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VOLUME NINETY

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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CONTRIBUTORS

Adauto Ara ujo
Fundaç~ao Oswaldo Cruz, Laborat
orio de Paleoparasitologia, Rio de Janeiro, RJ, Brazil
Geoff A. Boxshall
Department of Life Sciences, Natural History Museum, London, UK
Kenneth De Baets
Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€
urnberg, Erlangen, Germany
Paula Dentzien-Dias
N
ucleo de Oceanografia Geologica, Instituto de Oceanografia, Universidade Federal do Rio
Grande, Rio Grande, Brazil
Philip C.J. Donoghue
School of Earth Sciences, University of Bristol, Life Science Building, Bristol, UK
Stephen K. Donovan
Department of Geology, Naturalis Biodiversity Center, Leiden, The Netherlands
Luiz Fernando Ferreira
Fundaç~ao Oswaldo Cruz, Laborat
orio de Paleoparasitologia, Rio de Janeiro, RJ, Brazil
Joachim T. Haug
Department of Biology II, Functional Morphology Group, University of Munich (LMU),
Planegg-Martinsried, Germany
John Warren Huntley
Department of Geological Sciences, University of Missouri, Columbia, MO, USA
Adiël A. Klompmaker
Florida Museum of Natural History, University of Florida, Gainesville, FL, USA
D. Timothy J. Littlewood
Department of Life Sciences, Natural History Museum, London, UK
Piers D. Mitchell
Department of Archaeology and Anthropology, University of Cambridge, Cambridge,
United Kingdom
Christina Nagler
Department of Biology II, Functional Morphology Group, University of Munich (LMU),
Planegg-Martinsried, Germany
George O. Poinar, Jr.
Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA
Karl Reinhard
School of Natural Resources, University of Nebraska, Lincoln, NE, USA

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

Parasites are ubiquitous, numerous and diverse, and it is widely considered
that this must have been the situation for much of the history of life.
However, understanding the evolutionary history of parasites and their
impact on hosts and ecology through time has relied almost exclusively on
inferences extrapolated from the diversity and nature of parasite species
living today. To a large extent the fossil record of parasites has been over-
looked. Consequently, the role and potential of fossil parasites in the field of
evolutionary biology, and indeed parasitology more generally, has been
difficult to assess. Almost 25 years ago Simon Conway Morris published a
review of fossil parasites in the Journal of Parasitology (82:489–509), consid-
ering their importance in an evolutionary context and providing a com-
prehensive singular resource amenable to parasitologists and palaeontologists
alike. Subsequent reviews on this topic have focused on particular groups of
marine or terrestrial parasites, whilst consideration of fossil parasites more
generally has been invoked through palaeoecological interpretations of
behaviour, coevolution and the nature of trace fossils. This new knowledge
on fossil parasites is mostly scattered in the literature, making it harder to get
an overview of their usefulness and potential for illuminating or framing
their evolutionary history. Newly discovered fossils, the development of
sensitive techniques that enable fossils to be better visualized, manipulated
digitally, and analyzed chemically, and the need to integrate palae-
ontological data into time-calibrated phylogenies, have provided a wealth of
new opportunities to consider fossil parasites again. The combination of
frustrations balanced by advances and opportunities provided the impetus for
this volume. Fortuitously there are also currently many active researchers
considering fossil parasites and their role in better understanding the nature
of parasitism in evolution, disease and ecology. The sheer diversity of
approaches and innovations further merits a renewed perspective, not least
to demonstrate how much more integrative the study of parasitology has
become.
This volume aims to demonstrate that direct and indirect evidence from
the fossil record can be crucial in a variety of ways, providing empirical,
complementary and supplementary evidence in testing and developing
hypotheses on the nature of parasite diversity, phylogeny and host associa-
tions through space and time. In the first chapter, Kenneth De Baets and
Tim Littlewood review recent discoveries of fossil parasites and vectors and

