222
Evolutionary Implications
5. Concluding Remarks 225
Acknowledgements 226
References 226
Abstract
Parasitism is one of the most pervasive phenomena amongst modern eukaryotic life
and yet, relative to other biotic interactions, almost nothing is known about its history
in deep time. Digenean trematodes (Platyhelminthes) are complex life cycle parasites,
which have practically no body fossil record, but induce the growth of characteristic
malformations in the shells of their bivalve hosts. These malformations are readily pre-
served in the fossil record, but, until recently, have largely been overlooked by students
of the fossil record. In this review, we present the various malformations induced by
trematodes in bivalves, evaluate their distribution through deep time in the phyloge-
netic and ecological contexts of their bivalve hosts and explore how various tapho-
nomic processes have likely biased our understanding of trematodes in deep time.
Trematodes are known to negatively affect their bivalve hosts in a number of ways
including castration, modifying growth rates, causing immobilization and, in some
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.004 All rights reserved. 201
202 John Warren Huntley and Kenneth De Baets
cases, altering host behaviour making the host more susceptible to their own
predators. Digeneans are expected to be significant agents of natural selection. To
that end, we discuss how bivalves may have adapted to their parasites via heterochrony
and suggest a practical methodology for testing such hypotheses in deep time.
1. INTRODUCTION
Interpreting the history and evolutionary implications of antagonistic bi-
otic interactions in the marine invertebrate fossil record has been a primary
theme in palaeobiology during the last few decades. The primary focus of
this pursuit has been the examination of predatoreprey interactions, which
has highlighted the likely role of antagonistic interactions in shaping macro-
evolutionary trends (Vermeij, 1977; Signor and Brett, 1984; Kowalewski
et al., 1998; Kelley and Hansen, 2003; Madin et al., 2006; Huntley and
Kowalewski, 2007). Competitive interactions have received some attention
in the literature (Hermoyian et al., 2002; Huntley et al., 2008; Tyler and
Leighton, 2011), but may not be an important agent of natural selection in
benthic marine environments (Stanley, 2008). Parasitism, however, is one
of the most pervasive phenomena amongst modern eukaryotic life (Poulin
and Morand, 2000) and, relative to predation, almost nothing is known about
it in deep time (Littlewood and Donovan, 2003). Parasites and the traces they
leave behind have been preserved as fossils (Moodie, 1923; Cameron, 1967;
Fry and Moore, 1969; Conway Morris, 1981; Ruiz and Lindberg, 1989;
Boucot, 1990; Savazzi, 1995; Feldmann, 1998; Feldman and Brett, 1998;
Littlewood and Donovan, 2003; Boucot and Poinar, 2010), but the docu-
mentation of the intensity of specific parasiteehost interactions through
deep time is rare indeed (for some notable exceptions see Brett, 1978;
Baumiller and Gahn, 2002; Gahn and Baumiller, 2003; Klompmaker et al.,
2014; Wilson et al., 2014; De Baets et al., 2011, 2015a). Based upon their
relative positions within trophic webs, parasites are likely to be more abun-
dant and diverse than predators in modern ecosystems. There is an increasing
appreciation for the roles of parasites in shaping communities (Hudson et al.,
2006) and promoting evolvability (Zaman et al., 2014), but what role have
they played in shaping ecological and macroevolutionary trends of their hosts
in deep time? In order to discern the importance of parasitism in deep time,
one must first explore its origin in a phylogenetically informed context, sys-
tematically analyze the occurrence and intensity of parasiteehost interactions
through geologic time, consider the potential biases introduced by the process
of fossilization and try to disentangle these biases from the biotic record so that
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 203
we can understand how the biases might distort our view of the history of
parasiteehost interactions.
Bivalve molluscs serve as hosts to a diverse group of parasites and disease-
causing agents including viruses, prokaryotes (e.g. Chlamydia and Rickettsia),
fungi, protistans, parazoans (e.g. boring sponges like Cliona) and metazoans
(e.g. platyhelminths, annelids, molluscs, bryozoans and arthropods); see
Lauckner (1983) for an excellent account of the myriad parasites and diseases
of bivalves. Given that many parasites are typically small-bodied and often
lack biomineralized skeletons, we should not expect an extensive record
of body fossils (although, of course there are exceptions: Fry and Moore,
1969; Baumiller and Gahn, 2002; Gahn and Baumiller, 2003; Poinar,
2003; amongst others); therefore, we must seek evidence for parasitism in
the form of traces and malformations on the mineralized hosts. Unfortu-
nately, not all interactions result in the production of a trace or shell
malformation.
A variety of taxa can produce or induce the formation of a trace or shell
malformation when interacting with the bivalve. Indeed, one of the primary
challenges when interpreting these traces is determining if the interaction
was ante-mortem or postmortem, relative to the bivalve. From this perspec-
tive, we can categorize such interactions and their resulting traces into two
groups: (1) interactions that are the result of active boring or shell destruction
by the putative parasite, and, thereby, we cannot distinguish between a
liveedead and a liveelive interaction, and (2) interactions that induce a
growth reaction by the bivalve, and, thereby, we know that the trace or mal-
formation was the result of a liveelive interaction.
Many taxa produce this first type of trace in bivalves and they may not
be, in some cases, strictly parasitic in origin. For instance, spionid polychaete
worms will frequently bore into calcium carbonate substrates (including
bivalves) and produce characteristic U-shaped (and sometimes more com-
plex shaped) borings with paired openings adjacent to one another on the
valve surface (Blake and Evans, 1973; Thayer, 1974; Zottoli and Carriker,
1974; Huntley, 2007; Rodrigues, 2007; Huntley and Scarponi, 2015). Spio-
nids are generally capable of suspension- and deposit-feeding (Dix et al.,
2005). Their boring activity likely weakens their host’s shell and valve and
site preference of spionids suggests they kleptoparasitize the feeding currents
of their hosts (Huntley, 2007; Rodrigues, 2007). The work of Rodrigues
et al. (2008) revealed that spionid borings in live brachiopods of coastal Brazil
were nearly always occupied by live spionids, whereas live spionids were not
identified in borings found in dead brachiopods from the same location.
204 John Warren Huntley and Kenneth De Baets
Ruiz, 1991; Huntley, 2007; Todd and Harper, 2011; Huntley and Scarponi,
2012, 2015; Huntley et al., 2014; De Baets et al., 2015b), and there is no
other biotic interaction (known so far) that induces the growth of an
oval-shaped pit with a raised rim.
Ituarte and colleagues (Ituarte et al., 2001, 2005; Presta et al., 2014) have
described unusual igloo-shaped morphologies of trematode-induced traces
from high-latitude shallow marine deposits in Argentina (Figure 1(d)).
Ituarte et al. (2001) interpret the igloo structures to represent a response
of the host meant to isolate the parasite. In this case, however, the parasite
is able to maintain an opening between the interior of the would-be blister
pearl (see below) and the space between the mantle and shell, thus
Table 1 Instances of living trematodes identified in contact with shell malformations in living bivalve hosts
208
Trematode parasite Bivalve host
Feeding
Family Species Trace type Family Genus species Life mode mode Reference
Gymnophallidae Gymnophallus sp. Pits, discolouration Veneridae Venerupis pullastra Infaunal Suspension Johannessen (1973)
Parvatrema rebecqui Pits Semelidae Abra tenuis Deposit Campbell (1985)
P. rebecqui Cardiidae Cerastoderma glaucum Suspension
Gymnophallus somateriae Pearls Mytilidae Mytilus sp. Epifaunal Jameson (1903)
e ‘Unknown distome’ Pearls Mytilidae Mytilus edulis Epifaunal Suspension Stunkard and Uzmann
Brachycoelium luteum ICD Donacidae Donax trunculus Infaunal (1958)
B. luteum Tellinidae Tellina fabula Deposit
Tellina tenuis
Tellina solidula
Distomum margaritarum Pearls Mytilidae M. edulis Epifaunal Suspension
D. margaritarum Mytilus galloprovincialis
‘Unknown trematode’ Margaritiferidae Margaritifera margaritifera
Proctoeces milfordensis Mytilidae M. edulis
the igloo structures described by Ituarte et al. (2005) in the nuculanid Yoldia
woodwardi from modern death assemblages in Argentina (Ituarte et al., 2005).
If Liljedahl’s igloo-like structures are indeed the result of trematode infesta-
tion, then these would be, by far, the oldest fossil evidence for trematodes and
parasitic flatworms in the fossil record (De Baets et al., 2015b). Currently,
more comparative work is required to determine the relatedness of the Silu-
rian igloo-like traces and trematode parasites. It cannot therefore be ruled
out, that they are related with other organisms with similar behaviour (De
Baets et al., 2015b). Significant temporal gaps in the trematode record also
Table 2 Occurrences of trematode-induced traces on fossil and subfossil bivalve death assemblages
Bivalve host
213
(Continued)
Table 2 Occurrences of trematode-induced traces on fossil and subfossil bivalve death assemblagesdcont'd
214
Bivalve host
Trace type Family Species Life mode Feeding mode Environment Country Age Reference
Semelidae Abra sp. Deposit/suspension England
Tellinidae Macoma sp. Canada
Sweden
Veneridae Ch. gallina Suspension Italy Huntley and Scarponi
(2012)
Gemma sp. USA Ruiz and Lindberg (1989)
Canada
Gouldia sp. USA
Psephidia sp.
Transennella sp.
Venerupis sp. Sweden
Igloo Cyamiidae Cyamiomactra sp. e e Marine Argentina Holocene Ituarte et al. (2005)
Pits Mactridae Mactra sp. Infaunal Suspension Marine Sweden Pleistocene Ruiz and Lindberg
Blank cells indicate the same content as the above cell and the dashed lines indicate that the value is unknown.
215
216 John Warren Huntley and Kenneth De Baets
Figure 3 Life modes (a) and feeding modes (b) of bivalve hosts of trematodes (live in-
teractions and from traces in fossil and subfossil hosts).
others); and this is no less true for the fossil record of trematodes. Trematodes
are amongst the least likely organisms to be preserved as fossils; indeed, they
have little to no body fossil record (Ruiz and Lindberg, 1989; Littlewood and
Donovan, 2003; Boucot and Poinar, 2010; De Baets et al., 2015b). Trema-
todes are small-bodied metazoans (typically submillimetre in length) that
produce neither biominerals nor recalcitrant organic material for skeletons.
The only means we have to study their occurrence in deep time are their
trace fossils (e.g. Littlewood and Donovan, 2003; Littlewood, 2006), the
characteristic pits and igloos whose growth they induce in their bivalve hosts.
Fortunately, the biomineralized skeletons of bivalves are much more robust
to the taphonomic vagaries of the fossil record than trematodes, and their
body fossil record extends to the Cambrian. Moreover, the morphology
of bivalves and the stratigraphic context of the sediments in which they
are preserved yield much information about the environment of deposition
and how the bivalves functioned in their environment (Stanley, 1970).
Despite the robust nature of the fossil record of bivalves (compared with
other taxa), it is still subject to significant taphonomic biases.
Bivalve skeletons are a composite material comprised of calcium carbon-
ate crystals (calcite and/or aragonite) and an organic matrix (Rhoads and
Lutz, 1980 and the chapters therein). The calcite polymorph is more stable
under temperature and pressure conditions at Earth’s surface than aragonite.
Indeed, aragonite often recrystallizes to calcite or preferentially dissolves dur-
ing the processes of sediment lithification and diagenesis. Anatomical detail is
typically lost during recrystallization as the primary aragonitic microstructure
recrystallizes into much larger crystals of blocky calcite. Specimens whose
aragonite dissolves can sometimes be preserved as steinkerns, or complete in-
ternal moulds formed by lithified infilling sediment. The preferential loss or
lowered resolution of aragonitic taxa has been cited as a significant factor
biasing our understanding of Phanerozoic diversity trends (Bush and
Bambach, 2004), and this factor could likely play a role in diminishing the
fossil record of trematode traces. Trematode traces are likely to be obliter-
ated by the coarse process of recrystallization, and internal moulds are not
as likely to display pits as the original shell material. Trematode pits have
been found preserved in positive relief on a Holocene steinkern (Huntley
et al., 2014) and blister pearls can potentially also be traced further back in
time (cf. De Baets et al., 2011); however, in many cases steinkerns are
comprised of sediment whose grain size is similar to or larger than the
millimetre-scale trematode pits, thereby reducing the likelihood of pre-
servation of parasite-induced malformations. Therefore, aragonitic or mixed
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 219
One of the more intriguing results from Huntley and Scarponi’s (2012)
study was that trematode prevalence was significantly higher in lower shore-
face environments during times of sea-level rise (transgression) than in com-
parable environments during sea-level fall (regression). Huntley and
Scarponi (2012) suggested that differences in sedimentation rate and salinity
stability in the lower shoreface during sea-level rise and fall could have influ-
enced trematode prevalence, but, of course, it is very difficult to disentangle
the numerous abiotic and biotic variables that change with sea-level cycles.
In a follow-up study, Huntley and Scarponi (2015) examined modern death
assemblages from 11 locations in 2 sectors separated by the Po River Delta
along the Northern Adriatic coast of Italy. North of the Po River Delta,
conditions are very much like that during Holocene transgression with bar-
rier island/lagoon/estuary complexes. Conversely, the prograding Po River
Delta and adjacent strand plains to the south are quite similar to the environ-
mental conditions during relative regression in the Holocene. The counter-
clockwise flow of surface currents in the Northern Adriatic Sea diverts the
influence of the Po Delta to the south. This influence wanes with distance
to the south and is virtually absent to the north of the delta. As predicted,
trematode prevalence values amongst modern death assemblages were
high at north of the delta, nearly absent in the vicinity of the delta and
returned to higher values much further south of the delta, beyond its
222 John Warren Huntley and Kenneth De Baets
bivalves that reach first reproduction sooner (either via an increase in growth
rate or reproducing earlier at a smaller body size) would have an advantage
when dealing with trematode parasites. Ruiz and Lindberg (1989) and Ruiz
(1991) noted a statistically significant decrease in body size of the bivalve host
Transenella through the Pleistocene of California. They recognized that
trematode prevalence was positively correlated with host body size (also
recognized by Huntley (2007) and Huntley and Scarponi (2012)) and may
select for earlier first reproduction amongst bivalve hosts. Ruiz and Lindberg
(1989) interpreted the trend of decreasing body size through time as the
result of decreasing length of time to first reproduction in the ontogeny
of Transenella. However, this interpretation was based upon sizeeage rela-
tionships that need to be confirmed as consistent through geologic time.
An internal chronology can be established by investigating the presence of
seasonal variation and annual cycles in d18O (the ratio of 18O to 16O in a
sample relative to the same ratio in a standard, reported in per mil; often
an inverse proxy for temperature) values of bivalve carbonate along the
axis of maximum growth. Such seasonal variation could serve as an ‘ontoge-
netic clock’ for an individual that would enable one to calculate bivalve
longevity and growth rates through ontogeny (Jones et al., 1986; Romanek
and Grossman, 1989; Kirby et al., 1998; Goodwin et al., 2001; amongst
others). When these temperature proxy data are plotted relative to distance
from the umbo (the portion of the shell formed in the earliest stages of
ontogeny) growth rates can be quantified. Moreover, a significant decrease
in growth rate often indicates the onset of sexual maturity of marine inver-
tebrates (Romanek and Grossman, 1989). As an example, Figure 5 shows
the d18O values of shell carbonate samples (n ¼ 27) collected along the
growth axis from the umbo to the posteroventral margin of a Chamalea
gallina valve from the Northern Adriatic coast of Italy. The cycles are inter-
preted as three annual cycles and the sharp troughs likely represent growth
cessation in the winter. This specimen was live-collected and sacrificed in
February 2010; therefore, it is possible to determine the calendar years
that correspond to these annual cycles. Moreover, if we can estimate the
d18O value of the sea water in which this clam grew, it is possible to estimate
the actual temperature of the sea water (Grossman and Ku, 1986). In addi-
tion to providing an internal chronology for this individual clam, these data
suggest reduced growth in year two and an overall trend of increasing tem-
perature during the three years. Following this methodology, growth rates
and age at onset of sexual maturity of parasitized and nonparasitized individ-
uals could theoretically be approximated in order to test the influence of
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 225
Figure 5 Oxygen isotope (d18O V-PDB) profile for an individual specimen of Chamalea
gallina from the Northern Adriatic Sea (Primi Piatti sample). The cyclical nature of the
profile suggests 3 years of growth, and the sharp ‘bottoms’ of the winter portion sug-
gest a hiatus of growth during the coldest months.
trematode parasitism on the life history of hosts through geologic time and
should be a fruitful avenue for future research.
5. CONCLUDING REMARKS
There is an increasing interest in elucidating parasiteebivalve interac-
tions through deep time. Trematodes, though lacking a continuous body
fossil record, induce the growth of a number of characteristic malformations
on the interior shell walls of their bivalve hosts, which can be traced back
in the fossil record. Gymnophallid trematodes living in close association
with malformations on the interior of living bivalves have been well-docu-
mented. Trematode pits and igloos have been identified in four of the six
major lineages within the bivalve evolutionary tree spanning back as far as
the Eocene (when they appear rather suddenly, in terms of geologic time
that is, in seven families from three lineages). Igloo-like structures have
been found in Silurian Protobranchia, but further work is required to
confirm their trematode origin and to explain the subsequent 420-
million-year gap in the igloo fossil record (compare De Baets et al.,
2015b). Large gaps in the fossil record of such structures might potentially
226 John Warren Huntley and Kenneth De Baets
ACKNOWLEDGEMENTS
John Huntley is grateful to Kenneth De Baets and Tim Littlewood for the invitation to
contribute to this volume. We thank reviewers Michelle Casey (University of Kansas) and
David Thieltges (NIOZ, Royal Netherlands Institute for Sea Research) for their thoughtful
and constructive suggestions that improved this manuscript. Gabriel Carlier and Marie-
Madeleine Blanc-Valleron extended kind hospitality and assistance during Huntley’s visit
to the Museum National d’Histoire Naturelle in Paris. Daniele Scarponi (Universita di
Bologna) and Paola De Muro kindly prepared the Primi Piatti bivalve sample. Stable isotope
samples were collected and analyzed by Ken MacLeod’s Methods in Paleoclimatology class at the
University of Missouri (Claire Beaudoin, Jesse Broce, Shannon Haynes, Page Quinton and
Tara Selly). Funding to conduct these analyses was generously provided by the Keller
Opportunities for Excellence Fund of the Department of Geological Sciences, University
of Missouri. Franz T. F€ ursich kindly encouraged and enabled the exploratory fieldwork of
the senior author that led to this line of inquiry. Fieldwork was made possible by a generous
Ford Ka grant from the Corey and Heather Long Foundation (JWH). Funding for this proj-
ect was generously provided by the Alexander von Humboldt Stiftung (Renewed Research
Stay Grant; JWH) and the University of Missouri Research Council (SRF-14-019; JWH).
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CHAPTER SIX
Contents
1. Introduction 234
2. Crustaceans as Hosts of Parasites 236
2.1 Fossil evidence 236
2.1.1 Isopod parasites in decapod crustaceans 236
2.1.2 Rhizocephalan barnacles in decapod crustaceans 244
2.1.3 Platyhelminthes in crustaceans 246
2.2 Equivocal fossil evidence 246
2.2.1 Ciliates on ostracods 246
2.3 Modern evidence only 246
2.3.1 Non-crustacean parasites 246
2.3.2 Crustacean parasites 247
3. Crustaceans as Parasites of Non-crustacean Hosts 249
3.1 Fossil evidence 249
3.1.1 Ascothoracidan barnacles in invertebrates 249
3.1.2 Copepods in echinoderms 252
3.1.3 Copepods in fish 253
3.1.4 Gall crabs (Cryptochiridae) in corals 259
3.1.5 Pentastomida 261
3.2 Equivocal fossil evidence 265
3.2.1 Barnacle borings attributed to Acrothoracica in marine invertebrates 265
3.2.2 Barnacles (Pyrgomatidae) in corals 266
3.2.3 Isopods (Cymothooidea) in fishes and squids 267
3.2.4 Crabs (Trapeziidae) and corals 269
3.3 Modern evidence only 269
3.3.1 Copepods 269
3.3.2 Tantulocarida 270
3.3.3 Branchiura 270
3.3.4 Ostracoda 271
3.3.5 Facetotecta 271
3.3.6 Thoracica 272
3.3.7 Malacostraca 272
Abstract
Numerous crustacean lineages have independently moved into parasitism as a mode of
life. In modern marine ecosystems, parasitic crustaceans use representatives from many
metazoan phyla as hosts. Crustaceans also serve as hosts to a rich diversity of parasites,
including other crustaceans. Here, we show that the fossil record of such parasitic inter-
actions is sparse, with only 11 examples, one dating back to the Cambrian. This may be
due to the limited preservation potential and small size of parasites, as well as to pro-
blems with ascribing traces to parasitism with certainty, and to a lack of targeted
research. Although the confirmed stratigraphic ranges are limited for nearly every
example, evidence of parasitism related to crustaceans has become increasingly more
complete for isopod-induced swellings in decapods so that quantitative analyses can
be carried out. Little attention has yet been paid to the origin of parasitism in deep
time, but insight can be generated by integrating data on fossils with molecular studies
on modern parasites. In addition, there are other traces left by parasites that could
fossilize, but have not yet been recognized in the fossil record.
1. INTRODUCTION
Crustaceans can enter into a wide variety of interspecific associations
including mutualism, commensalism, phoresis, inquilinism and parasitism.
Discerning the precise nature of a close symbiotic association between two
species can be problematic, even when studying living organisms. It is espe-
cially difficult when dealing with fossils. Indeed, when considering fossil
symbiotic associations, Darrell and Taylor (1993) concluded that the terms
parasitism, mutualism and especially commensalism should be used with
caution or avoided altogether (compare Zapalski, 2011). In this chapter,
we define parasitism as a symbiotic relationship in which one organism
(the parasite) is nutritionally dependent upon another (the host) for at least
part of its life cycle and has a negative impact on the fitness of the host (cf.
Tapanila, 2008a, see also Kinne, 1980; Conway Morris, 1990; Rohde,
2005, for similar definitions). The parasitic nature of an association between
two fossil species can be inferred from (1) evidence of detrimental effects of
the inferred parasite on the host, such as reduced growth, by analogy with
related living taxa or (2) by the presence of cysts or swellings that were
inhabited by parasites. Parasitism can be further confirmed when the parasites
themselves are preserved. Surface scars caused by the attachment of sessile
Fossil Crustaceans as Parasites and Hosts 235
barnacles to the plastron and skull of turtles are known from the fossil record
(Hayashi et al., 2013), but modern turtle barnacles are not treated as parasites.
Such an association is a phoresis in which the barnacle is transported by the
host, but it is not nutritionally dependent on the host as it still uses its modi-
fied thoracic limbs for suspension feeding. Similarly, fossils of whale barnacles
such as Coronula are known (e.g. Hayashi et al., 2013), but again, these are
non-parasitic epibionts and are not the focus of this chapter.