xi j

xii Preface

consider them in their phylogenetic context, highlighting emerging tech-
niques and pathways for further progress. The fossil record of soft-bodied
parasites is understandably poor, but George Poinar’s contribution and that
of De Baets and co-workers, each explore how the fossil record of parasitic
helminths might be richer, or at least ‘less poor’, than that of their free-living
relatives. Poinar concisely discusses the evolutionary history of nematode
parasites of invertebrates, vertebrates and plants based on fossil remains in
amber, rock and coprolites ranging from the Palaeozoic to the Holocene
drawing from his long personal research on this topic. De Baets and co-
workers review the fossil record of parasitic flatworms for the first time and
illustrate how fossil and geological evidence may be used to calibrate
molecular clocks. Christina Nagler and Joachim Haug comprehensively
review the fossil record of insects, which includes some of the most
important terrestrial parasites, parasitoids and vectors today.
In reviewing the fossil record of crustacean parasites and hosts, Adiël
Klompmaker and Geoff Boxshall demonstrate that characteristic pathologies
and traces in hosts with fossilizable skeletons can provide a less patchy record
of parasitism compared with the body fossil record, thus demonstrating the
need to better understand and detect such traces. Pathologies in several other
groups of hosts with hard parts can be linked with parasitism, particularly in
bivalve molluscs, echinoderms and colonial organisms. John Huntley and
Kenneth De Baets discuss the indirect record of trematode flatworms in
bivalve shells. Stephen Donovan adds a new take on evidence for ecto-
parasitism on echinoderms, a group with a remarkable fossil record and one
that has captured numerous lesions, traces, burrows and attachments since
their appearance in deep time. Paul Taylor reviews for the first time the fossil
evidence for parasitism in fossil colonial organisms including sponges,
bryozoans, corals and graptolites and reveals a number of questions and
conundrums. In spite of this wealth of damage and evidence of association,
the identity of the perpetrators and the true nature of their associations
remain open to interpretation and speculation. For these predominantly
marine taxa, it seems that modern studies of parasite ecology in marine
environments may yet reveal more about ancient associations, and the
nature of traces caused by species (likely extinct) in other organisms also
extinct. The systematic review of fossil evidence at least provides focus for a
renewed search amongst modern marine assemblages.
Last but not least, the field of palaeoparasitology is drawn considerably
from techniques and methods introduced and still being developed rapidly
in the study of human parasites at archaeological sites. Drawing from a

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. 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. Timothy J.Preface xiii 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. famous and simple peasantry provide insights into archaeology as well as anthropology. Fascinating personal natural histories of the rich. Considering the links between human health. Littlewood October 2015 . Piers Mitchell provides the final chapter with a focus specifically on Medieval European parasite remains. The constraints of parasitic infections on lifestyle. Kenneth De Baets and D. medical practice and parasites.

1.debaets@gmail.apar.2. Techniques for Ancient Parasite Discovery 4 2.1016/bs. Erlangen. 1 .2 Trace fossils and pathologies 18 3. Littlewoodx. D. the timing of events and the resolution of the nature of the intimate relationships between parasites and their hosts in deep time remain problematic.doi.3 Coprolites 22 4.1 Body fossils 14 3. j ISSN 0065-308X http://dx. Volume 90 © 2015 Elsevier Ltd. However.2 Palaeoproteomics 7 3. 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.2. Despite its vagaries. London.ac.uk Contents 1. the fossil record provides the only direct evidence of parasites and parasitism in the fossil record of extant and extinct lineages. 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. Germany x Department of Life Sciences.com. Friedrich-Alexander-Universit€at Erlangen-N€urnberg.1 Ancient DNA 6 2.1 Thin sections and computed tomography 5 2.2 Ancient biomolecules 6 2. Natural History Museum. Other novel methods promise to provide additional evidence for the presence or the life habit of pathogens Advances in Parasitology. t.littlewood@nhm. Here. Introduction 2 2. 1 *Fachgruppe Pal€aoUmwelt. GeoZentrum Nordbayern. Molecular Perspectives on Parasite Phylogeny and Evolution 26 4.2015. Timothy J.2 HGT and ‘parasitic DNA’ 34 5.001 All rights reserved.07. UK 1 Corresponding authors: E-mail: kenneth. CHAPTER ONE The Importance of Fossils in Understanding the Evolution of Parasites and Their Vectors Kenneth De Baets*.1 Molecular clocks 29 4.org/10. The Parasite Fossil Record 8 3.