The classification of the Crustacea is in a state of flux, although it is now
widely accepted that the Hexapoda emerged from within the Crustacea
and, therefore, that the traditional Crustacea is a paraphyletic taxon (see
Edgecombe, 2010; Giribet and Edgecombe, 2013). We follow a recent sys-
tematic review of the arthropods (Regier et al., 2010) that recognized four
main lineages, Oligostraca, Vericrustacea, Xenocarida and Hexapoda, within
a monophyletic Pancrustacea. The first three of these constitute the traditional
Crustacea and provide the focus for this chapter: only the first two are known
to contain parasites today. The Oligostraca contains two main parasitic linea-
ges, the Branchiura (e.g. Boxshall, 2005a) and Pentastomida (e.g. B€ ockeler,
2005; Christoffersen and De Assis, 2013). The Vericrustacea contains a far
greater diversity of parasitic forms within the sublineage Multicrustacea
including the wholly parasitic Tantulocarida (e.g. Boxshall, 2005b) as well
as numerous parasitic lineages within the subclasses Thecostraca (e.g. Asco-
thoracida, Rhizocephala, Thoracica) (e.g. Pérez-Losada et al., 2004; Glenner
and Hebsgaard, 2006; Rees et al., 2014), Copepoda (Boxshall, 2005c) and
Malacostraca. Within the Malacostraca, the majority of parasitic forms are pe-
racarids belonging to the Amphipoda (L€ utzen, 2005) or Isopoda (e.g. Lester,
2005; Williams and Boyko, 2012). The hosts used by parasitic crustaceans
include representatives of many aquatic metazoan phyla, from sponges and
cnidarians to chordates, including tunicates, fishes, reptiles and mammals.
Crustaceans also serve as intermediate or definitive hosts to an enormous
range of parasites, including protists (e.g. Levine, 1988), acanthocephalans
(e.g. Taraschewski, 2000), nematodes (e.g. McClelland, 2002), cestodes
(e.g. Dollfus, 1976), monogeneans (e.g. Okawachi et al., 2012) and dige-
nean trematodes (e.g. Cribb, 2005), and even other crustaceans. In the great
majority of platyhelminthecrustacean associations, the crustacean serves as
an intermediate host as, for example, in parasites of humans such as Guinea
worm (Dracunculus) and fish tapeworm (Diphyllobothrium latum), both of
which use freshwater copepods as intermediate hosts.
Crustaceans have an extensive fossil record stretching throughout the
Phanerozoic, but evidence of crustaceans serving as hosts for parasites, or
236 Adiël A. Klompmaker and Geoff A. Boxshall
exhibiting a parasitic mode of life is relatively rare. Body fossils of the para-
sites themselves are particularly rare, but evidence of palaeoparasitism may be
found more commonly in traces such as structures formed as a result of the
interaction between parasite and host. In this chapter, we aim to discuss the
fossil evidence of crustaceans as parasites and hosts, provide a brief overview
of exclusively modern examples and discuss the potential of finding their
traces in the fossil record. We also explore what molecular clock studies
reveal concerning the stratigraphic range over which such parasitic interac-
tions involving crustaceans may have occurred.
Institutional abbreviations: Geomuseum Faxe, Faxe, Denmark (OESM),
Naturhistorisches Museum Wien, Vienna, Austria (NHMW); Florida
Museum of Natural History, University of Florida, Gainesville, Florida,
USA (UF); Oertijdmuseum De Groene Poort, Boxtel, The Netherlands
(MAB k); Natural History Museum of Denmark, Geological Museum, Uni-
versity of Copenhagen, Denmark (MGUH).
further species are added here (see Figure 1) plus K. crusta in the crab Speo-
carcinus berglundi from the late Miocene (Tortonian) of California (Tucker
et al., 1994) and the crab Cristafrons praescientis from the Late Cretaceous
(SantonianeMaastrichtian) of Antarctica (Feldmann et al., 1993) based on
evidence from figures. Recently, Beschin et al. (2015) mentioned a swelling
in the branchial region of the Eocene (Ypresian) squat lobster Acanthogalathea
squamosa from Italy, but this record is difficult to confirm in the absence of a
figure. New fossil specimens exhibiting K. crusta have been reported recently
in taxa from which such swellings were already known (Fraaije, 2014, for
Gastrosacus wetzleri; Hyzný et al., 2014, for Galathea weinfurteri; Kornecki,
2014, for Cretocoranina testacea), highlighting the relatively common occur-
rence of such swellings. These swellings have been found mostly in fossil
true crabs (Brachyura) and squat lobsters (Galatheoidea); evidence of infes-
tation of lobsters and shrimps is relatively scarce (Wienberg Rasmussen
et al., 2008; Klompmaker et al., 2014). Only one swelling is known from
a shrimp (Franţescu, 2014), despite the common occurrence of isopods in
modern shrimps (Boyko and Williams, 2009). This can be explained by
the lower fossilization potential of shrimps due to their relatively soft
exoskeleton. Of note is the recent discovery of a swelling in the fixed finger
of a propodus of the Holo-Pleistocene ghost shrimp Glypturus panamacana-
lensis, but this swelling was probably not caused by a parasitic isopod
(Klompmaker et al., 2015).
Modification of secondary sex characters by epicaridean isopods, such as
feminization of the male chelae in shrimps (e.g. Tucker, 1930; Beck, 1980)
and widening of the abdomen in male crabs (Reinhard, 1956), has been
recorded in modern decapods, but this would be difficult to detect in fossils
unless specimens are exquisitely preserved.
2.1.1.6 Age
This type of parasitism in decapods dates back to the Jurassic, possibly the
Early Jurassic (Toarcian) based on a lobster, although this is only inferred
from a drawing (Wienberg Rasmussen et al., 2008; Klompmaker et al.,
2014). Thus far, Middle Jurassic deposits have not yielded an example of
K. crusta, and this discontinuity adds to the uncertainty surrounding the Early
Jurassic record. Given the estimated occurrence of calanoid copepods as far
back as the Silurian, based on a phylogeny using morphological and mole-
cular evidence (Selden et al., 2010), and the presence of decapods since the
Devonian (e.g. Feldmann and Schweitzer, 2010; Gueriau et al., 2014; Jones
et al., 2014), Early Jurassic and older occurrences are theoretically possible as
the two host groups would have been available. Unfortunately, no rigorous
phylogenetic analyses of epicarideans including estimated divergence times
are known to us. The only study is based on limited evidence. Using three
species, Lins et al. (2012) showed that the last common ancestor of the
Bopyridae, Dajidae and Sphaeromatidae (non-parasitic) would root in the
Permian.
Some insight may come from related isopods such as the Cymothooidea
(e.g. Dreyer and W€agele, 2001; Boyko et al., 2013). Dreyer and W€agele
(2001, Figure 12) speculated that cirolanid-like cymothoids feeding on
fish evolved to become parasitic on/in fish (Cymothoidae), and also gave
rise to the Bopyridae infesting crustacean hosts, resulting in the radiation
of bopyrids. This radiation may be best expressed in the Late Jurassic
(Figure 2). The Cymothoidae have, however, no fossil record (Smit et al.,
2014), which may indicate a low preservation potential. The non-parasitic
Cirolanidae have an undisputed fossil record into the Middle Jurassic,
whereas the Cymothoida are known from the Early Triassic (Etter, 2014).
Thus, if Dreyer and W€agele’s (2001) hypothesis is correct and the fossil re-
cord is a reasonable representation of the occurrence of the Cymothoida,
then no isopod-induced swellings in decapod crustaceans are to be expected
from the Palaeozoic.
2.1.1.7 Biogeography
It is noteworthy that the oldest report of K. crusta originates from Indonesia
(although it is disputed), whereas all Late Jurassic and Early Cretaceous
occurrences are from Europe (Klompmaker et al., 2014, Table 3). A global
distribution of this type of parasitism does not occur until the Late Creta-
ceous with occurrences in Europe, North America, New Zealand and
Antarctica. Whether this European peak in the Late Jurassic and Early
242 Adiël A. Klompmaker and Geoff A. Boxshall
best preserved examples of this type of parasitism, from specimens of the crab
Tumidocarcinus giganteus from the Miocene of New Zealand (Figure 3). A
feminized male showed a broader than usual abdomen and its major claw
was more like those of females in terms of size. He specifically attributed
this to parasitism by rhizocephalan barnacles, unlike previous accounts. It
should, however, be noted that parasitism by epicarideans (including non-
bopyroids such as entoniscids) can also result in the feminization of males,
including a widening of the abdomen and reduction in claws (Reinhard,
1956; Rasmussen, 1973), so that these infestations can ‘duplicate closely
the effects by Rhizocephala’ (Reinhard, 1956, p. 91). Careful examination
of the carapace may show slight deformations in entoniscid-infested crabs
(e.g. Miyashita, 1941; Shields and Kuris, 1985), but its expression may not
Figure 3 Normal female and male specimens of the Miocene crab (Tumidocarcinus
giganteus) from New Zealand, and a possible rhizocephalan barnacle infested conspe-
cific specimen showing feminization of the abdomen and claws. (a) Abdomen of a
mature female. (b) Ventral side of a mature male. (c) Ventral side of a juvenile female.
(d) Ventral side of a feminized male. Scale bars 10 mm. (From Feldmann (1998),
Figure 3)
246 Adiël A. Klompmaker and Geoff A. Boxshall
3. CRUSTACEANS AS PARASITES OF
NON-CRUSTACEAN HOSTS
3.1 Fossil evidence
3.1.1 Ascothoracidan barnacles in invertebrates
These small barnacles (up to 8 mm in size) parasitize a variety of modern
marine hosts, particularly echinoderms (but not regular echinoids and sea cu-
cumbers) and cnidarians (gorgonians, zoanthids, scleractinians and antipatha-
rians) (e.g. Moyse, 1983; Grygier, 1996; Grygier and Høeg, 2005). Many are
endoparasitic in the main body cavity of asteroids and echinoids, but ectopa-
rasitic on anthozoans, crinoids and ophiuroids (references in Krawczy nski and
Wilson, 2011, but see Grygier and Høeg, 2005). Several ascothoracidans
(Ascothorax, Ulophysema and Dendrogaster) cause castration of their echinoderm
hosts (Grygier and Høeg, 2005). Grygier and Høeg (2005) noted that little is
known about their feeding behaviour, but basal forms have piercing and
sucking mouthparts while the more transformed genera such as Ulophysema
and Dendrogaster employ absorptive feeding, similar to rhizocephalans.
Body fossils of these barnacles are unknown, but structures attributed
to ascothoracidans have been reported from the fossil record (Figure 4;
Table 1). Voigt (1959) first recognized galls or cysts named Endosacculus
moltkiae in the Late Cretaceous octocoral Moltkia minuta that were attri-
buted to ascothoracidans because of morphological similarity to cysts of
modern representatives. Moyse (1983), for example, showed morphologi-
cally similar galls on modern octocorals. Subsequently, Voigt (1967) found
further Late Cretaceous evidence for infestation of octocorals, presumably
by an ascothoracidan, and a cyst in the early Palaeocene (Danian) hydroco-
ral Astya crassus was suggested to have been produced by parasitic crusta-
ceans (either copepods or ascothoracidans) by Bernecker and Weidlich
(2005), although their photograph (Figure 7(c-1)) does not allow identifi-
cation of the parasitic structure. Voigt (1959) was of the opinion that his
examples did not represent parasitism because the host was not particularly
damaged and continued to grow after infestation. He considered it did not
represent a true endoparasite deriving its food from the host; rather, he sug-
gested that commensalism or ‘syn€ okie’ (inhabitation of host and taking part
in meals of the host sensu K€ orner, 1979) was more appropriate. However,
research on modern ascothoracidans suggests that they are parasitic (see
Grygier and Høeg, 2005).
Fossils attributed to ascothoracidans have also been found in an echinoid
and possibly in a brachiopod. Madsen and Wolff (1965) described the
250 Adiël A. Klompmaker and Geoff A. Boxshall
Moltkia minuta Endosacculus Late Cretaceous The Netherlands ‘Maastrichter Voigt (1959)
(Octocorallia) moltkiae (late Tuffkreide’
Maastrichtian)
M. minuta E. moltkiae Late Cretaceous If€
o (Schonen), ‘Tr€
ummerkreide’, Voigt (1959)
(Octocorallia) (Campanian) Sweden rocks with
Actinocamax
mamillatus
Isis sp. Endosacculus (?) Late Cretaceous South Emba, Rocks with Voigt (1967)
(Octocorallia) najdini (late Kazakhstan Belemnella
Maastrichtian) arkhangelskii
Echinocorys Ulophysema Late Cretaceous Limfjord in North e Madsen and Wolff
(Echinoidea) ePalaeocene Jutland, Denmark (1965)
(?Maastrichtian
eDanian)*
Moorellina negevensis e Middle Jurassic Matmor Hills in Matmor Fm, Krawczy
nski and
(Brachiopoda) (late Callovian) Hamakhtesh lamberti Zone Wilson (2011)
Hagadol, Israel
* pers. comm. Sten Jakobsen to AAK.
251
252 Adiël A. Klompmaker and Geoff A. Boxshall
Figure 5 Examples of Halloween pumpkin-mask cysts (aee) and cysts ascribed to the
ichnotaxon Castexia douvillei (fei), all inferred to be caused by copepod parasites. (a, b)
The modern hydrocoral Stylaster papuensis from Tagula Island, Louisiade Archipelago,
southwest Pacific, showing cysts induced by the copepod Cystomyzon dimerum. (c,
d) Copepod cyst in the gonopore of an echinoid test of Acrosalenia spinosa from the
Middle Jurassic (Bathonian) of Bicqueley, Lorraine, France. (e) Three cysts in a crinoid
stem of Isocrinus tuberculatus from the Early Jurassic (Sinemurian) of Germany. (fei)
Two cysts in an echinoid test of Collyrites dorsalis from the Middle Jurassic (Callovian)
of Mortagne-au-Perche, Orne, France. Smallest cyst (h) located in an ambulacral co-
lumn, whereas the larger one (i) is positioned in an interambulacral column. Scale
bars unavailable in source articles. ((a, b) from Zibrowius (1981), pl. 1.8 and 2.4; (c, d)
from Radwan ska and Poirot (2010), Figure 4; (e) from sole figure in Weinfurtner (1989);
(fei) from Radwanska and Radwan ski (2005), Figure 11.1)
254
Host taxon Name cyst Age country unit (if known) References
Acrosalenia spinosa Halloween Middle Jurassic Bicqueley, Lorraine, Caillasse a Anabacia, Radwa
nska and
(Echinoidea) pumpkin-mask (early France convergens Poirot (2010)
e test Bathonian) Subzone
A. spinosa Halloween Middle Jurassic Luc-sur-Mer, Basse- Caillasses de Basse- Radwa
nska and
(Echinoidea) pumpkin-mask (late Bathonian) Normandie, Ecarde Poirot (2010)
e test France
Acrosalenia Halloween Middle Jurassic Calvados, France Richter (1991)
hemicidaroides pumpkin-mask (Bathonian)
(Echinoidea)
e test
Cidaroida Halloween Late Jurassic Germany Goldfuss (1829)
(Echinoidea) pumpkin-mask
e test
Plegiocidaris Halloween Late Jurassic (early Ludwag Quarry, Mehl et al. (1991)
255
(Continued)
Table 2 Echinoderms inferred to be infested by copepods resulting in cysts or swellingsdcont'd
Locality and Stratigraphic
256
Host taxon Name cyst Age country unit (if known) References
Echinoidea e Halloween Middle Jurassic Israel Matmor Borszcz et al. (2014)
spine pumpkin-mask (Callovian) Formation
Isocrinus Halloween Early Jurassic Autobahn A9, near Weinfurtner (1989)
tuberculatus pumpkin-mask (Sinemurian)* G€oggelsbuch near
(Crinoidea) e Allersberg,
stem Germany
Millericrinus Halloween Late Jurassic France De Loriol (1886)
horridus pumpkin-mask (Oxfordian)
(Crinoidea) e
stem
Collyrites dorsalis Castexia douvillei Middle Jurassic Marolles, Sarthe, Lambert (1927)
(Echinoidea) (late Callovian) France
e test
C. dorsalis C. douvillei Middle Jurassic Courgeou, Orne, Mercier (1936)
257
258 Adiël A. Klompmaker and Geoff A. Boxshall
Figure 6 The copepod Kabatarina pattersoni found in the fish Cladocyclus gardneri from
the Early Cretaceous of Brazil. (a) Lateral view of cephalothorax showing mouthparts
and anterior swimming legs. (b) Reconstruction of adult female ((a) from Cressey and
Boxshall (1989), pl. 1.2; (b) from Cressey and Patterson (1973), Figure 1, Science 180,
1283e1285, reprinted with permission from AAAS). Scale bars 100 mm.
Fossil Crustaceans as Parasites and Hosts 259
may result from the feeding activity of ectoparasitic crustaceans, such as co-
pepods. However, other causative agents are possible so the involvement of
copepods cannot be confirmed. Lesions in fishes can have diverse causes,
making it difficult to identify in fossil fishes without preserved pathogen
remains (Petit, 2010; Petit and Khalloufi, 2012).
impact on the resources of the coral to justify calling these crabs parasitic,
which is typically not specified in definitions of parasitism. Simon-Blecher
and Achituv (1997) suggested that C. coralliodytes is a parasite of faviid corals
because specimens settle on a coral polyp resulting in the death of that polyp,
they inhibit coral growth rate (as shown quantitatively) and create depres-
sions in the coral skeleton around the pits. Simon-Blecher et al. (1999)
found that the same species encouraged algal and fungal growth in and
around the pit, and that the crabs feed on coral mucus, possibly leading to
an energy loss for the coral. They also speculated that mucus removed by
crabs could decrease the efficiency of feeding by the polyps. Based on qua-
litative observations, Mohammed and Yassien (2013) considered that the
gall-forming species H. marsupialis and Opecarcinus aurantius would have no
effect on coral growth. Carricart-Ganivet et al. (2004) analysed the gut con-
tents of Troglocarcinus corallicola and found green pigments, filamentous algae,
foraminifera and some suspended material, suggesting that this species ob-
tained its food at least partially from material deposited in the depression
around its cavity. Recently, Nogueira et al. (2014) showed a positive, signi-
ficant correlation between cryptochirid (Kroppcarcinus siderastreicola) cavity
size and size of the depression around the coral Siderastrea stellata, high-
lighting the negative effect of that cryptochirid on coral growth. Recent
articles refer to cryptochirids by the all-inclusive term obligate symbionts
(e.g. Badar o et al., 2012; Van der Meij, 2014, 2015; Van der Meij and
Schubart, 2014; Canario et al., 2015), but Wei et al. (2013) mentioned
both obligate symbionts and parasites. Obvious benefits for the coral are
unknown. In conclusion, there is continuing debate as to whether crypto-
chirids are commensal or parasitic on their host corals, but the argument for
parasitism is strongest for C. coralliodytes. The fact that multiple species feed
on coral mucus and can impact coral growth indicate that at least some
cryptochirids can be considered as coral parasites.
Their fossil record was unknown until very recently, when Portell and
Klompmaker (2014) reported on characteristic crescentic domiciles attri-
buted to cryptochirids in Pleistocene corals from Florida. Subsequently,
De Angeli and Ceccon (2015) claimed the first cryptochirid body fossil,
Montemagrechirus tethysianus, from the Eocene (Ypresian) of Italy. The small
size (w5 mm) and the environment (coral reef) match the attributes of mo-
dern cryptochirids. The overall shape (longer than wide) of the carapace also
fits the Cryptochiridae, but several major differences are evident in the fron-
tal part (the posterior part exhibits few characters). First, the rostrum contains
two pronounced spines in Montemagrechirus that are not present in any of the
Fossil Crustaceans as Parasites and Hosts 261
52 currently known modern species. Moreover, the orbits of the fossil spe-
cies are directed anterolaterally, which is highly unusual for modern crypto-
chirids (only Pseudocryptochirus viridis and two deep water species of
Cecidocarcinus show a somewhat similar orbital position, 5.7%). Of further
note is the well-calcified shell, which is why Montemagrechirus was preserved.
The shell of modern cryptochirids is usually soft and can even be transparent
(Utinomi, 1944; Guinot et al., 2013, for H. marsupialis) or the posterior part
of the carapace is soft (Potts, 1915, for Cryptochirus), although Utinomi
(1944) mentioned that the carapace of Cryptochirus is rather hard. The some-
what transparent nature of cryptochirid carapaces may be observed also in
Badar o et al. (2012) and Van der Meij and Schubart (2014). Portell and
Klompmaker (2014) did not report any remains of cryptochirid shell associ-
ated with the domiciles and no other fossil cryptochirid body fossils have
been found to date, consistent with the relatively soft nature of the carapace.
The anterolateral position of the orbits in combination with the narrowing
of the carapace posteriorly in Montemagrechirus suggests that eyes would have
protruded anterolaterally from the carapace, which may not be most suitable
condition to inhabit a pit or tunnel (indeed, eyes and orbits are typically
directed forward in cryptochirids). This morphology would argue against
parasitism in corals together with the well-calcified shell that would not
be needed for a truly parasitic form living in a pit or gall. Therefore, we
do not consider this taxon further. Whether Montemagrechirus represents an
early cryptochirid (perhaps prior to becoming parasitic) or should be classi-
fied in a different family should be addressed anew.
3.1.5 Pentastomida
Molecular evidence consistently places the Pentastomida as sister group to
the Branchiura, and these two taxa together are referred to as the Ichthyos-
traca which, together with the Mystacocarida and Ostracoda, forms the Oli-
gostracan branch of the Pancrustacea (e.g. Regier et al., 2010; Oakley et al.,
2013; Giribet and Edgecombe, 2013). However, controversy still surrounds
the classification of the Pentastomida, since fossil and some morphological
data have been interpreted as evidence that they represent stem-lineage de-
rivatives of the Euarthropoda and, therefore, cannot be considered crusta-
ceans. Waloszek et al. (2006) concluded that the phylogenetic position of
the Pentastomida remained unresolved, but Castellani et al. (2011) consi-
dered their derivation from the Euarthropodan stem-lineage to be the
most plausible hypothesis. As molecular phylogenetics has moved away
from target-gene approaches towards phylogenomics and transcriptomics
262 Adiël A. Klompmaker and Geoff A. Boxshall
(see Giribet and Edgecombe, 2013), analyses of the flood of new sequence
data have continued to support a sister relationship between the Pentasto-
mida and the Branchiura within the Oligostraca (e.g. Regier et al., 2010;
Sanders and Lee, 2010; Oakley et al., 2013). There is not yet, however,
any stable estimate of divergence times between them: Sanders and Lee
(2010), using data from five genes, estimated a divergence time of 519 Ma
(but with confidence limits of 292e616 Ma), whereas Oakley et al.
(2013) arrived at a maximum estimate of 424 Ma for this split using new
transcriptome data sets plus existing nuclear genome, mitochondrial
genome, EST and ribosomal DNA data. The Oakley et al. (2013) estimate
of divergence time for the Pentastomida and Branchiura conflicts with the
suggested presence of pentastomids in the Cambrian.
Regardless of their correct taxonomic placement, we address parasitism of
this group here. Modern pentastomids, or tongue worms, are obligate para-
sites at all stages of their life cycle (B€
ockeler, 2005). Their definitive hosts are
frequently snakes, but also amphibians, turtles, crocodilians, lizards, birds and
mammals including humans; many of these same taxa, as well as freshwater
and marine fishes and insects, also serve as intermediate hosts (B€ ockeler,
2005; Poore, 2012; Christoffersen and De Assis, 2013). Modern pentastomids
are bloodsuckers (sea birds, reptiles) or feed on mucus and sloughed cells
(mammals) (B€ ockeler, 2005). Currently, 144 species and subspecies are
known (Christoffersen and De Assis, 2013); Poore (2012) listed 124 species.
From the fossil record, only 10 named species are known (Table 3;
Figure 8), all of them from the early Palaeozoic and most are based on phos-
phatized specimens. Andres (1989) was the first to suggest the resemblance of
fossil specimens to pentastomids based on Early Ordovician specimens from
€
Oland (Sweden), but Walossek and M€ uller (1994), Walossek et al. (1994),
Waloszek et al. (2006) and Castellani et al. (2011) described all known
CambrianeOrdovician species thus far, all presumably representing larvae.
Most fossil species are stratigraphically confined to Upper CambrianeLower
Ordovician strata (Table 3). Recently, putative adult pentastomids from the
Silurian Herefordshire Lagerst€atte were reported to be attached to ostra-
cods: such ectoparasitism is unknown in modern pentastomids (Siveter
et al., 2015). A targeted search for specimens in Palaeozoic or Mesozoic
fine-grained limestone deposits of deep-water origin should, eventually,
yield additional species. Such Konservat-Lagerst€atten, in which phosphati-
zation can take place, have yielded most of the species known thus far
(Walossek and M€ uller, 1994; Walossek et al., 1994; see Maas et al., 2006,
for discussion on preservation). Specimens may have been overlooked
Table 3 The species of Pentastomida known from the fossil record
Species Age Locality and country Stratigraphic unit References
263
* Putative pentastomid.
264 Adiël A. Klompmaker and Geoff A. Boxshall
Figure 8 Larvae from fossil pentastomids. (a) Lateral view of Heymonsicambria scandica
from the Late Cambrian (late Furongian) of V€astergo €tland, Sweden. (b) Ventral view of
Heymonsicambria taylori from the Late CambrianeEarly Ordovocian of Canada. (c)
Ventrolateral view of Boeckelericambria pelturae from the Late Cambrian (late Furon-
gian) of V€astergo €tland, Sweden. Scale bars 50 mm. ((a) from Walossek and M€ uller
(1994), Figure 4(a), reproduced by permission of The Royal Society of Edinburgh and Dieter
Waloszek from Transactions of the Royal Society of Edinburgh: Earth Sciences 85, 1e37; (b)
from Walossek et al. (1994), pl. 1.3).
(Waloszek et al., 2006). Walossek and M€ uller (1994) noted that all
CambrianeOrdovician pentastomids were associated with conodonts.
Thus, it could be speculated that these early vertebrates were hosts to penta-
stomids (compare Sanders and Lee, 2010; De Baets et al., 2015). Considering
the small size of early Palaeozoic pentastomids, which are interpreted as adults
by Sanders and Lee (2010; but compare Castellani et al., 2011 for a different
view) and resemblance to larvae of extant pentastomids that infect interme-
diate hosts such as fish, it has been suggested by these authors that the small
Palaeozoic forms confined their entire life cycle to small fish-like vertebrates
present around that time (Sanders and Lee, 2010). They may have transi-
tioned to a more continental habitat along with their hosts in the Late Devo-
nian, when the amphibians arose from lobe-finned fish (e.g. Daeschler et al.,
2006), giving rise to reptiles later in the Palaeozoic. The discovery of Silurian
pentastomids on marine ostracods suggests that early pentastomids used
invertebrate taxa (arthropods) as hosts (Siveter et al., 2015). This does, how-
ever, not preclude a mid-to-late Palaeozoic terrestrialization of pentastomids
during the vertebrate radiation on land, as Siveter et al. (2015) also pointed
out. Alternatively, an invertebrate route onto land cannot be entirely
excluded either. Further pentastomid fossil evidence, preferably still associ-
ated with their host, is needed to test these speculative hypotheses.
Figure 10 Holotype of Palaega nusplingensis from the Late Jurassic (late Kimmeridgian)
of Germany. This specimen is mentioned to be attached to the ventral side of a teu-
thoid squid. Scale bar 1 mm (Modified from Polz et al. (2006), pl. 3.2).
Fossil Crustaceans as Parasites and Hosts 269
subtle and highly unlikely to be detected in a fossil. Cysts and galls attributed
to infestation by parasitic copepods are known for some modern hard-
bodied host taxa such as scleractinian corals (Zibrowius, 1981; Dojiri,
1988; Buhl-Mortensen and Mortensen, 2004; Kim and Yamashiro, 2007),
echinoids (Stock, 1968, 1981, see also Section 3.1.2) and crustaceans
(Boxshall and Lincoln, 1983a), but not from others, such as the Mollusca.
No trace fossil attributed to a parasitic copepod has yet been reported
from soft-bodied hosts, such as polychaete worms or tunicates because of
the host’s low preservation potential.
3.3.2 Tantulocarida
About 35 species of tantulocaridans are currently known, either from para-
sitic stages attached to marine crustaceans, or from their free-living infective
larvae collected from the meiofauna in marine sediments from shallow
coastal waters to the deep-sea (Mohrbeck et al., 2010). Larvae are typically
about 100 mm in length. Whereas asexual adult females can attain a
maximum size of about 1.4 mm, sexual adults of both sexes are less than
1 mm in length (Boxshall and Lincoln, 1987; Huys et al., 1993). Their small
size and lack of a calcified cuticle indicate a poor fossilization potential.
3.3.3 Branchiura
Branchiuran fish lice are all external parasites of fishes (for example Figure 11),
with the exception of Dolops ranarum that uses freshwater amphibians as hosts.
Three genera, Chonopeltis, Dolops and Dipteropeltis, are exclusively freshwater
in distribution, while the largest genus, Argulus, occurs on both marine and
freshwater fishes. With the exception of Dolops that attaches by means of
paired clawed limbs, branchiurans typically attach to their host using paired
suckers derived from the maxillules (Gresty et al., 1993). They feed while
on the host, but adult females detach in order to lay eggs on submerged
hard substrates. In Argulus, the eggs hatch directly into an infective larva
equipped with cephalic swimming appendages that atrophy in subsequent
parasitic stages. Once erroneously treated as a subgroup of the Copepoda,
the Branchiura is now recognized as a distinct subclass of Oligostraca. No fos-
sils are known, but the estimated suggested sister-group relationship of Bran-
chiura with the Pentastomida (Sanders and Lee, 2010; Regier et al., 2010;
Oakley et al., 2013) suggests a Cambrian origin (see Section 3.1.5). The
feeding activity of branchiurans on the epidermis of their hosts can cause le-
sions including epidermal erosion, localized swelling and haemorrhaging
(Figure 11), but such traces, even if fossilized, are very general and would
be hard to attribute to a specific parasite taxon.
3.3.4 Ostracoda
Ostracods are a diverse modern group with a rich and extensive fossil record,
but the existence of parasitic forms is equivocal. A few ostracods live in close
symbiotic associations. Members of the podocopan family Endocytheridae,
for example, inhabit the burrows of freshwater decapods, but are probably
commensals according to Hobbs and Peters (1977), and will not be treated
further. It has also been argued that the myodocopan cypridinids Vargula
parasitica and Sheina orri are parasitic on the gills and in the nasal cavities of
various elasmobranch and actinopterygian fishes (e.g. Harding, 1966), but
Cohen (1983) considered that no myodocopids were truly parasitic and
she suggested that these ostracods were scavengers on injured or unhealthy
fish. Bennett et al. (1997) examined S. orri on the gills of a shark and docu-
mented local distortion of gill lamellae accompanied by tissue damage at all
sites of ostracod attachment, but they were unable to confirm that the ostra-
cods had ingested shark tissue. The ostracods were typically found in small
pockets between adjacent gill filaments. Bennett et al. (1997) concluded
that S. orri was parasitic, but such soft tissue features would have a low fossi-
lization potential.
3.3.5 Facetotecta
The adults of the Facetotecta are as yet unknown, but the free-swimming
larval stages are widely distributed in coastal marine waters. Facetotectan
larvae, the so-called Y-larvae, have their body enclosed within a bivalved
carapace (Glenner et al., 2008), but it is not calcified and no fossils are known
as a result. The hosts of the presumed parasitic adults are unknown.
272 Adiël A. Klompmaker and Geoff A. Boxshall
3.3.6 Thoracica
A scattered assortment of pedunculate thoracican barnacles has switched
from their ancestral suspension feeding to a parasitic mode of life. Anelasma
squalicola is the sole representative of the family Anelasmatidae and is typi-
cally found embedded in the skin of deep-sea sharks behind the dorsal fin
(Rees et al., 2014; Leung, 2014). A recent molecular clock study (Rees
et al., 2014) places the split of Anelasma from Capitulum at 126.5 Ma. Rhizo-
lepas species are parasitic on marine polychaete hosts (Day, 1939). Both
Rhizolepas and Anelasma have an atrophied suspension-feeding apparatus
and depend, at least in part, on nutrients absorbed from their host via an
embedded rootlet system. Heteralepadomorph barnacles typically live in as-
sociation with hosts, many inhabiting the gills of decapods, and they typi-
cally have reduced or absent valves, so their fossilization potential is
presumably lower than for typical barnacles. Most heteralepadomorph bar-
nacles are likely commensal, but Koleolepas species participate in a tripartite
symbiosis, living on gastropod shells inhabited by hermit crabs and carrying
sea anemones. They are typically attached beneath the pedal disc of the
anemone and feed by cropping its tentacles (Yusa and Yamato, 1999).
The shell plates are reduced or even absent in these thoracicans and their
fossilization potential is presumably lower than typical sessile or stalked
barnacles.
3.3.7 Malacostraca
The whale lice (Cyamidae) are dorsoventrally flattened amphipods found on
various cetacean hosts. Cyamids were traditionally treated as a wholly para-
sitic infraorder of the amphipod suborder Caprellidea (cf. Martin and Davis,
2001), but are now treated only as a family of parasites contained within a
much large clade (infraorder Corophiida) of free-living amphipods that
are predominantly detritivores (Myers and Lowry, 2003; Lowry and Myers,
2013). Whale lice cannot swim and lack any planktonic dispersal phase in
their life cycle; it is therefore presumed that infestation spreads only during
intraspecific bodily contact between host individuals.
Gnathiid isopods have free-living, non-feeding adults that inhabit ca-
vities in muddy sediments, in dead barnacles or in sponges, but the juveniles,
praniza larvae, feed on the blood of elasmobranch and actinopterygian fishes.
Engorged praniza larvae drop off their hosts between blood meals, rather as a
terrestrial tick. They have a very distinctive appearance, but their thin non-
calcified cuticle, which allows for their gorging feeding behaviour, is likely
to limit their fossilization potential.
Fossil Crustaceans as Parasites and Hosts 273
275
276 Adiël A. Klompmaker and Geoff A. Boxshall
ACKNOWLEDGEMENTS
We are very grateful to Kenneth De Baets and Tim Littlewood for the invitation to
contribute to this volume, for their useful comments, and the former also for useful literature
suggestions. We also thank John Jagt and Andrei Solovjev for providing useful literature;
G€unter Schweigert for useful literature and Figure 5(e), Barry van Bakel for discussion about
the specific placement of the Goniodromites specimen; Dieter Waloszek for Figure 8(a) and (c);
Sten Jakobsen for information on Echinocorys from Denmark; Rodney Feldmann for the sug-
gestion to work on this paper; Andreas Kroh for museum numbers for the Ernstbrunn spe-
cimens; Jesper Milan for the loan of a specimen from the Geomuseum Faxe; Roger Portell,
Sean Roberts and Alex Kittle for assistance with UF collections; René Fraaije for a museum
number of Oertijdmuseum De Groene Poort; Sancia van der Meij for Figure 6; Cristina
Robins for reading and commenting on part of the text. Mark Wilson and Joachim Haug
also kindly commented on earlier draft of this manuscript; their comments are much appre-
ciated. Our gratitude goes to all these persons. Furthermore, the following publishers,
Fossil Crustaceans as Parasites and Hosts 277
organisations, journals and persons are acknowledged for permission to reproduce various
images: PLOS ONE, The Paleontological Society, Springer, AAAS, Acta Geologica Polo-
nica, Contributions to Zoology, Micro Press, Rosenstiel School of Marine and Atmospheric
Science of the University of Miami, Dieter Waloszek, NRC Research Press, The Royal
Society of Edinburgh, The Palaeontological Association and Staatliches Museum f€
ur Natur-
kunde. This work was in part supported by the Jon L. and Beverly A. Thompson Endow-
ment Fund, an Arthur James Boucot Research Grant (Paleontological Society) and a
COCARDE Workshop Grant (ESF) to A.A.K. This is University of Florida Contribution
to Paleobiology 687.
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CHAPTER SEVEN
Contents
1. Introduction 292
2. Interpretations and Confidence 294
2.1 Problems of interpretation 295
2.2 Limits of confidence 297
3. Some Examples 298
3.1 A coralecrinoid association from the Mississippian 299
3.2 A growth deformity in a Mississippian crinoid 302
3.3 Epizoobionts infesting a Mississippian crinoid 304
3.4 Platyceratid gastropods infesting Upper Palaeozoic crinoids 306
3.5 Site selectivity of pits in echinoid tests, Upper Cretaceous 313
4. Discussion 319
5. Conclusions 323
Acknowledgements 323
References 323
Abstract
Recognizing the presence of a parasite and identifying it is a relatively straightforward
task for the twenty-first century parasitologist. Not so the pursuit of ancient parasites in
fossil organisms, a much more difficult proposition. Herein, Boucot’s seven-tiered
scheme of reliability classes is applied as a measure of confidence of the recognition
of putative parasitism in two echinoderm classes, Upper Palaeozoic crinoids and a
Cretaceous echinoid (high confidence is 1, low confidence 7). Of the five examples,
the parasitic(?) organism is preserved in only two of them. A zaphrentoid coral on
the camerate crinoid Amphoracrinus may have robbed food from the arms (Category
1 or 2B). A pit in what appears to be a carefully selected site on the disparid crinoid
Synbathocrinus is associated with a growth deformity of the cup (Category 4). Multiple
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.003 All rights reserved. 291
292 Stephen K. Donovan
pits in an Amphoracrinus theca are also associated with a deformed cup, but it is more
difficult to interpret (Category 4 or 7). Some specimens of the camerate crinoid
Neoplatycrinites have circular grooves or depressions posteriorly, presumably produced
by coprophagic/parasitic platyceratid gastropods (Category 1). Site selectivity of pits in
the echinoid Hemipneustes places them preferentially adjacent to respiratory tube feet
(Category 4). From these examples it is deduced that sparse infestations of borings or
epizoozoic organisms permit a more confident interpretation of organism/organism in-
teractions; dense accumulations, possibly following multiple spatfalls, mask such
patterns.
1. INTRODUCTION
Consider the task of the parasitologist. There may or may not be an
actual physical manifestation of the attentions of a parasite in a human being,
sheep, favourite pet dog or fish bought from a fishmonger, but its presence is
easily confirmed (or otherwise) using the wide range of biomedical, biochem-
ical and gene sequencing tools currently available. A stool is collected, blood
sampled or the fish cut open, and the hunt is on. Not only can the parasite be
identified, but its life cycle elucidated and its genes sequenced. In the twenty-
first century, all this can be done before lunch.
The hunter of fossil parasites, in my own case, in ancient echinoderms,
has none of these advantages. We may confidently speculate that many or
most parasites in ancient echinoderms left no evidence of their presence and
we will never know that they were ever there. Such navel contemplation is
the easy part. Commonly, where there is evidence of some interaction
between an organism, parasite or not, and the host, this is preserved as
some invasive structure (boring) into the echinoderm’s endoskeleton.
This may or may not be associated with a growth deformation of the
host. Borings without growth deformities must be regarded as not proven
parasitism, as such traces of interaction can occur after the death of the echi-
noderm, either soon after (Donovan, 2014; Donovan et al., 2014a) or mil-
lions of years later (Donovan and Lewis, 2011; Donovan, 2013). Associated
growth deformities show that the boring was engendered while the echino-
derm was alive and able to react to the invasion. What commonly does not
get preserved is the producer of the boring, which almost invariably lacks a
mineralized (and thus easily preserved) skeleton, so our interpretation of its
purpose (parasitism, or failed or successful predation, or something else)
must be made in ignorance of the simple fact, whodunit? The parasitologist
looks for parasites; the palaeoparasitologist works by necessity without
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 293
parasites, except for rare examples such as parasites with preservable skele-
tons such as parasitic snails (see below) or rare mineralized producers of pits
such as Phosphannulus M€ uller et al., 1974 (Welch, 1976; Werle et al., 1984;
Boucot, 1990, pp. 32e34).
So, what can we hope to achieve? As already intimated, many palaeon-
tological investigations of echinoderms and putative parasites begin with the
recognition of pits and boreholes in the echinoderm endoskeleton. Pits, bor-
ings and related structures in ancient substrates, such as tracks, trails, burrows
and coprolites, are trace fossils, representing evidence of ancient organic ac-
tivity. The study of trace fossils is ichnology. Only rarely is the producing
organism preserved adjacent to a trace except in certain settings, such as
the shells of boring bivalves which may be preserved in their borehole in
limestone (for example, Donovan and Jagt, 2013a). It is a mantra of ichnol-
ogy, the study of trace fossils, that a given organism may have produced a
range of trace fossils, representing different activities, and that a particular
morphology of trace fossil may have been produced by more than one group
of organisms, involved in similar activities. Trace fossils are given Latinized
binomens, but these do not refer to an organism per se, but to the sedimen-
tary structure that is the trace fossil. That is, their classification as sedimentary
structures is analogous to, but not part of, Linnean classification. It is a com-
mon ‘game’ in ichnology to speculate on the identity of producing organ-
isms, but it is incorrect to be too dogmatic about such assertions (Donovan,
2010). Pits in live echinoderms commonly produce growth reactions in the
endoskeleton, either inhibiting growth or causing swellings of various mor-
phologies, but these are pathologies of the echinoderm and are not part of
the trace fossil (Donovan, 2015). Further, trace fossils are named on
morphology and not substrate (Pickerill, 1994); for example, it was
suggested that borings in the echinoderm test that cause a range of growth
deformations should be referred to Tremichnus Brett, 1985, but all morpho-
logically similar small round holes are more correctly referred to Sedilichnus
M€ uller, 1977, a senior synonym of the widely used Oichnus Bromley, 1981
(Zonneveld and Gingras, 2014; see also Pickerill and Donovan, 1998;
Donovan and Pickerill, 2002).
If this sounds daunting, then add to this the confusion introduced by the
taphonomy, the study of the preservation of our infested echinoderm. There
are some organisms which have simple skeletons that are commonly pre-
served whole, such as gastropods, shelled cephalopods, tube-dwelling
worms, foraminiferans and stony corals, or disarticulated into just a few
pieces, including bivalve molluscs, brachiopods and ostracods. Most other
294 Stephen K. Donovan
Figure 1 Phthipodochiton thraivensis (Reed, 1911), BMNH G47258, lectotype, from the
Upper Ordovician of south-west Scotland. (After Donovan et al. (2010), Figures 2 and 3(c),
respectively.) (a) The specimen showing the valves of the chiton, preserved as natural
moulds and curving up from the lower centre to the right, past the label and towards
the top left. Scale bar represents 10 mm. (b) High-resolution X-ray microtomography
image of the complete gut contents (valves removed). Scale bar represents 1 mm.
296 Stephen K. Donovan
herein) from the Upper Ordovician Lady Burn Starfish Beds of south-west
Scotland. Mark Sutton and Julia Sigwart imaged the concealed structure of
this specimen using high-resolution X-ray microtomography (for full
details, see Donovan et al., 2010, pp. 935e936). This revealed a string of
shelly material preserved in a position that would correspond to the gut in
an extant chiton. The most prominent component of this string is a group
of nine crinoid columnals of more or less similar morphology that are inter-
preted as being derived from an individual of the camerate Macrostylocrinus
cirrifer Ramsbottom, 1961 (Donovan et al., 2011b), a common taxon at
Lady Burn.
Multiple lines of evidence indicate that this association is not a hydrody-
namic accumulation (Donovan et al., 2010). The columnals represent
ingested hard parts that were passing through the spiral gut of the chiton
at the time of death. Chitons are commonly thought of as simple grazers,
feeding on encrusting algae on rock surfaces, but many living chitons live
on animal matter (Fulton, 1975; Latyshev et al., 2004) and examination of
gut contents in living species shows a variety of food preferences, in some
species highly specialized (Sirenko, 2000).
Almost nothing is known regarding the predators and scavengers of
Ordovician crinoids (Meyer and Ausich, 1983; Baumiller and Gahn,
2003). Determination of predation and scavenging of Ordovician crinoids
has been mainly inferential, although there is suggestive evidence for pred-
atory decapitation in some disparids (Donovan and Schmidt, 2001), perhaps
a Category 3 association sensu Boucot (1990; see below). Category 1 asso-
ciations of crinoids as prey are rare throughout the fossil record, and the
example discussed herein is the oldest and the most unexpected.
Crinoid columnals may have been consumed by this chiton due to pre-
dation, scavenging or ingestion of sediment rich in crinoid bioclasts. The last
seems unlikely; unless the chiton was particularly unselective, it would more
likely have harvested organic matter from finer grained sedimentary parti-
cles. Predation or scavenging is thus more probable, but equally plausible.
The speculation of predatory versus scavenging behaviour may appear trivial
in this example, but it is analogous to the sometimes heated discussions of the
habits of Tyrannosaurus rex Osborn, 1905 e predator or scavenger e which
have engendered a diverse correspondence (for a recent discussion, see
Erickson, 2014). Whichever, such crinoidivory in this ancient Scottish
mollusc is unexpected, being unknown from extant chitons; like T. rex,
we lack a modern analogue to provide an answer.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 297
Of the two examples given above, I would place the Ordovician crinoi-
divorous chiton in Boucot’s Category 2A and would change it to Category 1
if a modern analogue was discovered. Predation on the arms of Palaeozoic
crinoids is best assigned to Category 4 or, perhaps, 5A.