for example. the evolutionary history of parasites is still poorly known. as evidenced by its convergent appearance in numerous lineages and its sheer absolute and relative abundance among extant biodiversity (Poulin and Morand. 2003). at least as a working hypothesis. including the discovery and analysis of ancient DNA and other bio- molecules. early divergent gyroco- tylidean cestodes found only parasitizing early divergent ‘primitive’ holoce- phalan fishes (Xylander. or rather inadequately explored. In these cases. despite their importance and ubiquity. 2003). Antagonistic interactions. INTRODUCTION Parasitism is one of the most successful modes of life. Timothy J. Littlewood and their vectors. 2001). 2012). For instance. is a difficult but as yet a largely unexplored means by which ancient associations may be revealed. it is tempting and compelling to assume a long and ancient association. not in the least because of the traps set by multiple assumptions (Page. 1. in the form of arms races between parasites and their hosts. This focus is narrow and fails to provide the wider evolutionary picture or an appreciation of the influence of parasitism on. when the timing of a host’s divergence can be estimated from molecular or preferably fossil evidence. Indeed. biodiversity. Establishing time-calibrated evolutionary frameworks to test the origins and radiations of parasites in parallel with studies on environmental param- eters. Parasitologists have often resorted to more circular lines of evi- dence.. 2001). it is here that most of the research effort is focused.. a calibration point for the parasite’s association also appears tractable. 2014) and might also have contributed to the origin of sexual repro- duction (Mostowy and Engelst€adter. a phenomenon not helped by their inadequate. have been considered important drivers of evolution (Zaman et al. 2000). as well as computed tomographic methods. fossil record (Littlewood and Donovan. veterinary or economic importance (Bush et al. Because parasitism also has an obvious societal importance with many parasitic taxa being of significant biomedical. phylogenies of hosts and parasites need to be untangled to better understand . where extant hosteparasite associations appear to be combinations of early divergent hosts and early divergent parasites. or the degree of coevolution between parasites and hosts. and as part of.2 Kenneth De Baets and D. Assumptions of cophylogeny are common but bring their own suites of problems. To reveal coevolutionary patterns. such as extrapolating from current host associations or distributions to put time constraints on the origins and evolution of parasites.

Koutsovoulos et al. 8. Katzourakis and Gifford.. to characteristic traces of preserved biomolecules in host remains (Dittmar. 2011. Usually such sampling relies on phylogenies determined from extant organisms and pays little heed to loss of lineages through extinction. 2012. where DNA from one organism can be detected buried within the genome of another. Accurate estimates of histor- ical events such as co-divergence. Dunlop et al. duplication or loss of an association require complex mathematics and computationally demanding algorithms. Of particular note have been advances in X-ray. Whilst these studies can be profitable.. Ford Doolittle considers horizontally transferred DNA fragments as ‘basically parasites’ (p. electron and laser-beam techniques. although perhaps not widely considered as such.. 2015) that have been parts of their host genomes for a considerable length of time. Gitschier. Addi- tionally. ranging from exceptionally preserved parasites and eggs assignable to modern (even family level) lineages (Cressey and Boxshall..The Importance of Fossils in the Evolution of Parasites 3 historical relationships. to a remarkable level of detail and resolution (Cappellini et al. 2014). Another facet of palaeoparasitology. 2010. Indeed. Katzourakis.. 1989. particularly collagen within bone. Da Silva et al. The past decades have seen a wealth of new discoveries. textures and underlying chemis- tries (Mietchen et al. Wood et al. 2014.. advances in mass spectrometry have allowed the detection and characterization of amino acid traces. and any estimate is contingent upon adequate sampling (Charleston and Perkins. 2014). Palaeontological data could also have a bearing on testing of how parasiteehost associations respond to environ- mental changes across longer time-scales and to what extent parasites could be prone to (co)extinction (Dunn et al... 2006). Gilbert et al.b. These so-called ‘genomic fossils’ offer clues as to the origins and nature of ancient associa- tions (Gilbert and Feschotte.. Sutton. Greenwalt et al.. 2013b). 2014). 2010. ion. Such techniques open up the prospect of detecting traces of parasites and para- sitism more frequently and revealing key systematic features and morpho- logical characters indicative of a parasitic way of life.. 2013. Schiffbauer and Xiao.. is the study of horizontally (laterally) transferred DNA including transposable elements. 2013. as well as extinctions. Cunningham et al. serial grinding/imaging techniques and magnetic resonance tomography characterizing fine structures. HGTs . 2010. 2014). direct evidence from the fossil record remains the most compelling evidence for past historical and deep evolutionary associations. The rise in genome studies has provided ever-increasing evidence for horizontal gene transfers. Sutton et al. 2009. 2014a. 2009). Hugot et al. 2008. 2008. but the task is complex.

Okamura and Gruhl. Wood et al. 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. 2015). 2014. see Scholl et al. Hartikainen et al. Regardless of approach. 2013b. Parasitic plants offer a particularly rich resource for understand- ing HGT (Davis and Xi... convergence or specializa- tions in their morphology that make homology assessment difficult. bdelloid rotifers: Gladyshev et al. Sum- mers and Rouse.. further possibilities and frustrations associated with using the fossil record in constraining the origins and evolu- tion of parasitism.g.. 2011. Timothy J. and grinding tomography) and nondestructive methods (e.. phase contrast synchrotron or microcomputed tomography. although such events detected among Metazoa appear to be more common in some groups (e. 2008) than in others. rehydratation or resedi- mentation techniques. 2015. Morphologically based classifications of parasites have proved chal- lenging due to frequent apparent simplifications. 2002. TECHNIQUES FOR ANCIENT PARASITE DISCOVERY Various destructive methods (thin sections. Blaxter and Koutsovoulos. 2015). 2.g. it is clear that genomes may also be gleaned for evidence of relictual genetic elements of nonhost (“parasitic”) origin.. 2015. Increasingly these can be supplemented with analyses of ancient . time points gathered directly from fossils or inferred from calibrated phylogenies remain critical in understanding when. which make it possible to more fully exploit information buried in fossil or genomic sequences of their hosts. Littlewood and Waeschenbach. 2004). 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.4 Kenneth De Baets and D. for example. 2003. We highlight novel methods. Littlewood. 2003). Whereas palaeontology looks towards the earth’s fossil and subfossil record for ancient biotic interactions.g. Littlewood (e. novel molecular methods. where and to some extent how hosteparasite interactions took place and how they might respond in the future. Here we provide an updated perspective on the merits. 2014. Lockyer et al. However. used with caution. mCT) are particularly relevant to discovering and characterizing the morphology of parasitic remains or host responses in older (fossil) samples.

Ara ujo et al. 2015). 2010). However. because of the destructive nature of the grinding technique. Today. 2013. Dentzien-Dias et al.The Importance of Fossils in the Evolution of Parasites 5 biomolecules. Dunlop et al. 2015) to provide evidence for helminth eggs or other parasitic remains in fossil coprolites (Poinar and Boucot.... exceptionally preserved fossil samples (Briggs and Summons. 2005). which had been the subject of some considerable speculation in the literature (Waloszek et al. Such investigations typically rely on thin sectioning and various dissolution/rehydration/resedimentation methods. computed tomography has only been rarely used to test such assertions (Dittmar et al.. Unfortunately. Phase contrast tomography and other tomographic methods are however ideally suited to characterize fossils in three dimensions (even in nontransparent amber) and corroborate . whereby 3D reconstruc- tions of serially sectioned material are rendered and visualized by computer.. pentastomids mostly parasitize terrestrial ver- tebrates exclusively as endoparasites. it has been suggested that these forms were parasitic on marine vertebrates (Sanders and Lee. 2014). 2014).1 Thin sections and computed tomography Various studies have demonstrated the merit of conventional preparation and imaging methods used for archaeological samples (Araujo et al. or analyses of more resistant biomolecules in older.. (2015) not only reveals a new host association but also shows the parasite as ectoparasitic.. the fossil now exists only as an image. which have been largely based on microscopic methods. 2013. The new Silurian record by Siveter et al. 2012). is developing rapidly as a means by which high resolution differentiation can be achieved from the fossilized remains of small and even soft-bodied organ- isms. 2011. Not only did this discovery reveal the first fos- sil occurrence of an adult pentastomid but also its host association.. including ancient DNA (aDNA) in younger (archaeological) samples.. One such case has recently revealed the remarkable discovery of a putative fossil pentastomid found in association with its ostracod host entombed for 425 Ma (Siveter et al. and although extinct representatives have been identified in Cambrian marine sediments at a time before these terrestrial hosts existed. the resolution of parasites and evidence of parasitism often remains a serendipitous by-product of investigating fossil microstructures. Computed tomography (Sutton et al. which destroy the original 3D structure and/or association of the parasites and may lose less-resistant parasite remains (Dufour and Le Bailly. Da Silva et al. 2014a).. 2015). Ara ujo et al. Wood et al. 2014). 2006. 2013b. 2. Although many reports for terrestrial parasites or vectors come from amber (Poinar. 2008..