3. SOME EXAMPLES
The structure of this paper was determined by personal preference. It
could have written as the echinodermal parts of Conway Morris (1981)
brought up-to-date, a revision of the parasitism parts of various reviews of
echinoderm taphonomy (such as Meyer and Ausich, 1983; Donovan,
1991b) or a parasitism paper modelled on the review of predation on cri-
noids by Baumiller and Gahn (2003). Rather, I have something a little
different in approach from all of these, preferring to focus on a few selected
examples from my own experience rather than a review that attempted to be
too broad and, in consequence, lacked detail.
Actual examples of putative parasitic infestations of fossil echinoderms
are desirable at this stage to demonstrate something of the range of evidence
available and how it has been interpreted. Most of the examples lean heavily
on my own research, which explains why they preponderantly concern my
beloved crinoids. I consider it preferable to discuss the familiar in this review
than try to spread the text too thinly across the many extinct and extant clas-
ses of echinoderms. My intention here is to demonstrate broad principles
that can be extrapolated to a reader’s own investigations.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 299
compactional strain. Although the position of the coral on the crinoid could
be merely coincidence, the unusual width, which we interpret as growth
rather than postmortem deformation (Figure 2(b)), of the AB interray is
reminiscent of the sorts of deformities that are known to be induced in
echinoderms by interactions with encrusting organisms (Meyer and Ausich,
1983).
All these lines of evidence support the supposition of an original
biotic relationship between the host crinoid and its attached coral in
life; that is, the living coral was an epizoozoan (sensu Taylor and Wilson,
2002) on the living crinoid. In the Mississippian of the British Isles, it is
more common to find crinoids, particularly their columns, encrusted by
colonial tabulate corals than by either solitary or colonial rugose corals
(see, for example, Donovan and Lewis, 1999). The close association of
A. gilbertsoni with a solitary rugose coral would thus be worthy of comment
under any circumstances, but it is the position with respect to the crinoid
calyx and the presumed life orientation of the latter that excites particular
comment. In attaching to the calyx of a crinoid, the solitary coral has
gained an advantage from its elevated position would have been above
the turbid bottom layers of the water column, so water currents would
have been essentially sediment free. The importance of feeding is further
emphasized by the corallite being hard against the B ray arm in the AB
interray. The A ray is anterior and, if A. gilbertsoni formed a parabolic filtra-
tion fanlike modern rheophilic crinoids (Macurda and Meyer, 1974), the
coral would have been directed into the clean water currents, being posi-
tioned up-current from the anal pyramid. The situation in close contact
with the B ray arm is at least suggestive that the coral may have actively
harvested food with its tentacles from the adoral groove of the crinoid’s
arm. Although obviously speculative, this supposition is supported by the
unusual width of the AB interray, a growth deformity which probably
resulted from a reaction to the coral and prevented it from interfering
with the feeding activity of the A ray arm, too. The available evidence is
at least highly suggestive that this coral was both a filter feeder and a parasite
on the crinoid.
Reliability: Category 1 or 2B. Boucot (1990, p. 9) stated (Category 2B)
that ‘With organisms belonging to extinct higher taxa [such as rugose corals
and camerate crinoids] functional analysis of behavior from morphology is
clearly less reliable’. But other groups of crinoids and stony corals are extant
and well known, so Category 1 is at least plausible.
302 Stephen K. Donovan
Figure 3 BMNH E71430, Synbathocrinus conicus Phillips, 1836. (a, b) Camera lucida
drawings of the dorsal cup and proximal column. (After Donovan (1991a), Figure 2.)
Scale bar represents 5 mm. (a) EA interray central (compare with Figure 2(e)), showing
the position of the boring. (b) DE interray central, showing how the oral surface slopes
down towards the region of infestation, presumably a growth reaction to the distur-
bance. Key: RR ¼ radial circlet; BB ¼ basal circlet; COL ¼ most proximal part of column.
(c) Schematic oral view based on BMNH E71430. (After Donovan (1991a), Figure 3.)
Carpenter rays (AeE) indicated, corresponding to the positions of the arms; X is the po-
sition of the anal series (¼ posterior). Small arrows mark positions of cryptic B:B:R plate
triple sutures; large arrows mark positions of prominent R:R:B plate triple sutures. Key:
1 ¼ in the same position of the anal series; 2 ¼ adjacent to the anal series; 3 ¼ distant
from the anal series; * ¼ position of boring. Current flow would have been from the top
of the page.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 303
Figure 4 Multiple Sedilichnus paraboloides (Bromley, 1981) infesting the dorsal cup of
the Lower Carboniferous crinoid Amphoracrinus gilbertsoni (Miller in Phillips, 1836),
BMNH EE8728. (After Donovan et al. (2006), Figure 1.) (a) Base of dorsal cup, D-ray to-
wards top of page. (b) Enlargement of (a), showing how pits are concentrated on plates,
not crossing sutures. (c) Enlarged lateral view of (mainly) dorsal cup, E-ray central,
showing sub-horizontal arrangement of closely spaced pits. (d) Theca in lateral view,
same orientation as (c). Note absence of pits above the line of the arm facets. Specimen
whitened by ammonium chloride. Scale bars represent 10 mm (a, d) or 5 mm (b, c).
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 305
avoided; these sutures are sunken between the plates, so it is probable that
the small difference in height between sutures and plate centres was impor-
tant to the producers. This strongly supports a suggestion that they were fil-
ter feeding. Interestingly, S. paraboloides is distributed on the lower part of
the theca through 360 , and is apparently not selective with respect to the
life orientation of the crinoid, there being no obvious preference for anterior
(A-ray) or posterior (CD-interray) (but see Section 4, ‘Discussion’, below).
Pits are close packed, but in only very few instances overlap, suggesting that
this represents a gregarious accumulation of an organism that thrived on
elevated calcareous substrates, rather than successive pits formed by one or
a few individuals (compare with Donovan and Lewis, 2010).
Reliability: Category 4 (compare with Section 3.2) or 7, ‘. so highly
speculative as to have little reliability at all .’ (Boucot, 1990, p. 9). The
sloping base of the theca is analogous to the example of S. conicus, above,
in which a single pit is interpreted as engendering the aberration. In the pre-
sent example, with the theca heavily covered by borings below arm level,
there seems little connection between a growth deformity and an infestation
through 360 . The pits would have gained advantages attached to an elevated
cup, but any evidence that the association may have been parasitic is masked
by the dense accumulation of pits. The pit producer may have been conspe-
cific with that in Section 3.2; the specimens are from the same locality.
that is typically bulbous anteriorly (Figure 5(b)), but, viewed from the side
(BC and DE interrays), the CD interray is flattened and slopes down to the
basals, slightly protruding just below the level of the arms. The radials of the
CD interray bear a prominent sub-circular groove, c. 8.9e9.7 mm in diameter,
situated below the periproct and more on the D than C radial (Figure 5(a)); a
comparable structure was illustrated by Wanner (1916, pl. 99, Figure 1(a)).
The central area is flattened on the C side and onto the D, but otherwise
slightly raised. Sutures between the radials are poorly apparent in this region.
Outside the groove, the test is sculpted by two (D) or three (C) sub-concen-
tric raised ridges. These structures do not encroach onto the basal circlet. This
suggests that they were not produced by the shell of the epizoozoic snail
(sensu Taylor and Wilson, 2002), which would not have been so careful as
to avoid adjacent plates in this manner. Rather, they are more likely a stereom
response to gastropod infestation (compare with, for example, Grygier, 1988;
Eckert, 1988; Grygier and Nomura, 1998; amongst many others).
The other three thecae (Figures 5(ceg) and 6(aec)) have a similar
structure to each other, albeit a little different from RGM B9. These three
thecae are distinctly truncated posteriorly (Figures 5(d, f) and 6(c); as is
also RGM B9). The radials in the CD interray form a depressed region
below the periproct, like an inverted triangle with bowed sides, with the
lateral extent determined by the positions of the arm facets. These depressed
regions are approximately parallel-sided to convex below the arms (Figures
5(c, g) and 6(a)), becoming constricted towards the base of the thecae.
The plate triple junction between the C and D radials, and the supporting
CDeDeDE basal are depressed. RGM T.3851[1] (Figure 6(aec)) has the
most rounded depressed region with a shallow, sub-circular groove appar-
ently extending around the periprioct. Comparable structures are not
apparent on RGM T.4439[1] and ST. 32842[1] (Figure 5(c) and (g)).
Discussion: The coprophagic/parasitic relationship between the platy-
ceratid gastropods, and Palaeozoic crinoids and blastoids has been recognized
for over 140 years. It persisted from at least the Middle Ordovician to
Permian (Bowsher, 1955; Conway Morris, 1981, p. 499; Meyer and Ausich,
1983, pp. 401e403, Figure 5; Baumiller, 1990, 1993; Boucot, 1990;
Donovan, 1991b, pp. 251e252; Gahn and Baumiller, 2003, 2006; amongst
others). The mollusc is commonly preserved surmounting the anal opening
(Figure 6(def)) where it produces no stereom overgrowth (but sometimes a
‘scar’), presumably because the platyceratid is vagile. Bowsher (1955) consid-
ered the platyceratidepelmatozoan association to be obligate commensalism,
the gastropod being a coprophage, feeding on the echinoderm’s excrement.
310 Stephen K. Donovan
Yet Rollins and Brezinski (1988) demonstrated that crinoids with platycera-
tid infestations tend to be smaller than those without associated gastropods,
thus indicating that the association was detrimental to the host, that is, para-
sitic. The platyceratid may have utilized the detritus concentrated by the
filtration fan of the crinoid. Further, Baumiller (1990) demonstrated that
some platyceratids drilled into the crinoid tegmen, which further suggests a
parasitic association (see also Baumiller, 1993; Baumiller et al., 1999).
One of the common associations by platyceratids in the Late Palaeozoic
was with the platycrinitid monobathrid camerates. The Permian of West
Timor has provided some of the youngest specimens to demonstrate this
interaction (e.g. Wanner, 1937, pl. 11, Figures 7 and 8; Baumiller et al.,
2004, pp. 393e395, Figure 1; Donovan and Webster, 2013). Specimens
from Timor discussed by Webster and Donovan (2012) either preserved
(or, at least, preserved evidence of) platyceratids on the tegmen or along
the radial summit of the platycrinitids Platycrinites Miller and Neoplatycrinus
Wanner (Figure 6(def)). The specimens described above do not retain
any platyceratid shells, but instead show evidence of different patterns of
infestation in the CD interray of the theca first discussed by Donovan and
Webster (2013). In these associations, the crinoid thecae show distinct modi-
fied morphologies, presumed to have been formed in response to the
gastropod infestation; whether these changes also altered the feeding capa-
bilities of the crinoids is equivocal. Part of the fascination of this association
is its age; ‘Hard substrate communities are poorly known in the Permian’
(Taylor and Wilson, 2003, p. 48).
The circular structures (Figure 5(a)) and depressed areas (Figures 5(c, g)
and 6(a)) of abutting C and D radials on the Neoplatycrinus thecae described
above are interpreted to be the results of the crinoids reacting to infestations
by platyceratid gastropods. Unlike other examples known from the Permian
of West Timor (Wanner, 1937; Baumiller et al., 2004; Webster and Dono-
van, 2012; Figure 6(def) herein), these snails were attached subapically in
the CD interray rather than apically on the tegmen or adjacent to it. This
was undoubtedly, at least in part, due to the posterior position of the peri-
proct of Neoplatycrinus. Note that these patterns of infestation are differently
positioned, either below the periproct, or extending between the C and D
arms to include the periproct.
The two broad morphologies of CD interray described are thus indica-
tive of differing positions chosen by the infesting gastropods and reactions
engendered by their hosts. Most obviously, the circular scars indicate the
homing positions of the producing gastropods (compare with Boucot,
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 311
1990, Figure 8). These scars are prominent external modifications of the cri-
noid’s endoskeleton. They may be the result of abrasion by the edge of the
aperture of the gastropod shell or chemical etching (Bromley, 2004, p. 463),
irregular growth of stereom as a reaction to this by the crinoid or, most prob-
ably, a combination of all of these. For example, RGM B9 (Figure 5(a)) has
both a deeply depressed, circular groove (situated below the periproct;
contrast with Figure 6(a)), but also concentric raised ridges outside it. The
former is presumably produced (mainly) by the gastropod, the latter by
the crinoid, raised above the level of the adjacent theca. It is considered
unlikely that these concentric structures represent occupancy by successively
larger platyceratids through time, although they could reflect the growth of
a single individual gastropod.
Despite these modifications, the gross, slightly inflated morphology of
the crinoid theca is retained, except posteriorly. The gastropod must have
stood proud of the surface of the theca, presumably giving the CD interray,
an inflated appearance in life. Whether the gastropod remained in this
position at least semipermanently is unknown, but these modifications to
the crinoid suggest that it was at least likely. Figure 6(def) shows a platycer-
atid gastropod from this locality so that its size and shape e low, moderately
broad and cap-like e may be compared to the other illustrations herein; its
position on the theca is in sharp contrast to where snails must have infested in
Figures 5 and 6(aec).
The round groove in the radials in the CD interray is a trace fossil that is
close in morphology to Lacrimichnus Santos et al., 2003, based on Neogene
gastropod attachment scars. Jagt (2007) identified an older Lacrimichnus? isp.
on a barnacle plate from the upper Maastrichtian of the type area. Lacrimich-
nus? isp. is also applied as an ichnotaxonomic name to the round scars pro-
duced by Permian capuliform platyceratid gastropods, such as the specimens
illustrated herein and by Boucot (1990, Figure 8). This would rescue such
trace fossils from the limbo that referring to them as circular grooves engen-
ders (compare with discussion by Donovan and Pickerill, 2004, p. 483).
Although produced by acorn barnacles rather than gastropods, the ichnoge-
nus Anellusichnus Santos et al., 2005, is broadly similar to Lacrimichnus, but
typically has an undulating outer furrow.
The second morphology described above involves the CD interray of
the crinoid being depressed, more so than in RGM B9, but without
obvious homing scars except, possibly, faintly in RGM T.3851[1]
(Figure 6(a)). Commonly, the test of uninfested Neoplatycrinus is bulbous,
conical or bowl-shaped. Infested tests retain this geometry in anterior
312 Stephen K. Donovan
view (Figures 5(e) and 6(b)), but, in other views, there is a marked flattening
posteriorly (Figures 5(d, f) and 6(c)), giving the test a prominent anteriore
posterior asymmetry, although remaining bilaterally symmetrical along a
mirror plane AeCD (that is, anterioreposterior). Such flattening is only
developed in the CD interray, that is, posteriorly. This is interpreted as a
different expression of infestation by a platyceratid.
The depressed CD interray produces a marked change in thecal gross
morphology, but, in life, the shell of the coprophagic platyceratid would
have been positioned here, presumably filling the depression. The shells
of these gastropods are low and cap-like (Bowsher, 1955; Boucot, 1990,
Figures 10e13; Webster and Donovan, 2012, Figures 1(aec) and 2(deh);
Figure 6(def) herein). It may have been that the gastropod in part ‘restored’
the gross morphology of the theca with its shell by filling the depressed area.
That is, with a shell in place in the depressed CD interray, the combined
morphology of crinoid þ gastropod may have approximated that of an
uninfested theca. The same may be true for the (less depressed) RGM B9.
This interpretation is speculative, but could be tested by a carefully defined
experiment in a flume tank.
If this supposition is accepted as possible, the question must be asked why
was it advantageous to host, coprophage or both? The gross morphology of
the crown presumably played a part in ensuring water currents for feeding
reached the arms (Jefferies, 1989). If, as I suggest, the platyceratid ‘filled
the gap’ in the theca, made as a response by the crinoid to the snail’s presence
in the CD interray, then the more or less restored hydrodynamics of the
crown would have engendered more efficient suspension feeding by the
crinoid. This would have resulted in greater production of faeces which,
in turn, would have benefitted the gastropod. But, overall, the relationship
was probably more parasitic than mutualistic.
Such a relationship was more than casual, and the modifications of the
theca that favoured this crinoidegastropod association were probably devel-
oped early and retained throughout life. The two morphologies of CD
interray seen in Neoplatycrinuseplatyceratid associations are indicative of
two different patterns of infestation. The depressed CD interrays (particu-
larly Figures 5(c, g) and 6(a)) suggest a mode of infestation in which the
gastropod extended between the C and D arms, perhaps covering the
periproct. This arrangement suggests a long-term relationship between
crinoid and gastropod, the former showing large thecal modifications to
accommodate the snail.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 313
Figure 7 Holasteroid echinoid Hemipneustes striatoradiatus (Leske, 1778) and the pits
Sedilichnus excavatus (Donovan and Jagt, 2002), all Upper Cretaceous (Maastrichtian)
of the Netherlands and Belgium. (After Donovan and Jagt (2002, Figures 2(a, c), 3(a, b)
and 5(aee).) (a, c, d) NHMM MK 4689. (a) Apical view, showing holotype (arrowed)
and paratype borings. (c) Holotype (arrowed) with two paratypes. Scale bar represents
5 mm. (d) Paratype with outline partly controlled by adjacent ambulacral column. Scale
bar represents 5 mm. (b) NHMM 699, right lateral view, paratypes; note the linear ar-
rangements of some groups of borings. (e, i) NHMM RN 452b, profile (test external sur-
face to left) and internal surface. (f, h) NHMM RN 452c, profile (test external surface to
left) and internal surface. (g) NHMM RN 452a, internal surface. Scale bars represent
10 mm unless stated otherwise.
00162 (Figure 8(aee)) is from the base of subunit IVf-6 of the Meersen
Member, Maastricht Formation, at the former Blom quarry, Berg en Terblijt
(for locality map, see Donovan et al., 2011a, Figure 1). NHMM MA 0234-1
(Figure 8(feh)) is from the same subunit (IVf-6), but from the nearby
Ankerpoort-Curfs quarry, now defunct, near Geulhem.
Description: (Based on Donovan and Jagt, 2013b, pp. 113e114) The
test of H. striatoradiatus, NHMM RZ 00162, was used as a substrate by a va-
riety of encrusting and boring invertebrates. The oral surface bears three
attached pycnodonteine oyster valves in close association; a cheilostome
bryozoan colony in the depressed region anterior of the peristome; more
than three poorly preserved spirorbid worm tubes; and a slot-like, figure-
of-eight boring aperture just posterior of the peristome, probably Caulostrep-
sis isp. (Figure 8(b)). Spirorbid worms occur at or just above the ambitus;
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 315
Figure 8 Holasteroid echinoid Hemipneustes striatoradiatus (Leske, 1778) and the pits
Sedilichnus excavatus (Donovan and Jagt, 2002), all Upper Cretaceous (Maastrichtian)
of the Netherlands and Belgium. (aee) NHMM RZ 00162. (After Donovan and Jagt
(2013b), Figure 1.) (a) Apical surface with the positions of four pits, S. excavatus, marked
by asterisks (*). The numerical designation of ambulacra (Roman numerals, IeV) and
interambulacra (Arabic numerals, 1e5) is provided as an explanation of the notation
used in the text. (b) Oral surface showing episkeletozoans (oysters, bryozoan colony,
spirorbids) and annelid boring, Caulostrepsis isp. (c, e) Two views of S. excavatus in
ambulacrum 4. (d) Sedilichnus excavatus in ambulacrum V; compare rounded outline
to (c, e). (feh) NHMM MA 0234-1. (After Donovan and Jagt (2013b), Figure 2.) All oblique
views of the apical surface. (f) Ambulacrum II (right anterior) central with closely group-
ed pair of S. excavatus pits. (g) Ambulacrum IV (left anterior) right of centre, with one
poorly developed S. excavatus in the upper part of the ambulacrum and two further
pits, in close association, in interambulacrum 3 (left anterior). (h) Ambulacrum V (left
posterior) right of centre with S. excavatus between the columns of pore pairs; other
specimens are in interambulacrum 4 (left lateral). An encrusting oyster, situated poste-
riorly, partly overgrows a S. excavatus (far right). Specimens uncoated. Scale bars repre-
sent 10 mm.
316 Stephen K. Donovan
each have one associated pit (Figure 8(g) and (h), respectively). In two inter-
ambulacra, pits are vertically one above the other (Figure 8(g) and (h)); in the
posterior interambulacrum (5; Figure 8(h), far right, oblique view) a pit sits
on the interradial suture at about mid-height of the test, about as far as it is
possible to be situated away from an ambulacrum, and partly overgrown by
an oyster.
Discussion: Donovan and Jagt (2002) erected the ichnospecies Oichnus
(now Sedilichnus) excavatus on the basis of locally common infestations of pits
in the late Maastrichtian echinoid H. striatoradiatus (Leske). Ample evidence
was presented to indicate that this association occurred while the echinoid,
which probably lived more or less epifaunally, was alive, most particularly by
the growth of internal blisters within the test and beneath the pits (Donovan
and Jagt, 2005, pl. 1, Figure 2; Figure 7(eei) herein). Sedilichnus excavatus was
diagnosed as ‘Circular to elliptical, non-penetrative Oichnus, almost invari-
ably with a broad, high, raised central boss. Aperture of boring overhanging,
and walls concave’ (Donovan and Jagt, 2002, p. 69).
The type series and related material of S. excavatus included pits in
numerous tests of H. striatoradiatus, some of which were densely infested;
most notably, Donovan and Jagt (2002, p. 69, Figure 2(c)) counted ‘at least
61 individual borings’ on NHMM JJ 699. Despite this wealth of material,
there was not any strong indication of site selectivity, although some pits
did occur in linear associations (Figure 7(b)) and most infested the test
supra-ambitally.
The two analogous specimens of H. striatoradiatus described above,
although relatively sparsely infested by S. excavatus, provide stronger indica-
tions that the settling behaviour of the infesting organism was site selective.
All encrustations on these tests are interpreted to have occurred after the
death of H. striatoradiatus (¼ episkeletozoans sensu Taylor and Wilson,
2002). In life, the tests would have been protected by both densely packed
spines and pedicellariae which would have prevented such varied infesta-
tions. A holasteroid such as H. striatoradiatus would not have been a deep
burrower; rather, it would have lived epifaunally, possibly furrowing
through the sediment at the surface. The occurrence of a partial marginal
(subanal) fasciole under the periproct points to such a mode of life. Thus,
the oral surface would have been in intimate contact with the sediment, pre-
cluding infestation of the oral surface of either specimen by oysters, bryo-
zoans, or spirorbid or serpulid annelids (Figure 8(b)). Further, with the
exception of S. excavatus, the tests preserve no evidence of the growth of
the echinoids being adversely affected by any boring or attachment. Thus,
318 Stephen K. Donovan
also successfully infested other areas of the test. All S. excavatus in Figure 8 are
above the mid-height of the test and, thus, were presumably above the sedi-
ment surface in this shallowly furrowing echinoid. None of the pits shows a
particularly strong association with the well-developed respiratory tube feet
situated posteriorly on each of the ambulacra of interest. We suggest, tenta-
tively, that this pattern of infestation may have placed the producers of
O. excavatus in advantageous positions to feed on plankton, anterior of the
tube feet on an echinoid moving slowly across the seafloor. The function
that the respiratory tube feet performed for the producer of O. excavatus is
uncertain, but may have been protective in part.