Advances in chemical analysis at the nanoscale. 2015). Novel approaches (Wood et al. confirmed its association to a waterbird ectoparasite (Wappler et al.. Greenwalt et al. 2013. 2013). 2. Littlewood parasite/vector interpretations as it has been used for phoretic associations (Dunlop et al.. 2014). 2013 and Cano et al. Penney et al. Bertazzo et al. therefore. Yao et al. may provide the tools to improve and apply these techniques in recognizing parasites and their influence on hosts in the fossil record. Preservation of feather remnants in a louse specimen’s foregut. 2014).. 2014). at least under certain conditions (Briggs. 2011. 2013. A better understanding of taphonomy (Briggs. but other complex organic structures such as iron-stabilized haem. 2013. for example.. the possible identity of the hosts. 2015..2.2 Ancient biomolecules Novel techniques make it possible to identify biomolecules (Greenwalt et al.. 2014. 2009. 2014).6 Kenneth De Baets and D. Large and fragile molecules such as DNA cannot survive fossilization (Briggs and Summons.. Dittmar et al. although it can only be detected and character- ized reliably in exceptionally well-preserved material up to 1 Ma (Hebsgaard et al. as applied to parasitic groups.. 2... 2014). 2005. Yao et al. 2014. 2012). Timothy J. 2012.. opens up a whole new world in revealing ancient colours. pigments. Wood et al. and as applied to fossils. opening up the prospects for protein-based detec- tion methods (Cappellini et al. The most familiar one is probably aDNA. microbiomes... can survive for longer.. 2014).. Dittmar. 2013b) focus on the amplification of total DNA of whole samples followed by the application of next generation sequencing . which has been applied to various parasitic (sub)fossils (Dittmar. 2013b).1 Ancient DNA Earlier aDNA studies focused on PCR to amplify specific short gene sequences targeted for particular parasite groups or species from single sam- ples (reviewed in Dittmar. 2014) in ancient remains and samples. 2011. This can be used as an extension to the analysis of gut contents of isolated parasite or vector remains to get an indication of the trophic targets and.. and the hidden remnants of soft-bodied organisms (Briggs and Summons. Briggs and Summons. Certainly there seems room for developing and applying these techniques to subfossil (unmineralized) remains where eggs are found intact without DNA and without clear morphological identity (see also Linseele et al. Briggs and Summons. Vinther. 2004). Dittmar et al. 2009.

. which has been crudely defined as a composite of collagen (protein) and hydroxyapatite (mineral) (see Hill et al. The application of palaeoproteomics more broadly to parasites or to other fossil remains. The characterization of the constituent peptides of fossil bone proteins. 2013. In spite of remarkable progress. can persist for w45 ky. 2014). Yao et al. requiring mass spectrometry. 2007). Subsequent bioinformatic interrogation of the data for various groups of parasites has been established in the field of metagenomics and environmental samples (Dittmar. palaeoproteomics can be a rewarding insight into ancient proteins. see Ostrom et al.. osteocalcin. in the hope of finding evidence for parasitism. 2009) and a 68-my-old Tyrannosaurus rex (Asara et al. and the second most abundant protein.2. However. 2013b). for vertebrates at least. (2012) and Collins et al.. the prospect of verifying the presence of porphyrins in fossilized haematophagous insects (Greenwalt et al. 2015). is in its infancy. aDNA techniques will always be constrained by the rapid deterioration of DNA. Hofreiter et al. 2012).The Importance of Fossils in the Evolution of Parasites 7 platforms for shotgun sequencing. 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. Brachylophosaurus canadensis (Schweitzer et al. the study of fossilized bone.. 2015). Collagen.. suggests that collagen (the most abundant protein) can survive up to 340 ky at 20  C. Certainly. some of these studies have attracted some criticism (Pevzner et al. has been isolated from vertebrate fossils of considerable age. 2009.. 2014) seems a tractable goal.2 Palaeoproteomics DNA is not believed to survive in sufficiently long lengths for sequencing over longer geological timescales (>1 Ma) (Hebsgaard et al. 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. (2000). 2. even putative erythrocyte remains were reported in dino- saur bones (Bertazzo et al. but analysis of more resistant biomolecules than DNA might make it possible to test other hypotheses associated with parasites or host- related biomolecules. providing evidence for phyloge- netics and an understanding of bone biochemistry (Wadsworth and Buckley.. 2008).... Recently.. (2000). has shown that. . in particular. Briggs and Summons. 2015). 2005. 2014) and is rarely found well preserved. including an 80 million year (my)-old Campa- nian hadrosaur. Wood et al.

limitations and associated frustrations.8 Kenneth De Baets and D. We will discuss the different sources of fossil evidence. 2015a) or weakly sclerotized arthropods (Cressey and Boxshall. 2015a. The fossil record of parasitism has been reviewed on various occasions (Conway Morris. 2015. 2010) with some others focusing particularly on marine parasites (Baumiller and Gahn. 2002. but also for various soft-bodied metazoan parasites such as helminths (Littlewood and Donovan. Huntley and De Baets.. The fossil record can also provide direct evidence for pres- ence of parasiteehost associations e some of which might now be extinct. Characteristic traces or pathologies in the skeletons of their hosts are more common and can be traced more continuously over longer timescales. Nagler and Haug. 2014a). Major important fossil discoveries of metazoan parasites and pathogens distributed by vectors underpinning our understanding of the ancient history of hosteparasite associations are detailed in Table 1. 2003. Littlewood 3.. bacteria and protozoa (Poinar. 2015). 2002. 1981. but the taxonomic affinity of the culprits is not always easy to disentangle (Donovan. 1990. 2015. 2002. Klompmaker and Boxshall. 2014a). and lack hard tissues (Conway Morris. 2011. 2015. Klompmaker and Boxshall. and hosteparasite interactions. Fossil pentastomids were long thought to be rare and restricted to the CambrianeOrdovician sites with Orsten preserva- tion. 2015). may go through some life cycle stages away from their hosts. 2003. Littlewood and Donovan. 2011). 1989.. THE PARASITE FOSSIL RECORD The fossil record of parasites or other pathogens is usually poor because they often reside within their hosts or vectors. Timothy J. Huntley and De Baets. Baumiller and Gahn. The table reveals considerable diversity of hosts and parasites. 2015. 2005a) or terrestrial pathogens (Labandeira. Castellani et al. New finds also highlight the potential of finding evidence in coprolites for parasitic remains in both marine and terrestrial realms. 2003. and amber as sources for haematophagous vectors. De Baets et al. 2015. Body fossils of parasites are rare and usually restricted to sites of exceptional fossil preservation (KonservateLagerst€atten). Boucot. Rouse. 1981. but new discoveries highlight they might be more common than . Poinar. Taylor. their merits. particularly those still associated with the remains of their hosts providing direct evidence of parasitism. Dittmar. Poinar. Boucot and Poinar. De Baets et al. Labandeira. 2010. Littlewood and Donovan. are small. 2002. as well as the impact of parasitism on their hosts in the geological past. This is particularly true not only for viruses.

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.Table 1 Ancient history of hosteparasite associations Higher taxon Taxon Fossil evidence Age Source Host References Environment Bacteria Spirochaetes Palaeoborrelia Direct: spirochaete. Poinar (2014b) T dominicana like cells Rickettsiales Palaeorickettsia Direct: rickettsial-like Early Cretaceous Amber Cornupalpatum Poinar (2015b) T protera cells burmanicum Eukaryota Metamonada Parabasalia: Indirect: lesions Cretaceous Skeletal Tyrannosaurus rex Wolff et al. (1992) A. (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. (1992) Archeococcidia antiquus. Direct: aDNA in Holocene Coprolite Moas Wood et al. Indirect: oocysts Pleistocene Coprolite Ground sloth Schmidt et al. Miocene Amber Amblyomma sp. (2013b) T Eimeriorina coprolite Eimeria lobatoi Indirect: oocysts Holocene Coprolite Deer Ferreira et al. 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) .

b) Paleoleishmania Direct: erythocytes Miocene Amber Lutzomyia adiketis Poinar (2008b) T neotropicum Phylum Arthropoda Copepoda ? Indirect: exocysts Jurassic Skeletal Crinoids. Castellani et al. echinoids Mercier (1936). (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) .b). deformation Radwa nska and Radwa nska (2005). (2005a.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. Cressey and Boxshall (1989) Isopoda ?Bopyridae Indirect: swellings ?Early Jurassic. 10 species Direct: phosphatized Cambrian Calcareous ? early chordates. Waloszek et al. (2011). (1994). Middle Skeletal Crustacea Klompmaker et al. M JurassiceRecent deformation (2014). Waloszek from host Silurian? et al. Waloszek and M€ uller M remains isolated eOrdovician. Radwanska and Poirot (2010) Kabatarina pattersoni Direct: Early Cretaceous Calcareous Fish Cressey and Patterson M nodules (1973). Klompmaker and Boxshall (2015) Pentastomida 5 genera. nodules ostracod (1994). Siveter et al.