Reliability: Category 4. ‘For some types of behavioral evidence there is
an even larger degree of uncertainty about the maker of this evidence. This is
particularly true for many trace fossils’ (Boucot, 1990, p. 9).
4. DISCUSSION
The echinoderms are a promising group of fossils with which to inves-
tigate the nature of biotic reactions because the endoskeleton may produce
growth deformities of various types if infested in life. Other reviews of para-
sitism on echinoderms have tried to do too much in a restricted space (such
as Kowaleski and Nebelsick, 2003, pp. 294e295, on echinoids); I have
aimed to be expansive, but selective. There are some good examples that
I have chosen to ignore because they are well covered elsewhere (such as
various entries for parasitism on echinoids in Boucot, 1990). Five specific
examples are given in this essay, but none belong to the typical swollen
deformity for which the echinoderms are so well known (Figure 9) and
which have been determined as parasitic infestations by many authors
(Moodie, 1918). Although such structures are locally common, I suggest
that they are more difficult to interpret than some of the examples discussed
in detail herein. Certainly, some modern parasites produce identifiable galls
and cysts in echinoid spines, asteroid arms, ophiuroids discs, and crinoid pin-
nules and cirri (see, for example, Grygier, 1988). But similar pits and swell-
ings may be the result of embedment by an organism that is merely seeking
elevation above the substrate. It will gain an advantage, but is it parasitism
(Zapalski, 2011)?
Pits in the endoskeleton in crinoids and blastoids (such as Figure 9(a)) are
difficult to interpret. A crinoid column would provide very little nourish-
ment, so a bored fossil pluricolumnal should best be interpreted as an
320 Stephen K. Donovan
(a) (b)
Figure 9 (a) Pentagonocyclicus (col.) sp., RGM 544 426 (After Donovan and Lewis (2010),
Figure 2.), perforated by three pits. Wenlock Edge, Shropshire [NGR SO 588 980], England;
Much Wenlock Limestone Formation, Lower Silurian (Wenlock, Homerian). Note the
irregular outline of the pluricolumnal, due to swelling, and the large size and irregular
outline of the pit in the centre; the other two pits, including one at the top, are more
circular and assigned to Sedilichnus paraboloides (Bromley). Specimen whitened with
ammonium chloride for photography. (b) A strongly swollen pluricolumnal, RGM 791
727, in which the living crinoid grew over an encrusting coral. (After Donovan et al.
(2014b), Figure 4(g).) Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England; lower
Viséan (¼ upper Chadian) Salthill Cap Beds, Bellman Limestone Member. Scale bars
represent 10 mm.
that apparently were exploiting part of the crinoid’s feeding capability sensu
lato and one example of a bored echinoid where site selectivity suggests an
interaction in life with the ambulacra. In two examples we actually know (or
at least have a very strong suspicion of) the producing organism. The inter-
action between a solitary stony coral and a crinoid theca (Section 3.1) in the
Mississippian is an unexpected one. There are strong indications that the
coral was interfering with the crinoid’s feeding, including its situation at
the level of the base of the crinoid arms and the unusual width of this inter-
ray, suggesting that growth of the crinoid was minimalizing the interference
by the parasite. What this interference was is the subject of informed spec-
ulation and was most probably as simple as robbing food from the adoral
grooves of the arms.
The coprophagic/parasitic association of platyceratid gastropods and
Palaeozoic crinoids is one of the best known organism/organism associations
in the fossil record, being based on many hundreds of specimens worldwide.
The circular scars on or below the anal pyramid in a posterior position on
Neoplatycrinus from Timor, Lacrimichnus? isp. (Section 3.4), provide data
on the nature of these associations additional to than commonly available,
that is, with the snail astride the anal pyramid on the apical surface.
It is apparent from the above examples that sparse infestations provide a
more cogent tale of organic interactions than dense infestations, which are
more likely to confuse the issue. The crinoid theca with multiple pits
through 360 (Section 3.3) preserves excellent evidence of biotic interac-
tions e the pit-forming organisms could not settle on those parts of the theca
that could be swept clean by the tube feet of the arms and the theca itself
shows a growth deformity (Figure 4) e but was any of it parasitism? To
use this example as an excuse for speculation, as in the title of this paper,
perhaps the multiple pits in this specimen represent more than one spatfall.
All pits are of similar size and spacing, but they could have formed in a pro-
gression of multiple reproductive seasons if the producing organism had a
much shorter life history than an adult crinoid. The pits of dead producers
may even have been recycled by juvenile settlers. But if the earliest pit(s)
was solitary or sparse and concentrated on one side of the cup, it may
have produced the sloping base as a growth reaction analogous to that in
Section 3.2 (Figures 2(def) and 3). Later, perhaps larger spatfalls were
excluded from making new pits where the originals were now inhabited
by larval ‘squatters’ because of biological constraints determined by the
size of the adult organism (¼ regular spacing of pits) and avoidance of sunken
plate sutures (Figure 4(b) and (c)). If we think in terms of a progressive
322 Stephen K. Donovan
5. CONCLUSIONS
‘The fossil record contains many examples of the interactions that
occurred between organisms . evidence of interactions may be . cryptic
or difficult to interpret, none more so than the evidence of ancient para-
sitism’ (Littlewood and Donovan, 2003, p. 136). The evidence provided
by the endoskeletons of fossil echinoderms may be particularly rich, but
difficult to interpret. Too rarely is there a good answer to basic questions;
what was the parasite; what was being parasitized exactly and why infest
an innutrious structure like a crinoid stem when the real tasty guts of the an-
imal was in the cup? Some structures that give the superficial impression that
they were formed by parasites, such as deformities in the crinoid column, are
difficult to explain and probably do not represent parasitism per se. Most, at
least, probably represent dwelling traces, the pit or gall produced looking
like parasitism, but being little removed behaviourally from an encruster
attached to the outside of the test which would rarely, if ever, be thought
to be truly parasitic. Dense infestations may mask patterns that are apparent
in weakly infested specimens. And, in the absence of the producing organ-
ism in many examples, which is represented by its trace fossil, a sedimentary
structure, we are forced to speculate not just on whodunit, but also what it
was that they were doing.
ACKNOWLEDGEMENTS
I thank the editors, Tim Littlewood (The Natural History Museum, London) and Kenneth
De Baets (Friedrich-Alexander Universit€at, Erlangen), for inviting me to contribute to this
volume. I also thank my co-authors of the papers that form the backbone of this contribution
for their collaboration and collegial companionship, namely John Jagt (Natuurhistorisch
Museum Maastricht), David Lewis (the Natural History Museum, London), Paul Kabrna
(Barnoldswick, Lancashire) and Gary Webster (Washington State University, Pullman).
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CHAPTER EIGHT
Contents
1. Introduction 330
2. Colonial Animals 331
3. Putative Parasites of Fossil Colonial Animals 333
3.1 Recognition of parasitism in fossils 333
3.2 Symbiotic intergrowths and bioclaustrations 334
3.2.1 Caunopores 335
3.2.2 Rugose corals and stromatoporoids 336
3.2.3 Chaetosalpinx and other bioclaustrations 336
3.2.4 Cornulitids and colonial hosts 338
3.2.5 Celleporaria and Culicia 338
3.2.6 Pyrgomatid barnacles 339
3.3 Galls 340
3.4 Borings 340
3.5 Supposed parasites of graptolites 341
4. Fossil Colonial Animals as Parasites 341
5. Discussion 342
Acknowledgements 343
References 343
Abstract
Colonial species occur in a wide range of aquatic invertebrates, some having excellent
fossil records, notably corals, bryozoans and graptolite hemichordates. In contrast to
unitary animals, colonial animals grow by adding repetitive modules known as zooids.
The ability of colonies to endure partial mortality and the typically plastic growth of
benthic colonial species facilitates the formation of macrosymbiotic associations,
some of which may be parasitic. However, as with unitary fossils, it is notoriously
difficult to identify whether the symbioses are parasitisms (þ/) or mutualisms
(þ/þ). Intergrowths between host colonies of stromatoporoid sponges, corals or bryo-
zoans, and skeletal or soft-bodied symbionts are particularly common in Ordoviciane
Devonian shallow-water deposits. Soft-bodied symbionts in such intergrowths are
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.002 All rights reserved. 329
330 Paul D. Taylor
1. INTRODUCTION
Coloniality has evolved on multiple occasions in invertebrates
(Blackstone and Jasker, 2003). All colonial animals are aquatic and most
are marine, including corals and bryozoans (see Hughes, 1989 for a good
introduction to colonial and other clonal animals). Colonial animals are
characterized by a modular construction, comprising repetitive clonal units
called zooids. New zooids are budded to bring about colony growth,
which is usually indeterminate and plastic: different colonies belonging
to the same species may grow for different lengths of time and in different
patterns, achieving a range of sizes and shapes.
Relatively little is known about the parasites of colonial animals living
today (e.g. Hill and Okamura, 2007; but see Hooper, 2005 for sponges,
and Boero and Bouillon, 2005 for cnidarians). These can range from unicel-
lular microparasites e some of which might be closely related with mutual-
istic endosymbionts (Okamoto and McFadden, 2008) e to multicellular
macroparasites including helminths (Aeby, 2003), molluscs (e.g. Lorenz,
2005) and various arthropods (e.g. Duffy, 2003; Boxshall, 2005; Grygier
and Hoeg, 2005; L€ utzen, 2005). In some cases, sponges and cnidarians can
be important parasites of colonial organisms themselves (e.g. Hooper,
2005; Boero and Bouillon, 2005). Some of the most-studied endoparasites
of extant colonial organisms are myxozoans parasitizing freshwater bryozoans
(Okamura et al., 2015), which have not yet been reported from the fossil
record. Myxozoans are now considered to be cnidarians and impact their
bryozoan hosts by reducing colony growth, causing periodic castration and
zooid gigantism (Hartikainen and Okamura, 2012; Hartikainen et al., 2013).
Even less is known about parasites of ancient animal colonies found in
the fossil record. Direct fossil evidence of microbial parasites in colonial
Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms 331
2. COLONIAL ANIMALS
The zooids in animal colonies are clonal and primitively have iden-
tical morphologies. However, zooidal polymorphism occurs in some
species, with zooids showing functional and morphological specialization,
e.g. for sexual reproduction or defence. Zooids of colonial species are typi-
cally reduced in size relative to individuals of related solitary animals. Small
zooid size is usually paralleled by a reduction in complexity.
Animal colonies divide into two basic ecological groups e benthic
and pelagic e both represented in the fossil record. Benthic colonial
species are found among the following phyla: Cnidaria, Bryozoa,
Entoprocta, Urochordata and Hemichordata. Anthozoan cnidarians are
often colonial, including many scleractinian and rugose corals and all
tabulate corals, as are the majority of hydrozoan cnidarians. Bryozoans
are an exclusively colonial phylum, while a few species of entoprocts
(¼kamptozoans) are colonial. Many urochordates, such as ascidians, and
pterobranch hemichordates are colonial. In addition, key aspects of the
growth and life history of species belonging to Porifera are closer to colo-
nial than to unitary organisms (see Simpson, 1973; but cf. Ereskovskii,
2003), and for the purpose of this review sponges are included among colo-
nial animals. Benthic colonies are usually sessile, fixed permanently to a
substrate such as a rock, shell or seaweed, although a few have evolved
automobility and others move by virtue of being attached to mobile
animals. A significant proportion of benthic animal colonies have bio-
mineralized skeletons, typically of calcium carbonate, and as a result they
are common components of the fossil record, especially in shallow-water
marine deposits.
332 Paul D. Taylor
the effective unit of natural selection (at least in colonies that are not frag-
mented). In the case of colonial species with biomineralized or resistant
organic skeletons, clear evidence of the presence of macrosymbionts may
be preserved in the fossils. Indeed, Tapanila (2008) stated that the majority
of marine symbioses in the Palaeozoic involved colonial animals. As discussed
below, however, ascertaining the nature of the interaction between the sym-
bionts (i.e. parasitism or mutualism) in fossil material is a major challenge.
(3) detriment to the host. Among the 33 tabulated associations, they found
very few instances in which all of these criteria were satisfied, and none of
these involved colonial symbionts. Probably the best-supported example
of a fossil parasitism is the Ordovician to Permian symbiosis between crinoids
and nutrient-stealing platyceratid gastropods, for which a detrimental impact
on the host crinoids can be inferred from the fact that infested crinoids are
smaller than noninfested examples. No comparable reduction in host colony
size seems yet to have been demonstrated in any fossil symbioses involving
colonial species. Palmer and Wilson (1988) argued that any interaction pro-
moting a growth response of a symbiont may be energetically costly, and
therefore potentially parasitic, as is any infestation that eliminates zooids of
a colonial animal, but this cost may of course have been balanced or sur-
passed by unknown advantages of living with a symbiont.
Middle Devonian. A similar pattern seems to pertain for other symbiotic in-
tergrowths too.
3.2.1 Caunopores
The best known intergrowths involve ‘caunopores’ (Figure 2(a)), which are
branching, tubular symbionts found embedded in the skeletons of stromatop-
oroid sponges (Stel and Stoep, 1982; Mistiaen, 1984; Kershaw, 1987; Young
and Noble, 1989; Darrell and Taylor, 1993; Zhen, 1996). Caunopores are
common in the Silurian and Early to Middle Devonian, particularly in reefal
settings. Although the tubular symbionts are usually assumed to be syringop-
oroid tabulate corals, some examples have a different skeletal microstructure
and are of smaller diameter than is typical for such corals. If caunopores
were indeed corals (or other cnidarians), then possible disadvantages to the
host stromatoporoids may have been offset by the protection afforded by
the stinging nematocysts of the corals. However, the net cost or benefit to
the host stromatoporoids is unclear, placing a question mark over whether
this symbiosis is a parasitic or mutualistic association.
particularly interesting for two reasons. Firstly, the presence of the coral
brings the pyrgomatids into symbiosis with bryozoans with which they
are not otherwise associated. Secondly, the barnacles smother the individual
corals on which they settle, prompting lateral budding and quite possibly
entailing a significant cost, suggesting that the pyrgomatids in this instance
were parasites of the corals.
3.3 Galls
Diverse modern parasites induce their hosts to form galls (e.g. Rouse, 2005),
sometimes in colonial hosts. For example, pycnogonid arthropods may
inhabit galls in gorgonian and scleractinian hosts (Staples, 2005), corallio-
philid gastropods can form galls in various cnidarian groups (Lorenz,
2005), and gall-inducing copepods are known to occur in stylasterine
hydrozoans (Zibrowius, 1981). Coralliophilids have a fossil record dating
back to the Eocene, with the oldest example inhabiting galls apparently
being a species of Coralliophila found in the coral Cladocora from the Early
Oligocene of SW France (Lozouet and Renard, 1998). Voigt (1959) intro-
duced the genus Endosacculus for galls in Cretaceous octocorals considered to
have been induced by the presence of ascothoracican cirrepedes (see also
Voigt, 1967).
3.4 Borings
A plethora of macroboring organisms are capable of penetrating into the
hard skeletons of colonial animals (see Bromley, 2004; Wilson, 2007).
Benthic colonies with calcareous skeletons, particularly corals (e.g. Wilson
et al., 2014), have been targets for diverse macroboring organisms (see
Wilson, 2007) since the Cambrian. Glynn (1997) reviewed bioerosion of
coral reefs, in which sponges, annelids, crustaceans, sipunculans and molluscs
are the dominant macroendoliths. While the great majority of these animals
bioerode dead coral skeletons, some attack living tissues and may be agents
of partial mortality and therefore are potentially parasites of the host corals.
When dense or large relative to the host colony, macroborers may weaken
the skeleton, resulting eventually in breakage, detachment from the substrate
and colony mortality (see Highsmith, 1981). However, the impact of
macroborers on still-living colonial hosts is less clear and is potentially com-
plex. While bored colonies may need to divert resources to strengthening
and be otherwise disadvantaged, pointing to a parasitic relationship,
Kleemann (1994) made the interesting suggestion for bivalves boring into
Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms 341
scleractinian corals that after death the decaying tissues of the bivalve could
provide an extra source of nutrition for the coral host.
Microendoliths are also commonly found in the calcareous skeletons of
benthic fossil colonies. For example, Kolodziej et al. (2012) described pre-
mortem microborings into scleractinian corals of Early Cretaceous age.
These include traces attributed to autotrophic chlorophyte algae as well as
those of probable fungal origin. Like the macroborings described above,
both of these groups of microendoliths are capable of weakening the skele-
tons of the host corals. By analogy with extant analogues (see Golubic et al.,
2005), the fungal microendoliths may additionally have attacked the coral
polyps, raising the possibility of a parasitic relationship.
clionid sponges that are capable of undermining the skeleton beneath the
polyps of living corals as they compete for space with their hosts (L opez-
Victoria et al., 2006). There is a rich fossil record of sponge borings (ichno-
genus Entobia) into corals and other biotic substrates (see Bromley, 2004),
which warrant further study in this context.
Berkowski and Zapalski (2014) recently described examples of the tabu-
late coral Hamarilopora minima that encrusted the stems of living crinoids in
the Early Devonian of Morocco. Loss of stem flexibility as a result of encrus-
tation would have impacted the host crinoid negatively, suggesting that the
association was parasitic. Similar associations have been reported involving a
wide range of epibionts, both colonial and unitary, on crinoid stems else-
where in the fossil record (see references in Berkowski and Zapalski, 2014).
5. DISCUSSION
Benthic colonial invertebrates today are hosts for numerous microen-
dosymbionts. These include multifarious bacteria in sponges (Vogel, 2008),
the dinoflagellate Symbiodinium (zooxanthellae) in reef-building corals (e.g.
Baker, 2003), and the bryostatin-producing bacteria of the bryozoan Bugula
neritina (e.g. Davidson et al., 2001; Linneman et al., 2014). Direct fossil
evidence for such microsymbionts is scant and determining which are para-
sitic can be difficult. Exceptions are the boring microsymbionts mentioned
above, which leave traces (ichnofossils) in the skeletons of their hosts.
Whereas microsymbionts are typically cryptic and difficult to study in
fossil animal colonies, macrosymbionts offer opportunities for future
research, especially when both partners have fossilizable mineralized skele-
tons that are intergrown. In cases where the symbiosis is not obligatory, it
should be possible to make a comparative study of colonial hosts with and
without symbionts. The comparative sizes of hosts could be compared
and a parasitic association inferred if hosts with symbionts were smaller
than those without. In addition, relative growth rates in hosts with and
without symbionts could be compared in cases where the hosts have clear
morphological or isotopic growth banding, again permitting inference of
parasitisms if the presence of symbionts lowered the growth rate of the
host colonies. Given the abundance of symbiotic intergrowths in fossil ani-
mal colonies in some geological sections (e.g. Silurian of Gotland), there is
clearly scope for studying the temporal dynamics of the associations if a suf-
ficient amount of material can be collected for rigorous analysis.
Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms 343
ACKNOWLEDGEMENTS
The final version of this paper benefitted from the comments of the reviewers e Beth
Okamura, Leif Tapanila, Olev Vinn and Miko1aj Zapalski e to whom I am extremely
grateful.
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CHAPTER NINE
Palaeoparasitology e Human
Parasites in Ancient Material
jo*, 1, Karl Reinhardx, Luiz Fernando Ferreira*
Adauto Arau
*Fundaç~ao Oswaldo Cruz, Laborat orio de Paleoparasitologia, Rio de Janeiro, RJ, Brazil
x
School of Natural Resources, University of Nebraska, Lincoln, NE, USA
1
Corresponding author: E-mail: adauto@ensp.fiocruz.br
Contents
1. Introduction e Parasitism 350
2. Humans and Parasites 352
3. Palaeoparasitology 353
4. Recommended Material and Techniques for Microscopic Examination in 363
Palaeoparasitology
4.1 Light microscopy techniques 363
4.2 Counting remains under the microscope 365
4.2.1 Analysis of sediments 365
4.2.2 Coprolites in mummies 367
4.3 Molecular techniques applied to palaeoparasitology 368
4.3.1 Molecular diagnosis 368
5. Parasite Finds in Human Archaeological Remains 369
5.1 Ascaris lumbricoides and Trichuris trichiura 369
5.2 Hookworms 371
5.3 Enterobius vermicularis 372
5.4 Diphyllobothrium sp. 373
6. Other Parasites: Parasites of Animals Found in Human Coprolites; Parasites in 374
Prehistoric Asia
7. Origin and Evolution of Trypanosomatids in Humans and the Paradigm Shift 375
from Results in Palaeoparasitology
8. Ectoparasites 376
9. Conclusions 377
Acknowledgements 378
References 378
Abstract
Parasite finds in ancient material launched a new field of science: palaeoparasitology.
Ever since the pioneering studies, parasites were identified in archaeological and palae-
ontological remains, some preserved for millions of years by fossilization. However, the
palaeoparasitological record consists mainly of parasites found specifically in human
archaeological material, preserved in ancient occupation sites, from prehistory until
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.03.003 All rights reserved. 349
350 Adauto Ara
ujo et al.
closer to 2015. The results include some helminth intestinal parasites still commonly
found in 2015, such as Ascaris lumbricoides, Trichuris trichiura and hookworms, besides
others such as Amoebidae and Giardia intestinalis, as well as viruses, bacteria, fungi and
arthropods. These parasites as a whole provide important data on health, diet, climate
and living conditions among ancient populations. This chapter describes the principal
findings and their importance for knowledge on the origin and dispersal of infectious
diseases.
1. INTRODUCTION e PARASITISM
This chapter uses the broad definition of parasitism. The concept
ranges all the way from mobile fragments of genetic material, both transmis-
sible and non-transmissible, up to higher plants and vertebrate animals
(Trager, 1988; Ara ujo et al., 2003; Araujo and Ferreira, 2014; Schmid-
Hempel, 2011; Ewald and Swain Ewald, 2014). The definition considers
the complex parasiteehosteenvironment system and its interdependent
relations, where changes or alterations in one component can influence
the others. This is an ecological focus to parasitism, since both the macro-
environment and microenvironment induce changes and influence rela-
tions. The study of parasitism should be based on ecology. These
relations consider the classifications between symbionts, commensals,
mutualists and parasites, among others, as a single concept called parasitism.
This unified approach allows a better understanding of parasitic diseases in
their evolutionary process.
The broad definition of parasitism is not new. Brazilian parasitologist
Samuel B. Pessoa, in the first edition of his book Parasitologia Médica in
1945, already reminded parasitologists that ‘parasitism, commensalism, and
symbiosis are categories created by our spirit, all displaying characteristics
of the same general laws’ (Pessoa, 1951, p. 5).
When German scientists Karl Georg Friedrich Rudolf Leuckart and
Heinrich Anton de Bary independently created the concepts of symbiosis
and parasitism, respectively (both in 1879), they made no mention of dis-
eases, benefits or harm that could result from the relationship between spe-
cies. The same connotation was already revisited by various other authors,
including French parasitologist Emile Brumpt (Brumpt, 1913). Beginning
with the first editions of his book, Brumpt highlighted the fact that para-
sitism and symbiosis converged in a single concept, since beings that were
considered parasites and those viewed as symbionts or commensals could
all cause harm or benefit to their hosts.
Palaeoparasitology e Human Parasites in Ancient Material 351
intestinal content. However, when raising the temperature alters the envi-
ronment, the parasites invade the tissues and the snake can die. Barrow
and Stockton (1960) conducted experiments in eight species of snakes
infected with this parasite under different temperatures, from 13 C to
25 C. No lesions were observed at lower temperatures, although the
amoebae continued to be isolated in culture. However, at a temperature
25 C, the snakes presented lesions, and even those that did not show
lesions at low temperatures became sick at higher temperatures.
When Carlos Chagas described the signs and symptoms of American
trypanosomiasis, later named Chagas disease in his honour, the first case of
an infected patient was a child with an acute manifestation of the disease,
in whom trypanosomes were found in the bloodstream (Coura, 1997).
The child was Berenice, and she died at 79 years of age from a cause other
than Chagas disease. For years she attended congresses during which she was
examined without presenting severe symptoms, but it was always possible to
isolate Trypanosoma cruzi from her peripheral blood during her >70 years of
life (Salgado, 1980).
3. PALAEOPARASITOLOGY
Palaeoparasitology is the study of parasites found in archaeological or
palaeontological material (Ferreira, 2014). This branch of palaeopathology
and parasitology opened new avenues for studying the evolution of the
health-disease process in the human species, as well as in other hosts
(Mitchell, 2013). Palaeoparasitological findings provide a consistent source
for palaeoepidemiology by revealing the presence of infection in a given
archaeological context and the possible consequences for the emergence
or disappearance of infectious diseases in prehistoric populations.
Franco-British physician and microbiologist Sir Marc Armand Ruffer
was the pioneer of palaeoparasitology. Ruffer studied Egyptian mummies
in the early twentieth century, developing rehydration techniques for
mummified tissues, allowing their visual examination in histological sections
with staining used in routine histopathology. He found calcified and well-
preserved Schistosoma haematobium eggs in the kidney tissue of a mummy
dated 3200 BC (Ruffer, 1910). This was the first parasite find in ancient
human material, shedding light on haematuria in Egypt, which had been
described in ancient texts but not previously proven. Although Ruffer’s
article does not show an image of the egg, his diagnosis was confirmed by
German parasitologist Arthur Looss and Scottish pathologist Dr Alexander
R. Ferguson, Ruffer’s faculty colleagues at the Cairo School of Medicine.
354 Adauto Ara
ujo et al.
Figure 1 Archaeological layers at the Site of Toca do Boqueir~ao da Pedra Furada, 1986
(Piauí state, Brazilian northeast).
Palaeoparasitology e Human Parasites in Ancient Material 355
Figure 2 The Italian archaeologist Fabio Parenti excavating a coprolite in the Site of
Toca do Boqueir~ao da Pedra Furada, 1986 (Piauí state, Brazilian northeast).
this field of knowledge (Ferreira et al., 1979). At the time, there was little
research production in the area, with just a few articles on parasite finds pub-
lished by North American authors in important journals or even mimeo-
graphed copies (Samuels, 1965; Heizer and Napton, 1969; Fry, 1970) and
reviews on analyses in human coprolites in the United States, especially
focussing on diet and food remains (Wilke and Hall, 1975), while England
and a few other European countries featured studies on parasites in ancient
material (Gooch, 1972; Jones, 1982). As with the first studies in these coun-
tries, Brazilian researchers developed collaborations with archaeology teams,
since the entire palaeoparasitological analysis hinged on painstaking
Figure 3 Archaeological layer showing the coprolite evidenced in the Site of Toca do
Boqueir~ao da Pedra Furada, 1986 (Piauí state, Brazilian northeast).
356 Adauto Ara
ujo et al.
2012; Reinhard and Bryant, 2008). Parasitologists recover data that have been
unique in fulfiling archaeological research goals (Reinhard, 1992a,b).
The vitality of archaeological populations has been an inherent theme in
archaeology that was codified in ‘bioarchaeology’, which focuses on the
analysis of skeletal human remains (Buikstra and Beck, 2008). By compara-
tive analysis of bone pathology, bioarchaeologists assess the relative adaptive
success of past populations. Because skeletons were the source of data, evi-
dence of infectious disease was often limited to nonspecific indicators of
stress, periosteal bone reaction and porotic hyperostosis. The evidence for
actual infectious organisms comes from analysis of sediments associated
with skeletons (Fugassa, 2014) or from coprolites (Jiménez et al., 2012).
A long-standing archaeological hypothesis was that ancient hunter-
gatherers, relative to later agricultural peoples, were free of infections
(Diamond, 1987). Testing this hypothesis was a research design of many
coprolite recovery excavations in the 1960s and 1970s. To a large degree,
archaeology and ethnography support this hypothesis (Reinhard, 1988;
London and Hruschka, 2014). The low prevalence of parasitism led to a
desire to explore the basis for hunter-gatherer avoidance of parasitism.
One aspect is related to the presence of medicinal plants in the diet
(Reinhard, 1985). Beyond the use of anthelmintics among hunter-gatherers,
small band size, diffuse population and frequent movement of camps helped
reduce parasite infection (Reinhard, 1988). The agricultural revolution was
recognized by archaeologists as an abrupt change in the human condition
that gave rise to a dramatic increase in infection (Diamond, 1987). The
bone pathology, porotic hyperostosis, generally exhibits a higher prevalence
among agricultural skeletal series. Porotic hyperostosis is exhibited as ‘spongy’
expansions of the cranial diploe coinciding with an erosion of the outer cra-
nial table of the parietals and occipital of effected skulls. The aetiology of the
pathology was long debated and finally resolved by Walker et al. (2009) who
concluded that porotic hyperostosis lesions ‘are a result of the megaloblastic
anemia acquired by nursing infants through the synergistic effects of depleted
maternal vitamin B12 reserves and unsanitary living conditions that are
conducive to additional nutrient losses from gastrointestinal infections around
the time of weaning’ (Walker et al., 2009, p. 119). The fluctuations of
porotic hyperostosis have been a key issue in archaeology, especially in the
Americas, that now can be asserted to have an origin in large part to parasitism
(Reinhard, 1992a,b). Jiménez et al. (2012) underscored Walker et al. (2009)
model in their characterization of extreme helminth prevalence at a site in
Durango, Mexico, the skeletons from which exhibited porotic hyperostosis.
Palaeoparasitology e Human Parasites in Ancient Material 359
peoples of the coast of northern Chile. The data suggest that El Ni~ no events
caused fluctuation in coastal fish resources that in turn led to varying suscep-
tibility of fishers to fish tapeworm infection. But drought in another part of
the hemisphere is reflected in the archaeoparasite record. The excavation of
Antelope House in Canyon de Chelly, Arizona, revealed the hundreds of
years of prehistory of a Puebloan village that terminated with the Great
Drought that lasted from 1276 and continued through 1299 (Morris,
1988). Parasite prevalence and diversity increased at the end of the occupa-
tion as people aggregated at the last villages with persistent water sources
(Reinhard, 2008). This was mirrored at Elden Pueblo near Flagstaff, Ari-
zona, that showed the highest concentration of helminth eggs in the final
occupation strata of the site. Parasitism peaked around the time of
abandonment.
The emergence and control of parasitism in historic times, and relation
of ethnicity to infection, is a topic among historic archaeologists. Charles
Fisher and his colleagues directed excavations of latrine sediments, as well
as sediments from yards, streets, drains and other contexts to reconstruct
the emergence and control of parasitism in Albany, New York. The analysis
of hundreds of samples showed the introduction of geohelminths (soil-
transmitted helminths) with the original Dutch colony. Infection peaked
in the late 1700s and early 1800s but began to abate in the late 1800s as
drainages were covered and as water projects brought clean water into
the city. Interestingly, the water projects were designed first to provide
water for fighting fires. By the turn of the twentieth century, faecal-borne
parasitism was controlled in both the elite and poor neighbourhoods
(Fischer et al., 2007).
The longer-term emergence and control of faecal-borne geohelminths
have been a source of research for many analysts working in Europe (Reinhard
and Pucu, 2014). This research falls into the archaeological construct of
palaeoepidemiological transitions. There were two palaeoepidemiological
transitions. The first was associated with the Neolithic Revolution, which
separated the ancient hunter-gatherer prehistory with the agricultural period.
The Neolithic Revolution is thought to have resulted in a rise in infectious
diseases. The Industrial Revolution is thought to represent reduction of
infectious disease and a rise of occupational disease. This scheme was tested
by Reinhard and Pucu (2014) for both Europe and the Americas. Interest-
ingly, the palaeoparasitology record of Europe bears out the hypothesized
changes. The Neolithic Revolution is accompanied by the ubiquitous pres-
ence of whipworm and roundworm (Ascaris lumbricoides) infections. By
Palaeoparasitology e Human Parasites in Ancient Material 361
Roman times, these parasites are found wherever archaeologists sample lat-
rines, burials or mummies. This transition, strangely, does not exist in the
Americas where geohelminths, although introduced long in prehistory,
never take hold as ubiquitous parasites among agriculturalists. The reasons
for a relatively geohelminth free American prehistory have yet to be eluci-
dated. Reinhard and Pucu (2014) suggest that Native American medicinal
treatments, settlement patterns, faecal avoidance and lower population den-
sity may have helped maintain post-agricultural revolution parasitism at low
levels. In addition, the European use of human faeces as fertilizer and depen-
dence on the humoral theory of disease may have contributed to spread of
infections and failure to effectively treat infections (Reinhard and Pucu,
2014).
When ideal archaeological preservation can be combined with historical
documents, very detailed reconstruction of infection patterns can be recon-
structed. Kim et al. (2013) and Seo et al. (2014b) accomplished this for the
city of Hansung, the capital area of the Joseon Dynasty, which is now
located within Seoul, South Korea. By examining legal documents relating
to the distribution of night soil (latrine contents) from the city to farmers,
and the economic interdependence between major cities and nearby farm-
lands, researchers discovered that the night soils produced in a major city
were recycled by farmers as fertilizers for fields. With that night soil, soil-
transmitted parasites were spread on the fields to contaminate vegetables
that were then marketed back to the city. High levels of geohelminth infec-
tion were an unavoidable result of this legally defined recycling process.
Flood-deposited sediments in the city that were washed in from farm fields
during periodic torrential rains in ancient times show that parasite eggs were
indeed contaminants of the fields.
Remarkable preservation of Joseon Dynasty mummies provides fasci-
nating evidence of food-borne fluke infection. Eighteen Joseon mummies
have been studied for parasites as reviewed by Seo et al. (2014a,b). Four spe-
cies of trematodes were found. Two species, Clonorchis sinensis (Chinese liver
fluke) and Metagonimus yokogawai, are similar in that they are transferred by
the consumption of fish. A total of six mummies were infected with one or
both of these flukes, five with C. sinensis and three with M. yokogawai. Para-
gonimus westermani, a lung fluke, was found in four of the mummies. Its final
intermediate host includes species of freshwater crabs. Finally, oyster con-
sumption was a source of infection with Gymnophalloides seoi, an intestinal
fluke. Two mummies were found to be positive for eggs of this parasite
(Shin et al., 2012). In total, 11 of 18 Joseon mummies, representing the elite
362 Adauto Ara
ujo et al.
of this society, were infected with one or more species of fluke and under-
scores the importance of uncooked meat in Ancient Korean diet.
The studies summarized above present a sampling of the ‘big picture’
issues that have been addressed by cooperation of parasitologists and archae-
ologists. Other studies provide ‘vignettes’ of ancient parasitism. Such studies
focus on brief archaeological moments or give a detailed glimpse of humane
parasite interactions. Kristjansd
ottir and Collins (2011) excavated cemeteries
from Skriðuklaustur, a medieval monastic site and hospital used between AD
1493 and 1554 in Eastern Iceland. During this brief period, eight individuals
died with hydatid cysts from eight of 160 burials recovered. The eight burials
were clustered together in one part of the cemetery, which suggests that they
were recognized as a specific symptom complex and were treated as such.
A cyst in one of the skeletons was 17 cm in diameter. The cysts are a result
of infection with Echinococcus granulosus. It was probably introduced in Ice-
land sometime after the late ninth century and became endemic by AD
1200. Although some of infected individuals lived with other diseases,
including syphilis, the authors note that ‘they seem to have first been buried
according to this shared condition and not relative to any of the other iden-
tified illnesses or age. The indications are that this ailment may have been
recognised in medieval Iceland as having its own classification and perhaps
requiring distinct treatment if not in life, at least in death’ (Kristjansdottir
and Collins, 2011, p. 485). The implication is that hydatid cyst disease
was recognized early in Icelandic medical history. Thus, this excavation pro-
vides a ‘vignette’ of a symptom complex recognized by monastic scholars.
Latrines provide other ‘vignettes’ of human parasitism. The diet and
parasitism of a single Roman Centurion were presented by Kuijper and
Turner (1992). Along with a great diversity of pollen and seeds of spices
and food, the eggs of intestinal parasites were found. The authors report
that ‘many thousands’ of eggs were present per cubic centimetre. Whip-
worm and Ascaris lumbricoides were most common, but taeniid eggs, consis-
tent with the genera Taenia or Echinococcus, were also present. Thus, the
dietary habits and intestinal infections of a single officer were evidenced in
the latrine sediments. Another vignette of parasites carried by pilgrims comes
from a thirteenth century latrine in the city of Acre, Israel. At that time, Acre
was part of the Frankish Kingdom of Jerusalem. The fish tapeworm (eggs
consistent with Diphyllobothrium latum) was identified. The authors note
that fish tapeworm was also found in the latrine block of the Hospital of
St John. The Order of St John was a religious order that cared for crusaders
and pilgrims. The presence of fish tapeworm eggs in a crusader period latrine
Palaeoparasitology e Human Parasites in Ancient Material 363
in the Levant indicates that infected pilgrims from northern Europe travelled
to Acre with active fish tapeworm infections (Mitchell et al., 2011).
This sampling of studies reflects the popularity of parasitology as a tool
for archaeologists (Reinhard, 1992a). The productive collaboration of
archaeology and parasitology will continue to grow in regional distribution
and in the development of new research questions beneficial to both fields.
(b)
(d)
Figure 4 Lutz’ sedimentation technique steps e (a) mixing the sediment, after rehyd-
rating the coprolite or the sediment; (b) pouring the rehydrated sediment through the
gauze to the conical glass jar; (c) after 2e4 h, the sedimentation process is completed;
(d) preserved macroresidues; (e) collecting the sediment for microscopic analysis.
Palaeoparasitology e Human Parasites in Ancient Material 365
5.2 Hookworms
The hookworms that most frequently parasitize humans, Ancylostoma duode-
nale and Necator americanus, contributed to the debate on transpacific contacts
or migrations of Asian populations to the Americas (Ara ujo et al., 1981,
1988, 2008; Ferreira and Ara ujo, 1996; Reinhard et al., 2001). The two spe-
cies have probably accompanied the human host since the first human
migrations from Africa (Ferreira et al., 2014). Like Ascaris lumbricoides and
Trichuris trichiura, the hookworms that parasitize humans dispersed
throughout the globe in regions that allowed maintenance of their life cycle.
However, hookworm egg finds are rare in archaeological material from
Europe and Africa, but are more frequent in both South America and North
America (Gonçalves et al., 2003). These parasites require passage through the
soil for approximately two weeks until their soil cycle is complete, from the
elimination of the eggs in the feces until the release of infective larvae. These
changes require temperatures >20 C and moist soil. Only then are the
larvae capable of penetrating the host and continuing their life cycle. Under
microscopy, the eggs are nearly indistinguishable, but A. duodenale eggs are
slightly smaller (46.4e77.5 23.5e61 mm) than those of N. americanus
(54.2e85.3 30e54 mm), based on statistical analyses (Rep, 1963).
Due to these biological characteristics, the humans that crossed the
Bering land-and-ice bridge could not have introduced hookworm infection
by this route. Prehistoric transpacific migrations or contacts by seafaring
372 Adauto Ara
ujo et al.
Asian populations to the Americas were thus hypothesized (Ara ujo et al.,
1981, 2008; Montenegro et al., 2006).
Infections with high parasite burden, associated with deficiencies in the
human host’s health and nutrition, cause severe cases of ancylostomiasis,
with intense anaemia due to intestinal blood loss through faeces, oedema
of the lower limbs, paleness, weakness, and other signs and symptoms. Texts
by naturalists and chroniclers from the colonial period in the Americas
include descriptions consistent with ancylostomiasis, with such details as
generalized oedema and the habit of eating dirt or clay among indigenous
people (Sousa, n.d.; Ara
ujo et al., 1981). Geophagy is one of the symptoms
of hypochromic microcytic anaemia, associated with hookworm infection
and deficient iron intake, especially in malnourished children and young
people and pregnant women with iron deficiency.
between individuals. More serious clinical cases only occur rarely, caused by
bacterial invasion of the lesions provoked by the itching. Transmission of this
helminthic infection is facilitated by the agglomeration of hosts and is easily
diagnosed in day care centres, nursing homes, and other locations that can
facilitate transmission directly from host to host or by dispersal of eggs in
circulating air or contaminated food, in addition to autoinfection by eggs
carried directly from hand to mouth or the simple penetration of larvae
hatched from the eggs deposited in the perianal region. Prehistoric infection
in North America was very well documented by Hugot et al. (1999), study-
ing this parasite among the Ancestral Puebloans that inhabited the dwellings
built of clay and wood in the rock shelters and caves in the canyons, which
were clustered and with intercommunications. There were also collective
rooms with directed air circulation, which facilitated aerosol transmission
of the parasite’s eggs.
(Ara
ujo et al., 1983). It was later shown that the infection was quite common
in the different human groups that inhabited the region (Reinhard and
Urban, 2003).
8. ECTOPARASITES
This group of parasites includes different classes of arthropods and
some other invertebrates. The most common classes in humans are Insecta
and Arachnida (mites and ticks). Some of these ectoparasites, such as head
lice Pediculus humanus, are also shared with nonhuman primates, and thus
likely infested humans since the prehominids (Araujo et al., 2003; Mitchell,
2013). According to Reed et al. (2004) and Raoult et al. (2008), lice have
parasitized primates for some 25 million years, and when chimpanzees
diverged from humans 6 million years ago, genus Pediculus remained in
both species. This parasite has been found in Egyptian mummies and in
archaeological sites in North America and South America. Infestation
became as widespread in the Andean region (Arriaza et al., 2012; Dutra
Palaeoparasitology e Human Parasites in Ancient Material 377
et al., 2014) as in medieval Europe, where the hairdos of the nobility were
veritable breeding grounds for lice (Fornaciari et al., 2009). The same was
true of the refined hairdos of the Tiwanaku: when the Incas arrived as con-
querors of other Andean empires, they levied ‘lice taxes’, now interpreted
as a way to control infestation or simply as a form of human head count
(Souffez, 2001).
There is extensive research on the origin and evolution of pediculosis.
Reed et al. (2004) and Raoult et al. (2008) provided important evidence
on the antiquity and evolution of this parasite infection in humans, with
the oldest finding thus far in the Americas (Ara ujo et al., 2000). Studies
on the meaning and impact of mass lice infestations were conducted in
Andean populations (Dutra et al., 2014; Arriaza et al., 2012, 2013b), where
exceedingly well-preserved mummified bodies are found, including well-
preserved hair.
The preservation of eggs or lice is so extraordinary that they were found
on human shrunken heads from the Jívaro, an indigenous group on the
border of Brazil with Ecuador, dated to the colonial period and the Second
Empire in Brazil, in the nineteenth century (Ara ujo et al., 2005). Eggs of
ectoparasites have in rare cases even been found on dinosaur feathers or
mammal hair preserved in amber (e.g. Martill and Davis, 1998; Poinar,
2014). Both lice (Order Phthiraptera) and fleas (Order Siphonaptera), which
currently parasitize bird and mammals, can be traced back to the Cretaceous
at least (see the review in Nagler and Haug, 2015).
9. CONCLUSIONS
Palaeoparasitology contributes new data to knowledge on the origin
and evolution of parasitic diseases. It situates e in time and space e the pres-
ence of infection in human groups that have already disappeared, situating
their distribution and tracing prehistoric migrations across the continents
through parasites preserved in the occupation sites.
Palaeoparasitology has also contributed greatly to studies on the evolu-
tion of parasites and their hosts. Despite previous claims that parasites do
not leave fossils (e.g. Dorris et al., 1999), parasite finds have become frequent
in remains from extinct animals dating back millions of years (Littlewood
and Donovan, 2003; Poinar, 2014), particularly those preserved in amber
and in coprolites found in palaeontological sites (Poinar and Boucot,
2006; Dentzien-Dias et al., 2013). It is thus possible to study the presence
378 Adauto Ara
ujo et al.
of parasites millions of years old and their relations with current species, as in
the case of Oxyurid and Ascarid eggs found in cynodonts, dated 240 million
years BP (Silva et al., 2014; Hugot et al., 2014). This group of parasites has
persisted to 2015, sharing a long evolutionary history with its hosts.
The development and growing interest of research groups in palaeopar-
asitology have stimulated progress in knowledge on parasiteehosteenviron-
ment relations, reinforcing the ecological approach that should be
encouraged in studies on parasites and hosts.
ACKNOWLEDGEMENTS
The research received funding from the Brazilian National Council on Scientific and Tech-
nological Development (CNPq), Coordinating Division for the Advancement of Graduate
Studies (CAPES) in the Science without Borders programme (Ciencia sem Fonteiras), Carlos
Chagas Filho Rio de Janeiro State Research Foundation (FAPERJ) and InovaENSP (Sergio
Arouca National School of Public Health).
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CHAPTER TEN
Contents
1. Introduction 390
1.1 Sources of evidence 391
1.2 Survival of intestinal parasite eggs over archaeological time 392
1.3 Prevalence of parasites in the past 393
2. Parasites in Europe Prior to the Medieval Period 395
3. Medieval Period 397
3.1 Sanitation 398
3.2 The fishing industry 403
3.3 Farming animals 404
3.4 Detecting migrations 406
3.5 Reduction in some zoonotic parasites 408
3.6 Ectoparasites in medieval Europe 408
3.7 Medical history of medieval parasites 410
4. Conclusion 412
References 413
Abstract
Parasites have been infecting humans throughout our evolution. However, not all
people suffered with the same species or to the same intensity throughout this
time. Our changing way of life has altered the suitability of humans to infection by
each type of parasite. This analysis focuses upon the evidence for parasites from archae-
ological excavations at medieval sites across Europe. Comparison between the patterns
of infection in the medieval period allows us to see how changes in sanitation, herding
animals, growing and fertilizing crops, the fishing industry, food preparation and migra-
tion all affected human susceptibility to different parasites. We go on to explore how
ectoparasites may have spread infectious bacterial diseases, and also consider what
medieval medical practitioners thought of parasites and how they tried to treat them.