l.Thecostraca ?Ascothoracida Indirect: borings Cretaceous Skeletal Echinoidea Madsen and Wolff M deformation (1965) ?Ascothoracida Indirect: borings Cretaceous Skeletal Octocorallia Voigt (1959). (2014) F (Athericidae) deposits Phylum Nematoda Ascaridida Ascarites rufferi Indirect: eggs Upper Triassic Coprolite Cynodont Da Silva et al. (2012). T host deposits and/or small Huang et al. Paleopsylla: 4 species Direct: isolated from Eocene Amber ?mammals Dampf (1911). (2013). mammals Gao et al. (2014) T (Heteroxyne- matidae) (Continued) . Gao et al. Huang (2014) Siphonaptera s. dinosaurs Gao 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. (2013). (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. (2012). Beaucournu (2003) Phthiraptera Megamenopon rasnitsyni Direct: isolated from Eocene Lacustrine ?water birds Wappler et al.s. Huang et al. T host Beaucournu and Wunderlich (2001). (1967) M deformation Insecta Siphonaptera s. Pseudoculidae Direct: isolated from JurassiceCretaceous Lacustrine ?pterosaurs. (2014).

M developing embryo (2013). T (1999) ?Gymnophallidae Early Eocene Indirect: characteristic Skeletal Ruiz and Lindberg M pits in bivalve shells deformation (1989). De Baets et al. (2015a) . De Baets et al.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. structure sediments acanthodians 2011). Todd and Harper (2011). Upeniece (2001. (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. (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. Huntley and De Baets (2015) ?Monogenea Middle Devonian Direct: attachment Fine-grained Placoderms.

(2012). M eJurassic deformations (galls) Hess (2010) Clitellata ?Hirudinae Triassic Indirect: cocoons Freshwater ? Manum et al. Fry and Hall (1969). Anodonta Quaternary Direct: glochidium Freshwater ?fish Brodniewicz (1968) F larvae deposits . (1998) 1 species. (1991). F deposits Bomfleur et al. (1994) Phylum Annelida Myzostomida ? Carboniferous Indirect: skeletal Crinoids Welch (1976). Parry et al. OligoceneeMiocene Direct: shells associated Skeletal Corals (Cladocera. Galeropsis: Pocillopora) 1 species Unionidae Unio. T humans) Noronha 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.Phylum Acanthocephala ? ? Holocene Indirect: eggs Coprolite Mammals (canids. Lozouet and Renard M Coralliophila: with coral host deformation Thegioastraea.

Nagler and Haug. which goes as far back as the middle Triassic (Skawina and Dzik. Other important Konservat Lagerst€atten for the preservation of parasites include phosphatized remains of arthropods (Cressey and Patterson. Maas et al. claims that Cambrian tardigrades (Muller et al. 1989.. 2015a). eggs or cysts are known. 1989. Siveter et al. In rare cases. Cressey and Boxshall. The body fossil record is restricted to sites of exceptional preservation. 2008) in ..1 Body fossils Body fossils are usually defined as remains or representations of the whole or actual parts of organisms (Goldring 1999. but in some cases it can only be corroborated by finding the parasite in situ parasitizing its host. body fossils of nonparasitic life stages of extant parasites hint that their parasitic life stages might potentially also be present (e. which suggests that this is a synapomorphic trait for this group.. 2001. 2011). 3. 2015). the oldest fossil glochidia cannot be used to test this hypothesis as they are only found as late as the Pleistocene (Brodniewicz. 2015). 1973. parasite body fossils are still associated with host remains. while in other cases they are isolated. 1995) have certain resemblances to extant parasitic forms. to nematodes exiting their dying hosts (Poinar. All extant members of Unionida have parasitic larvae. but this can only be confirmed by future discoveries (Skawina and Dzik. Further work needs to be done on establishing characteristic trace fossils and pathologies. In exceptional cases. Labandeira (2002)... 2014a. making it difficult to identify the hosts or even decide if these forms were parasitic or not.g. 2011. Maas and Waloszek. 2006) in carbonate nodules (the so-called Orsten preservation).14 Kenneth De Baets and D. silicified nematodes (Poinar et al. particularly in verte- brates. 2007). Often. Littlewood expected even during different ages. Timothy J. 2015a). 2015). for example. which indicates at least a possible phylogenetic relationship and potentially a mode of life. back in time. which can still be characterized sufficiently to assign them to particular taxa (De Baets et al. 1968). Establishing them as parasites is usually achieved by comparing them with the morphology of modern relatives or analogues. Such fossil Lagerst€atte should therefore be systematically screened for parasites. parasitic stages of arthropods or unionids). parasites are so well and completely preserved that they can be accu- rately assigned to modern taxa (Cressey and Boxshall. only sclerotized attachment organs. Unfortunately. but this still needs to be further corroborated. One of the most important types of preservation is found in fossil ambers which have preserved the remains of unicellular pathogens from a variety of terrestrial parasitic arthropods (Nagler and Haug. Foote and Miller. In other cases.