While modern research has shown the use of a toilet decreases the risk of contracting
certain intestinal parasites, the evidence for past societies presented here suggests that
the invention of latrines had no observable beneficial effects upon intestinal health.
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.001 All rights reserved. 389
390 Piers D. Mitchell
This may be because toilets were not sufficiently ubiquitous until the last century, or
that the use of fresh human faeces for manuring crops still ensured those parasite
species were easily able to reinfect the population.
1. INTRODUCTION
The last 10,000 years has seen dramatic changes in the way humans
lived and the kinds of parasites infecting them. As a species we are thought
to have originated about 200,000 years ago in east Africa. Early humans
started to migrate around the planet from around 60,000 BP (before present)
and they had started to settle in Europe by 30e40,000 BP (Pasternak, 2007;
Holmes, 2009; Stone and Lurquin, 2007). Humans were not the first such
species to reach Europe of course, as evidence for Homo erectus and Homo
neanderthalis have been found well before Homo sapiens sapiens arrived
(Mellars, 2004; Mosquera et al., 2013). However, no faecal samples from
hominins have so far been analysed for ancient parasites, and it is only
humans who have been studied in this way.
Until about 12,000 years ago, all humans are thought to have been
hunter-gatherers, obtaining their food by collecting it from their environ-
ment. However, around that time in the Middle East a major change
took place. Somebody decided to sow some of the seeds they had gathered
and the concept of farming was born. Roughly the same time people started
to catch and herd sheep and goats rather than just eating wild caught animals,
and this again radically changed the lives of many people (Zeder, 2011).
These ideas also spread to other populations such as Europe. More reliable
food sources seem to have allowed populations to grow so that towns and
small cities developed, with higher population densities to earlier times
(Gates, 2011). As population densities increased, people began to travel in
order to trade (Simmons and DiBenedetto, 2014). From the fourth millen-
nium BC sanitation technologies were also developed in the Middle East,
such as latrines, drains and clean piped water (Mitchell, 2015).
We can see that over this 12,000-year period there have been marked
changes in those factors that may have affected our risk of contracting and
spreading different kinds of parasites. The increasing size of towns and
numbers of burials in cemeteries over this time clearly suggests that these
changes allowed the population to increase. One possible explanation is
that the populations became larger because they were healthier in general.
However, an alternative hypothesis is that fertility increased as food was
Human Parasites in Medieval Europe: Lifestyle, Sanitation and Medical Treatment 391
more reliable for farmers (Lawson et al., 2012), but people were actually less
healthy since they harboured more infectious diseases and parasites. If we
were to compare the archaeological evidence in Europe for parasites in pre-
history and in the medieval period, we should be able to see the effects these
changes had upon disease in the past, and hopefully enable us to understand
which of the two hypotheses is correct.
As well as looking for changes in parasite infections over time, we can
also look for differences between geographical regions and the cultural habits
of the people who lived there (Gonçalves et al., 2003; Araujo et al., 2015a).
Comparison of parasites in different parts of medieval Europe can be made
using our knowledge of the different lifestyles of the populations in those
regions. This can help us to understand which factors were most important
in allowing such infections in the past, and so allow us to understand the
health implications of being born into different past societies. Such an
approach could assist with attempts to explain why some past empires or
civilizations were more successful than others.
They may also preserve the DNA of the parasites, proteins secreted by these
parasites during life and potentially the antibodies produced by the host
against the parasite (Deelder et al., 1990; Ara ujo et al., 1998; Bianucci
et al., 2008; Dittmar, 2009; Anastasiou and Mitchell, 2013a). All these
sources of evidence may be used to identify the species of parasite present
in the past.
Historical evidence in medieval texts can enable us to understand what
people thought of parasites. Sometimes their records allow us to suggest
possible diagnoses from the descriptions of worms passed from the anus,
mouth or nose (Cox, 2002; Trompoukis et al., 2007). However, since there
are many challenges associated with diagnosing diseases in the past using
written sources, we do have to be careful in our interpretation of ancient
written texts if we are to be realistic in how much we can tell about the
past (Mitchell, 2011a). Also, since we already know which species were pre-
sent in Europe at different times based upon archaeological evidence, what is
probably of much more interest to us is where texts explain what medieval
people thought of parasites. Manuscripts of most value to us today are those
that give the accepted views of the time as to how intestinal worms were
created, what it meant when parasites were seen, if the worms needed to
be treated by doctors, and how to treat them if a decision was made to treat.
This brings study of parasites in the medieval period to a new level compared
with prehistory, where by definition there were no records to explain what
people thought of their worms.
sediment dating from 30,000 to 24,000 BP was found to contain the egg of a
roundworm (Ascaris sp.) (Bouchet et al., 1996). It was thought to be of
human origin due to the archaeological context, so argued to probably be
an A. lumbricoides. No other parasite eggs were found at this site. It is difficult
to analyse faecal material for parasites at European hunter-gatherer sites as
the groups were by definition mobile. This means there were no permanent
buildings to us to excavate, no rubbish tips where faeces may have been
deposited, latrines had not yet been invented, and often no cemeteries
where the dead from a tribe may be placed close to one another for archae-
ologists to find their skeletal remains. In most European societies, these only
appeared once people decided to settle in one place, and the trigger for their
staying put seems to have been practicing agriculture.
Farming started to be practiced in Europe during the Neolithic period
(about 4000e2800 BC), when both agriculture and herding was practiced.
The exact dates vary across the region as these techniques gradually spread
over time. Across Neolithic Europe a large number of parasite species
have been identified, in what is now France, Germany, Greece, the
Netherlands and Switzerland. These include beef and/or pork tapeworm
(Taenia sp.), bile duct fluke (Opisthorchis sp.), Capillaria sp., dysentery proto-
zoa (E. histolytica), fish tapeworm (Diphyllobothrium sp.), giant kidney worm
(Dioctophymidae), hookworm (Ancylostomids), lancet liver fluke (Dicrocoe-
lium sp.), fasciola liver fluke (Fasciola hepatica), roundworm (A. lumbricoides),
whipworm (T. trichiura) (Anastasiou, 2015; Bouchet et al., 2003).
It is clear that the number of sites positive for parasites, and the range of
species present, is dramatically different in the Neolithic to the earlier Palae-
olithic period. Some of these parasites are zoonoses that people probably
contracted from eating raw or undercooked wild animals (e.g. Opisthorchis
sp., Capillaria sp., Dioctophymidae, Dicrocoelium sp., Diphyllobothrium sp.).
We might expect similar findings in earlier pure hunter-gatherer groups if
such studies had been possible. Other species of parasite are those that we
associate with sedentary lifestyle in farmers. Some are typically spread by
faecal contamination and poor sanitation (Ancylostomids, A. lumbricoides,
E. histolytica, T. trichiura), and others by the consumption of undercooked
farm animals (Taenia solium and Taenia saginata).
The Bronze Age (about 2800e500 BC) and Iron Age (about 700e100
BC) heralded a move from stone tools to those made of metal, and the overlap
in dates reflects how this was a gradual process spreading across the continent.
Parasites in humans from this time have been found in what is now Austria,
Britain, the Czech Republic, Denmark, France, Germany and Poland. The
Human Parasites in Medieval Europe: Lifestyle, Sanitation and Medical Treatment 397
species identified are dysentery protozoa (E. histolytica), lancet liver fluke
(Dicrocoelium sp.), roundworm (A. lumbricoides), whipworm (T. trichiura)
(Anastasiou, 2015; Bouchet et al., 2003). There does appear to be a trend to-
wards parasites spread by faecal contamination and poor sanitation, and little
evidence for those parasites spread by the eating of undercooked wild animals.
Whether this means those animals are no longer being caught and consumed,
or whether they are just being cooked better, is not clear from the parasite
evidence.
With the Roman period (about 100 BCe400 AD) we move from prehis-
tory to a time when written records complement archaeological assessment of
past societies. Parasites have been identified from excavations undertaken in
what is now Austria, Britain, France, Germany, Italy and Poland. The species
found are beef and/or pork tapeworm (Taenia sp.), dog tapeworm calcified
cysts (Echinococcus granulosus), fish tapeworm (Diphyllobothrium sp.), lancet liver
fluke (Dicrocoelium sp.), roundworm (A. lumbricoides), whipworm (T. trichiura)
(Anastasiou, 2015; Bouchet et al., 2003). Again, we see a similar pattern of
parasite species to the Bronze and Iron Ages. The dominant parasites seem
to be those spread by poor sanitation, faecal contamination and working
with dogs. It is interesting that in all time periods lancet liver fluke is found.
Since this is a parasite spread by the consumption of ants, this would indicate
either that people liked eating ants in the past, or that they were inadvertently
consumed along with foods. With the fall of the Roman Empire we move to
the early medieval period.
3. MEDIEVAL PERIOD
The medieval period in Europe lasts from about 500 to 1500 AD,
varying in different parts of the continent. There have been a large number
of medieval European archaeological sites where parasites have been studied
(for example, Boersma and Jansen, 1975; Jones, 1982; Herrmann, 1988;
Anastasiou and Mitchell, 2013b; Yeh et al., 2014). However, this does
not mean that the time period is a boring one to research because there is
nothing new to discover. It is actually the very body of evidence and the
contrasting findings in different contexts that means we can look in a
more nuanced way than is the case for continents or time periods for which
there are few published studies. These excavations have provided many
distinct pieces of fascinating evidence, and we are reaching a stage where
bigger questions can be examined using this data. Here we will interpret
398 Piers D. Mitchell
3.1 Sanitation
One of the key observations from this table is that roundworm and whip-
worm were found in more countries than any other parasites. They are
both faecal-oral parasites, spread by poor sanitation and faecal contamination
of food. This finding is well known, and has been commented upon many
times before (Herrmann, 1985; Reinhard et al., 2013; Reinhard and Pucu
de Ara ujo, 2014). Roundworm and whipworm (Figure 1) were not
restricted to the poor who may not have had clean water, clean clothes or
latrines in their houses. Even kings such as Richard III of England (ruled
1483e1485) were infected with roundworm (Figure 2) (Mitchell et al.,
Human Parasites in Medieval Europe: Lifestyle, Sanitation and Medical Treatment 399
Figure 1 Whipworm egg from Viking period latrine at York, UK. Dimensions
50 23 mm. Black bar indicates 20 mm.
Human Parasites in Medieval Europe: Lifestyle, Sanitation and Medical Treatment 401
Figure 2 Decorticated roundworm egg from the pelvic soil of King Richard III of
England (died 1485 AD). Dimensions 61 44 mm. Black bar indicates 20 mm.
2013). So we must ask ourselves why there seems to have been so much
roundworm and whipworm around in medieval Europe.
Modern studies have shown that when nomadic hunter-gatherers
around the world settle and change their lifestyle, the prevalence of infection
of roundworm, whipworm, hookworm and pathogenic amoebae increase
dramatically (Dounias and Froment, 2006). While these studies are generally
on forest-based groups living in the tropics, this is quite a significant finding
and starts to help us interpret why sedentary medieval people experienced so
much roundworm and whipworm too. Clinical research has also shown that
use of latrines, clean drinking water and washing hands with soap all reduce
the likelihood of contracting soil-transmitted helminths (geohelminths) such
as roundworm and whipworm (Zeigelbauer et al., 2012). Applying human
faeces to agricultural fields is known to increase crop yields (Heinonen-
Tanski and van Wijk-Sebesma, 2005). However, it has also been found
that either avoiding using human faeces as fertilizer, or at least composting
it for a minimum of 6 months prior to applying it to fields, greatly reduces
the risk of contracting these geohelminths from the food grown there (Uga
et al., 2009; Phuc et al., 2006; Jensen et al., 2008).
Archaeological evidence shows that the latrine was in use in people’s
houses in the Middle East by the late 4th millennium BC (McMahon,
2015), and in Greece by the 2nd millennium BC (Antoniou and Angelakis,
2015). The Romans adopted the sanitation technology of the Greeks,
402 Piers D. Mitchell
Figure 3 Fish Tapeworm egg from a fourteenth century AD latrine at Riga, Latvia.
Width 45 mm. Black bar indicates 20 mm.
404 Piers D. Mitchell
contaminated by dog faeces then these hydatid cysts develop in the chest,
abdomen or brain (Garcia, 2009, p. 362; Gunn and Pitt, 2012, p. 108).
The walls of these cysts often calcify and are preserved after death, to be
recovered at archaeological excavation of burials. Examples of these calcified
hydatid cysts have been recovered from medieval contexts in Britain, Iceland
and Denmark (Table 1). It has been proposed that hydatid disease became
endemic in Iceland following the shipment of dogs from Germany around
1200 AD (Kristjansd ottir and Collins, 2011). This shows these individuals
must have been exposed to dog faeces on their food. Those medieval people
using dogs to herd sheep or hunt wild animals would clearly have been in this
high risk group.
Some parasites specific to humans spend part of their life cycle in an an-
imal before they are spread to people who eat it. If those animals are species
we chose to farm, then it is logical to assume that those parasites will become
more common as a result. Good examples of this scenario are the beef and
pork tapeworms (T. saginata and T. solium). The eggs of these parasites
appear identical under the microscope, so are not easy to differentiate in
archaeological contexts. Genetic studies of the Taenia genus suggest beef
tapeworm evolved as a specialist parasite of humans in Africa at least 1 million
years ago, while the origins of pork tapeworm is less clear and has been
linked with both lions and bears (Hoberg et al., 2001; Mitchell, 2013; Terefe
et al., 2014). It is likely that the two species survived in wild cattle and wild
pigs that were hunted or scavenged by human hunter-gatherers. However,
when people started to farm large animals, they found that cattle and pigs
were very suitable to domestication. Taenia tapeworm eggs have been found
in medieval Denmark, Belgium, Britain and Germany (Table 1), although it
has been found in other European countries in earlier time periods (Sianto
et al., 2009). Taenia sp. seems to have been less common in medieval times
than was fish tapeworm. This may reflect the different cooking methods
used for these meats, as in Europe pork and beef were typically cooked
and not generally eaten raw, dried, smoked or pickled.
Fasciola liver fluke (F. hepatica) has been found in Belgium, Denmark and
Germany during the medieval period (Table 1), but again in other countries
in earlier time periods (Sianto et al., 2009). It was clearly not as widespread as
roundworm, whipworm or fish tapeworm in medieval times. It is a zoonotic
parasite that typically infects sheep, cattle and other ruminants that may eat
semiaquatic plants contaminated by the metacercariae. If humans eat those
plants and do not cook them first, they can become infected by the fluke
(Garcia, 2009, p. 368; Gunn and Pitt, 2012, p. 91). One might expect
406 Piers D. Mitchell
that the farming of such animals would therefore increase the likelihood of
contracting the disease. Farming sheep and cattle was a major activity in
northern Europe in the medieval period, and the numbers of animals
were significantly higher than in earlier time periods (Astill and Langdon,
1997; Hoskins, 1955; Faith, 2010; Lucas, 1989). For example, there are
thought to have been over 10 million sheep in England by the thirteenth
century (Hurst, 2005). For these reasons, we would expect the expanding
farming sector to have increasingly predisposed those living in farming areas
to contracting fasciola liver flukes, so long as they continued to eat fresh salad
leaves.
Europe, and lay within the Frankish Kingdom of Jerusalem. The Order of St.
John was a military and hospitaller order, founded in 1112 AD to care for sick
pilgrims in the Holy Land (Nicholson, 2007; Riley-Smith, 2012). Not all
crusader latrines have been positive for fish tapeworm eggs, suggesting that
infection with Diphyllobothrium was by no means ubiquitous among crusaders
(Mitchell and Tepper, 2007; Anastasiou and Mitchell, 2013b). In the medie-
val period fish was not eaten raw, pickled or smoked in the Middle East as the
hot temperatures meant it decomposed more quickly than in northern
Europe. Medieval textual sources from the Middle East show that it was al-
ways eaten cooked (Lewicke, 2011). Cooking kills the intermediate forms of
the parasite and so prevents its transmission. Finding the eggs of fish tapeworm
in two separate medieval latrines used by crusaders from Europe suggests they
probably contracted the parasite in northern Europe where it was common,
and travelled to the east on crusade taking the tapeworms with them in their
intestines. The parasite does not seem to have ever become endemic in the
freshwater fish of the region (such as at Lake Tiberias), suggesting the local
environment probably did not meet all the requirements for its life cycle.
Such parasitological evidence complements written descriptions in textual
sources of the period, recording how epidemics and other infectious diseases
seem to have been spread by crusaders and pilgrims as they travelled (Mitchell,
2011b).
Potential evidence for long distance travel can be found following the
analysis of a Mamluk period cesspool from the Christian Quarter of Jerusalem
(Yeh et al., 2015). Radiocarbon dating and pottery fragments show the
cesspool was in use during the late 1400s and early 1500s. The pottery in
the latrine came from both the Jerusalem region and also from northern Italy.
Six species of parasites were found in coprolites and cesspool sediment, four
helminths (roundworm, whipworm, Taenia tapeworm and fish tapeworm)
and two protozoa (E. histolytica and G. duodenalis). Entamoeba histolytica seems
to have originated in Europe as all the early examples come from there
(Le Bailly and Bouchet, 2015). We have already seen how fish tapeworm
was common in northern Europe during the medieval period, and has
recently been identified in northern Italy (Florenzano et al., 2012). There
are a number of potential explanations as to how this picture may have
come about. One possibility is that merchants from Jerusalem travelled to
northern Italy, bought pottery and contracted parasites before returning
home. Another option to consider is that E. histolytica may have become
endemic in the region after its spread there by crusaders in the thirteenth cen-
tury, but the same would be unlikely for fish tapeworm as fish was typically
408 Piers D. Mitchell
eaten cooked in the Middle East and this would prevent parasite transmission.
A further possibility is that this was a hostel providing accommodation for
European traders or pilgrims travelling to the Christian quarter of the holy
city (Yeh et al., 2015).
that the pandemic was caused by Y. pestis (Bos et al., 2011; Cui et al., 2013).
However, it is not entirely clear if rat fleas were also responsible for the
spread of the Black Death between humans. Medieval written records do
not describe dead rats in the streets as generally happens in recent epidemics
(Slack, 1989; Cohn, 2008). Bubonic plague swept across fourteenth-century
Scandinavia just as it did elsewhere on the continent, but archaeological
studies have shown the black rat (Rattus rattus) to have been rare or
completely absent in Nordic countries at that time (Hufthammer and
Walløe, 2013). If there were few or no rats in the region, this would suggest
it could not have been the bite of the rat flea that was spreading the
infection. It has been argued that in the Black Death pandemic the Yersinia
bacteria may have been spread instead by fleas normally found on other
mammals including humans (e.g. P. irritans), the body louse (Pediculus
humanus humanus), or as pneumonic plague by coughing (Houhamdi
et al., 2006; Hufthammer and Walløe, 2013; Carmichael, 2014).
in the body that had been defined by Hippocrates (blood, phlegm, black bile
and yellow bile). Maurus believed that when there was an excess of phlegm
because the person was not eating the right balance of foods or was getting
elderly, the body would try and get rid of the phlegm by producing worms
and expelling them. Hence worms were not regarded as a disease in their
own right, but rather as a sign of humoural imbalance due to excess phlegm
(Saffron, 1972). Medieval medical practitioners would try to treat this imbal-
ance by modifying the diet, by bloodletting and with medicines that were
thought to reduce the levels of phlegm in the body and so return the
humoural balance to normal (Harington, 1953; York, 2012; Mitchell,
2014).
Medieval texts sometimes describe outbreaks of dysentery in armies on
campaign. The 7th Crusade took place from 1248 to 1252, and armies
from across Europe led by King Louis IX of France invaded Egypt. After
some months of campaigning the army was surrounded by Egyptian troops,
trapped between canals clogged with corpses (Bartlett, 2007; Jackson, 2007).
Personal hygiene, latrines and clean drinking water were not available, and
widespread dysentery took hold. We hear how King Louis had diarrhoea so
frequently that he had the bottom of his breeches cut off, so his liquid stool
could run down his legs without having to remove his clothes (Hague, 1955,
p. 24). The fact that Louis was reduced to this low level of personal hygiene,
compared with that normally expected for a medieval French king, high-
lights the challenging position of the whole army. It shows how accepted
attitudes to smells, sights and sounds can be lost in desperate times. The
army later surrendered to the Egyptians, and after ransoming themselves
they travelled to the city of Acre, a crusader city on the Mediterranean coast
of the Frankish Kingdom of Jerusalem. ELISA analysis of thirteenth-century
sediments from the latrines of the crusading Order of St. John at Acre has
found evidence for two parasites that can cause dysentery, E. histolytica
and G. duodenalis (Mitchell et al., 2008b). It is possible that either or both
of these species may have been responsible for the outbreak of dysentery
on the 7th Crusade.
There is some evidence for the use of topical medications containing
mercury to treat ectoparasites in 1400s Europe. Ferdinand II of Aragon
was the King of Naples in Italy, and he lived from 1467 to 1496. Analysis
of his naturally mummified body shows that he was infected with both
head lice (P. humanus capitis) and pubic lice (P. pubis). Tests of the hair
from his head showed very high levels of mercury (827 parts per million),
suggestive of the topical application of a mercury-containing medicine to
412 Piers D. Mitchell
try and kill off the head lice. However, his pubic hair did not show these
very high levels (10 parts per million), implying that he did not undergo
treatment for his pubic lice (Fornaciari et al., 2011).
4. CONCLUSION
In the medieval period, Europe was a diverse continent in terms of its
geography, climate, population density and lifestyles. This resulted in quite
different patterns of parasitism in different regions. Past work has tended to
amalgamate the evidence for the continent in order to gain an overview, and
to provide a data source with which to compare with parasitism in other
continents. Here we do the opposite, by exploring the differences within
the continent and attempting to understand why these differences existed.
This approach has shown that roundworm and whipworm were found
right across the continent, with little evidence for significant variability
between regions. Despite the modern evidence that latrine use decreases the
prevalence of these faecal-oral parasites, there does not seem to be any archae-
ological evidence for a decrease in these parasites with increasing numbers of
latrines. It is quite possible that the widespread use of human faeces as a crop
fertilizer in medieval Europe meant that food plants became contaminated
with parasite eggs and this negated any health benefits from latrine use.
However, a number of parasite species demonstrated marked variability
in prevalence across Europe. In some cases it was due to local culinary prac-
tices, such as the eating of raw, smoked or pickled fish predisposing the pop-
ulation to widespread fish tapeworm infection in many parts of northern
Europe. Farming herbivores such as pigs, cattle and sheep seems to have
facilitated the spread of parasites such as pork tapeworm, beef tapeworm
and liver fluke to medieval people. In regions where herding sheep was
common, and dogs were widespread, we see evidence for hydatid disease
in humans too. The medieval archaeological evidence for hydatid cysts
seems to be concentrated in northern Europe.
Migrations can be detected when parasites are identified in locations
incompatible with their life cycle, or where they had not previously been
identified. Examples of such parasites include two species of schistosomiasis
in France, and both fish tapeworm and entamoeba dysentery in crusaders
and Mamluk period pilgrims.
A range of ectoparasites have been recovered from medieval Europe.
Some would have just led to itchy skin and annoyance, but others have
Human Parasites in Medieval Europe: Lifestyle, Sanitation and Medical Treatment 413
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INDEX
‘Note: Page numbers followed by “f” indicate figures and “t” indicate tables.’
A B
Acanthocephala, 109–110, 246–247 Barnacles, 249–252, 250f
Acrothoracica, 265–266 Benthic colonies, 331
Aculeata, 165 Bioarchaeology, 358
aDNA. See Ancient DNA (aDNA) Bioclaustrations, 242, 334–338
Amber Bivalve skeletons, 218–219
Baltic amber, 25, 60–65, 145, 170, 173 Blister beetles, 161–162
Dominican amber, 16t, 65–75, 109–110, Body fossils, 14–17, 55–60, 96–97, 140,
157, 160, 179, 375 203, 237–239, 249, 339
Mexican amber, 75–77, 160 Bopyroids, 237–239
Amblycera, 143 Borings, 292–293, 340–341
Amblyceropsis indica, 145 Brachylophosaurus canadensis, 7
Amphoracrinus gilbertsoni, 300f, 301 Branchiura, 270–271
Ancient biomolecules
aDNA, 6–7 C
palaeoproteomics, 7 Cambrian, 5–6, 79–80, 108–112, 140,
stabilized haem, 6 211–216, 261–262, 340–341
Ancient DNA (aDNA), 4–7, 369 Cambrian–Ordovician species, 29–30,
Ancient parasite discovery 262–264
ancient biomolecules Capillaria sp., 408
aDNA. See Ancient DNA (aDNA) Carboniferous, 82, 105, 113, 140, 161, 173
palaeoproteomics, 7 Carboniferous coprolite. See Coprolites
stabilized haem, 6 Cascofilaria baltica, 64
computed tomography, 5–6 Castexia douvillei, 252–253
See also Computed tomography (CT) Catastrophic climate events, 359–360
destructive/nondestructive methods, Catellocaula vallata, 337
4–5 Caunopores, 335, 335f
thin sections, 5–6 Celleporaria palmata, 338
Anodonta piscinalis, 222–223 Cephalotes serratus, 67
Anoigmaichnus odinsholmensis, 337 Ceratoconcha, 266–267
Anoplura, 142–143 Ceratopogonidae, 152, 157
Antedon bifida, 297 Cercomer theory, 94–95
Antliophora Cestoda, 9t–13t, 94–95, 97–100, 104f
Diptera, 152–159 Chaeotosalpinx tapanilai, 337
Mecopteroidea, 147 Chironomidae, 152
Siphonaptera, 139, 147–152 Chrysidoidea, 165, 168–169
Aphelenchoides marinus, 83 Ciliates, 246
Archicnephia ornithoraptor, 157 Cladocyclus gardneri, 253–258
Ascaris lumbricoides, 362–363, 369–371 Clonorchis sinensis, 361–362
Ascarites priscus, 58, 59f Cobelodus aculeatus, 105
Asterolepis ornata, 97–99 Coleoptera
Astya crassus, 249 Adiphlebia lacoana, 161
421 j
422 Index
I J
Ichneumonoidea, 165 Jurassic, 9t–13t, 80, 148, 151–152, 156,
Ichnology, 293 158, 160–161, 173, 212f, 237–241,
Insect-parasitic tylenchs, 81 238f, 253f, 254t–257t, 313
Index 425
K Montemagrechirus, 260–261
Kabatarina, 253–258, 258f Myxozoa, 27
K. patersoni, 9t–13t, 253–258
Kanthyloma crusta, 237–239, 238f N
Kato-Katz technique, 363–364 Nematode parasites
Kerodon rupestris, 77 from cenozoic
baltic amber, 60–65, 61f–66f
L fossil nematodes
Latrines, 394 amber, 54
Light acetolysis, 365–366 coprolites, 55
Liposcelidae, 143 rock fossils, 54–55
Lodeacanthus gaujicus, 97–99, 246 invertebrates, 79–81
Lutz spontaneous sedimentation method, mesozoic, body fossils from, 55–60,
366–367 56f–58f
Oligocene–Miocene
M Dominican amber nematodes, 65–75,
Maculo, 371 67f–75f
Malacostraca, 272 Mexican amber nematodes, 75–77, 76f
Mallophaga, 142 Palaeozoic parasitic nematodes, 55
Marine crustaceans, 9t–13t, 235, 248 plants, 83
Mass spectrometry, 3 Pleistocene and Holocene, 77–79
Megalosaurus dunkeri, 105–106 humans, 78–79
Megalyroidea, 167–168 from Pliocene, 77
Megamenopon rasnitsyni, 145–146 vertebrates, 81–82
Metagonimus yokogawai, 361–362 Nematoida
Microendoliths, 341 fossil representatives, 175
Microniscus larva, 236–237 general aspects, 174
MicroRNAs, 94–95 phylogenetic inference, 174
Mineralized coprolites, 394–395 Neolithic Revolution, 360–361
Miocene, 9t–13t, 108–109, 115, 149, 158, Neuroptera, 159
162, 205, 237–239, 339, 375 fossil representatives, 160–161
Mites general aspects, 159–160
fossil representatives, 176 phylogenetic inference, 160
general aspects, 175 Neuropteroida, 159
phylogenetic inference, 176 Coleopterida, 161–162
Molecular clock methods Neuroptera, 159–161
biogeographic calibrations, 116 Nilonema, 32–34
cophylogenetic approach, 113 Nothrotheriops shastensis, 78
fossil calibrations, criteria, 113–114 Nucleotide sequencing, 369
Polystomatidae, 116–117 Nuculodonta gotlandica, 211–216
pseudo-congruence, 116
Schistosoma, 115 O
taxon sampling, 117–119 Oligaphelenchoides atrebora, 75–76, 76f
Westollrhynchus, 116–117 Oligocene, 156, 160–161, 266–267,
Moltkia minuta, 249 339–340
Monogenea, 94–95, 119–120 Ordovician, 29–30, 81–82, 110–112, 114,
Monopisthocotylea, 94–95 262–264, 296, 333–334, 338
426 Index
R T
Rhizocephalan barnacles, 244–246 Tantulocarida, 248, 270
Rhynchophthirina, 143 Tarbellastrea reussiana, 266–267
Rhynie Chert, 14–15, 55, 56f Tarwinia australis, 149–150
Torquaysalpinx, 336
S Trace fossils/pathologies, 18–22, 108–109,
Salmonella enterica, 357 242, 293, 311, 337
Saurodectes vrsanskyi, 145 blister pearls, 209–210
Saurophthirus borings
S. exquisitus, 151 in colonial organisms, 340–341
S. longipes, 149 in crustaceans, 340–341
Schistosoma, 115 in echinoderms, 292–293
S. haematobium, 108 gymnophallid-induced pits, 18–19
Schistosomiasis mansoni, 363–364 igloo-shaped concretions, 18–19
Sedilichnus unicellular eukaryotes, 20–21
S. excavatus, 316–317 ‘zombie’ ants, 20–21
S. paraboloides, 302, 305 Trapeziidae, 269
Shergoldana australiensis, 175 Trematodes
Silurian, 5–6, 57, 101–103, 140, 209–216, Abra tenuis, 209–210
241, 334–335, 335f bivalve molluscs, 203, 206–210
Siphonaptera, 9t–13t, 15–17, 377, blister pearls, 209–210
391–392, 398 detrimental effects of, 222–225
fossil representatives, 149–152 Anodonta piscinalis, 222–223
general aspects, 148 Chamalea gallina, 223–225, 225f
phylogenetic inference, 148–149 Transenella, 223–225
Smilium zancleanum, 248 fossil and subfossil bivalves, trematode-
Smithsoninema inaequale, 60 induced pits occurrences, 211–222
Spinther, 29–30 paleoenvironmental indicators,
Strashila incredibilis, 149 220–222, 221f
Strepsiptera taphonomy and origin, 217–220
fossil representatives, 171–172 taxonomic/temporal and ecological,
general aspects, 169–170 211–216, 212f, 213t–215t, 217f
phylogenetic inference, 170 Gymnophallus rebecqui, 209–210
Strongylus edentatus, 77 parasite–host interaction, 204–205
Symbiodinium, 342 Triaenodes balticus, 64–65
Symbiotic intergrowths/bioclaustrations, Triassic, 9t–13t, 101–103, 140, 145,
334–340, 334f 152–154, 156, 167, 209–210, 313
caunopores, 335, 335f Trichuris trichiura, 354, 369–371
Celleporaria, 338 Trigonalyoidea, 168
Chaetosalpinx and bioclaustrations, Trisodium phosphate aqueous solution,
336–338 363
cornulitids and stromatoporoids, 338 Troglocarcinus corallicola, 259–260, 259f
Culicia, 338 Trypanosoma
pyrgomatid barnacles, 339–340 T. antiquae, 375
rugose corals and stromatoporoids, 336 T. cruzi, 352, 375
Synbathocrinus conicus, 302, 302f Tumidocarcinus giganteus, 244–246
Syringonomous typicus, 60 Tyrannosaurus rex, 7, 296
Index 429
U X
Ulophysema, 249 Xenopsylla cheopis, 409–410
V Z
Venericor clarendonensis, 102f, 106, Zooids, 330
213t–215t, 216, 219–220
Vespoidea, 165–166
CONTENTS OF VOLUMES IN THIS SERIES
Volume 41 Volume 43
Drug Resistance in Malaria Parasites of Genetic Exchange in the Trypanosomatidae
Animals and Man W. Gibson and J. Stevens
W. Peters
The Host-Parasite Relationship in Neosporosis
Molecular Pathobiology and Antigenic A. Hemphill
Variation of Pneumocystis carinii
Y. Nakamura and M. Wada Proteases of Protozoan Parasites
P.J. Rosenthal
Ascariasis in China
P. Weidono, Z. Xianmin and Proteinases and Associated Genes of Parasitic
D.W.T. Crompton Helminths
J. Tort, P.J. Brindley, D. Knox,
The Generation and Expression of Immunity K.H. Wolfe, and J.P. Dalton
to Trichinella spiralis in Laboratory Rodents
R.G. Bell Parasitic Fungi and their Interaction with the
Insect Immune System
Population Biology of Parasitic Nematodes: A. Vilcinskas and P. G€otz
Application of Genetic Markers
T.J.C. Anderson, M.S. Blouin Volume 44
and R.M. Brech
Cell Biology of Leishmania
Schistosomiasis in Cattle B. Handman
J. De Bont and J. Vercruysse
Immunity and Vaccine Development in the
Volume 42 Bovine Theilerioses
N. Boulter and R. Hall
The Southern Cone Initiative Against Chagas
The Distribution of Schistosoma bovis Sonaino,
Disease
1876 in Relation to Intermediate Host
C. J. Schofield and J.C.P. Dias
Mollusc-Parasite Relationships
Phytomonas and Other Trypanosomatid H. Moné, G. Mouahid, and S. Morand
Parasites of Plants and Fruit
The Larvae of Monogenea (Platyhelminthes)
E.P. Camargo
H.D. Whittington, L.A. Chisholm, and
Paragonimiasis and the Genus Paragonimus K. Rohde
D. Blair, Z.-B. Xu, and T. Agatsuma
Sealice on Salmonids: Their Biology and
Immunology and Biochemistry of Hymenolepis Control
diminuta A.W. Pike and S.L. Wadsworth
J. Anreassen, E.M. Bennet-Jenkins, and
C. Bryant Volume 45
Control Strategies for Human Intestinal The Biology of some Intraerythrocytic
Nematode Infections Parasites of Fishes, Amphibia and Reptiles
M. Albonico, D.W.T. Cromption, and A.J. Davies and M.R.L. Johnston
L. Savioli
The Range and Biological Activity of FMR
DNA Vaocines: Technology and Applications Famide-related Peptides and Classical
as Anti-parasite and Anti-microbial Agents Neurotransmitters in Nematodes
J.B. Alarcon, G.W. Wainem and D. Brownlee, L. Holden-Dye,
D.P. McManus and R. Walker
431 j
432 Contents of Volumes in This Series
Volume 53 Volume 55
Interactions between Tsetse and Contents of Volumes 28–52
Trypanosomes with Implications for the Cumulative Subject Indexes for Volumes
Control of Trypanosomiasis 28–52
S. Aksoy, W.C. Gibson, and M.J. Lehane Contributors to Volumes 28–52
434 Contents of Volumes in This Series
The Mitochondrial Genomics of Parasitic The Curious Life-Style of the Parasitic Stages
Nematodes of Socio-Economic of Gnathiid Isopods
Importance: Recent Progress, and N.J. Smit and A.J. Davies
Implications for Population Genetics
and Systematics
M. Hu, N.B. Chilton, and R.B. Gasser
Volume 59
Genes and Susceptibility to Leishmaniasis
The Cytoskeleton and Motility in
Emanuela Handman, Colleen Elso, and Simon
Apicomplexan Invasion
Foote
R.E. Fowler, G. Margos, and G.H. Mitchell
Cryptosporidium and Cryptosporidiosis
Volume 57 R.C.A. Thompson, M.E. Olson, G. Zhu,
S. Enomoto, Mitchell S. Abrahamsen and
Canine Leishmaniasis N.S. Hijjawi
J. Alvar, C. Ca~navate, R. Molina, J. Moreno,
and J. Nieto Ichthyophthirius multifiliis Fouquet and
Ichthyophthiriosis in Freshwater Teleosts
Sexual Biology of Schistosomes R.A. Matthews
H. Moné and J. Boissier
Biology of the Phylum Nematomorpha
Review of the Trematode Genus Ribeiroia B. Hanelt, F. Thomas, and A. Schmidt-Rhaesa
(Psilostomidae): Ecology, Life History,
and Pathogenesis with Special Emphasis
on the Amphibian Malformation Problem Volume 60
P.T.J. Johnson, D.R. Sutherland, J.M. Kinsella Sulfur-Containing Amino Acid Metabolism
and K.B. Lunde in Parasitic Protozoa
The Trichuris muris System: A Paradigm of Tomoyoshi Nozaki, Vahab Ali, and Masaharu
Resistance and Susceptibility to Intestinal Tokoro
Nematode Infection The Use and Implications of Ribosomal DNA
L.J. Cliffe and R.K. Grencis Sequencing for the Discrimination of
Scabies: New Future for a Neglected Disease Digenean Species
S.F. Walton, D.C. Holt, B.J. Currie, Matthew J. Nolan and Thomas H. Cribb
and D.J. Kemp Advances and Trends in the Molecular
Systematics of the Parasitic
Volume 58 Platyhelminthes
Peter D. Olson and Vasyl V. Tkach
Leishmania spp.: On the Interactions they
Establish with Antigen-Presenting Cells Wolbachia Bacterial Endosymbionts of Filarial
of their Mammalian Hosts Nematodes
J.-C. Antoine, E. Prina, N. Courret, and Mark J. Taylor, Claudio Bandi, and
T. Lang Achim Hoerauf
Contents of Volumes in This Series 435
Volume 62
Volume 61
Models for Vectors and Vector-Borne Diseases
Control of Human Parasitic Diseases: Context D.J. Rogers
and Overview
David H. Molyneux Global Environmental Data for Mapping
Infectious Disease Distribution
Malaria Chemotherapy S.I. Hay, A.J. Tatem, A.J. Graham,
Peter Winstanley and Stephen Ward S.J. Goetz, and D.J. Rogers
Insecticide-Treated Nets Issues of Scale and Uncertainty in the Global
Jenny Hill, Jo Lines, and Mark Rowland Remote Sensing of Disease
Control of Chagas Disease P.M. Atkinson and A.J. Graham
Yoichi Yamagata and Jun Nakagawa Determining Global Population Distribution:
Human African Trypanosomiasis: Methods, Applications and Data
Epidemiology and Control D.L. Balk, U. Deichmann, G. Yetman,
E.M. Févre, K. Picozzi, J. Jannin, F. Pozzi, S.I. Hay, and A. Nelson
S.C. Welburn and I. Maudlin Defining the Global Spatial Limits of Malaria
Chemotherapy in the Treatment and Control Transmission in 2005
of Leishmaniasis C.A. Guerra, R.W. Snow and
Jorge Alvar, Simon Croft, and Piero Olliaro S.I. Hay
Dracunculiasis (Guinea Worm Disease) The Global Distribution of Yellow Fever and
Eradication Dengue
Ernesto Ruiz-Tiben and Donald R. Hopkins D.J. Rogers, A.J. Wilson, S.I. Hay, and
A.J. Graham
Intervention for the Control of
Soil-Transmitted Helminthiasis in Global Epidemiology, Ecology and Control
the Community of Soil-Transmitted Helminth Infections
Marco Albonico, Antonio Montresor, S. Brooker, A.C.A. Clements and
D.W.T. Crompton, and Lorenzo D.A.P. Bundy
Savioli Tick-borne Disease Systems: Mapping
Control of Onchocerciasis Geographic and Phylogenetic Space
Boakye A. Boatin and S.E. Randolph and D.J. Rogers
Frank O. Richards, Jr. Global Transport Networks and Infectious
Lymphatic Filariasis: Treatment, Control and Disease Spread
Elimination A.J. Tatem, D.J. Rogers and S.I. Hay
Eric A. Ottesen Climate Change and Vector-Borne Diseases
Control of Cystic Echinococcosis/Hydatidosis: D.J. Rogers and S.E. Randolph
1863-2002
P.S. Craig and E. Larrieu Volume 63
Control of Taenia solium Cysticercosis/ Phylogenetic Analyses of Parasites in the New
Taeniosis Millennium
Arve Lee Willingham III and Dirk Engels David A. Morrison
436 Contents of Volumes in This Series
OnchocercaSimulium Interactions and the Dynamic Use of Fruit Odours to Locate Host
Population and Evolutionary Biology of Larvae: Individual Learning, Physiological
Onchocerca volvulus State and Genetic Variability as Adaptive
María-Gloria Basa~nez, Thomas S. Churcher, Mechanisms
and María-Eugenia Grillet Laure Kaiser, Aude Couty, and
Raquel Perez-Maluf
Microsporidians as Evolution-Proof Agents of
Malaria Control? The Role of Melanization and Cytotoxic
Jacob C. Koella, Lena Lorenz, and By-Products in the Cellular Immune
Irka Bargielowski Responses of Drosophila Against Parasitic
Wasps
A. Nappi, M. Poirié, and Y. Carton
Virulence Factors and Strategies of Leptopilina
Volume 69 spp.: Selective Responses in Drosophila
Hosts
The Biology of the Caecal Trematode
Mark J. Lee, Marta E. Kalamarz,
Zygocotyle lunata
Indira Paddibhatla, Chiyedza Small,
Bernard Fried, Jane E. Huffman, Shamus Keeler,
Roma Rajwani, and Shubha Govind
and Robert C. Peoples
Variation of Leptopilina boulardi Success in
Fasciola, Lymnaeids and Human Fascioliasis,
Drosophila Hosts: What is Inside the Black
with a Global Overview on Disease
Box?
Transmission, Epidemiology,
A. Dubuffet, D. Colinet, C. Anselme,
Evolutionary Genetics, Molecular
S. Dupas, Y. Carton, and M. Poirié
Epidemiology and Control
Santiago Mas-Coma, María Adela Valero, and Immune Resistance of Drosophila Hosts Against
María Dolores Bargues Asobara Parasitoids: Cellular Aspects
Patrice Eslin, Genevieve Prévost, Sebastien
Recent Advances in the Biology of
Havard, and Géraldine Doury
Echinostomes
Rafael Toledo, José-Guillermo Esteban, and Components of Asobara Venoms and their
Bernard Fried Effects on Hosts
Sébastien J.M. Moreau, Sophie Vinchon, Anas
Peptidases of Trematodes
Cherqui, and Genevieve Prévost
Martin Kasný, Libor Mikes, Vladimír Hampl,
Jan Dvorak, Conor R. Caffrey, John P. Strategies of Avoidance of Host Immune
Dalton, and Petr Horak Defenses in Asobara Species
Geneviéve Prevost, Géraldine Doury, Alix D.N.
Potential Contribution of
Mabiala-Moundoungou, Anas Cherqui, and
Sero-Epidemiological Analysis for
Patrice Eslin
Monitoring Malaria Control and
Elimination: Historical and Current Evolution of Host Resistance and Parasitoid
Perspectives Counter-Resistance
Chris Drakeley and Jackie Cook Alex R. Kraaijeveld and H. Charles J. Godfray
Contents of Volumes in This Series 439
Volume 83 Volume 85
IronSulphur Clusters, Their Biosynthesis, Diversity and Ancestry of Flatworms Infecting
and Biological Functions in Protozoan Blood of Nontetrapod Craniates “Fishes”
Parasites Raphael Orélis-Ribeiro, Cova R. Arias,
Vahab Ali and Tomoyoshi Nozaki Kenneth M. Halanych,Thomas H. Cribb,
and Stephen A. Bullard
A Selective Review of Advances in Coccidiosis
Research Techniques for the Diagnosis of Fasciola
H. David Chapman, John R. Barta, Infections in Animals: Room for
Damer Blake, Arthur Gruber, Mark Jenkins, Improvement
Nicholas C. Smith, Xun Suo, and Cristian A. Alvarez Rojas, Aaron R. Jex,
Fiona M. Tomley Robin B. Gasser, and
Jean-Pierre Y. Scheerlinck
The Distribution and Bionomics of
Anopheles Malaria Vector Mosquitoes in Reevaluating the Evidence for Toxoplasma
Indonesia gondii-Induced Behavioural Changes in
Iqbal R.F. Elyazar, Marianne E. Sinka, Rodents
Peter W. Gething, Siti N. Tarmidzi, Amanda R. Worth, R.C. Andrew Thompson,
Asik Surya, Rita Kusriastuti, Winarno, and Alan J. Lymbery
J. Kevin Baird, Simon I. Hay, and
Michael J. Bangs Volume 86
Next-Generation Molecular-Diagnostic Tools Historical Patterns of Malaria Transmission in
for Gastrointestinal Nematodes of China
Livestock, with an Emphasis on Small Jian-Hai Yin, Shui-Sen Zhou, Zhi-Gui Xia,
Ruminants: A Turning Point? Ru-Bo Wang, Ying-Jun Qian, Wei-Zhong
Florian Roeber, Aaron R. Jex, and Yang, and Xiao-Nong Zhou
Robin B. Gasser
Feasibility and Roadmap Analysis for Malaria
Elimination in China
Volume 84 Xiao-Nong Zhou, Zhi-Gui Xia, Ru-Bo Wang,
Joint Infectious Causation of Human Ying-Jun Qian, Shui-Sen Zhou, J€urg
Cancers Utzinger, Marcel Tanner, Randall Kramer,
Paul W. Ewald and Holly A. Swain Ewald and Wei-Zhong Yang