. In some cases.. Hemiptera (Yao et al. ectoparasites are still attached or associated with their hosts. larvae (Ferreira et al.. but are known to be transmitted by various vectors.The Importance of Fossils in the Evolution of Parasites 15 hydrothermal vent environments (the so-called Rhynie Chert preservation). The latter includes oil shales deposited not only in maars or other lacustrine environ- ments (Wappler et al. Fossils of modern-type fleas can be traced back to the Eocene at least .c. fine-grained lacustrine or marine deposits where the remains were quickly buried and/or anoxic environments contributed to fossilization. Direct fossil evidence for vector feeding behaviour is even rarer than parasitism (Table 2). are sometimes also recovered from coprolites. 2014a). so that Phthiraptera. 2014). Possible exceptions include the recent discovery of haemoglo- bin-derived porphyrins in the stomach content of an Eocene mosquito (Greenwalt et al. Poinar and Telford. 2004. eggs including those with developing embryos. 2011b. 2006). 2013).. Greenwalt et al.2).b. 2014. Poinar. 2006. but also in low energetic. one of the many types of trace fossils (see Section 3. Nagler and Haug. Some unicellular pathogens have also been reported from fossil and subfossil archosaur coprolites. Poinar.. Direct evidence for vector behaviour of haematophagous taxa has been restricted so far to amber deposits (Poinar and Poinar. 2013b). 2015b). Most common vectors are arthropods which feed on blood. 2014b. 2013.. Wood et al. marginal marine or deeper marine environments. which are mainly specialized on mammals. Such morphological adaptations have even been used to suggest ectoparasitic behaviour in lineages where larvae are no longer parasitic (Chen et al. Pe~ nalver and Pérez-De la Fuente. 2004). 1993) or remains of juveniles. although microscopic taxa are harder to identify in older occurrences than in more recent occurrences where aDNA is available (Poinar and Boucot.. 2005a. 2015). 2015). Hughes et al. 2010. 2013) as well as higher Fe contents in fossilized true bugs.. probably evolved later than did fleas (Nagler and Haug. which might themselves fossilize. while earlier reports are most likely erroneous determinations of mites (Dalgleish et al. 2013. Cysts. Greenwalt et al. 2014). Protozoan parasites or other pathogens like viruses and bacteria are usu- ally hard to verify in the fossil record (Frías et al.. 2004b. Our ability to identify parasitic and haematophagous insects is mostly based on their possible taxonomic affinities and morphological adaptions of their mouth parts or other structures similar to extant taxa (Lukashevich and Mostovski. Modern-type lice can be traced back to the Eocene (Wappler et al. although forms feeding on feathers or hairs might also be involved.... Poinar. 2003. 2005. while endoparasites are still found in situ within their hosts or escaping their dead hosts.

Timothy J. (2013) concentrations. (2014) . Direct Fe ? Kishenehn Formation Greenwalt et al. Kenneth De Baets and D. Indirect Spirochaete-like cells Dominican amber Poinar (2014b) Diptera Ceratopogonidae Proticulicoides sp.b) Lutzomyia adiketis Indirect Trypanosomatidae Dominican amber Poinar (2008b) Streblidae Enischnomyia stegosoma Indirect Plasmodiidae Dominican amber Poinar (2011b). Boucot and Poinar (2010) Leptoconops nosopheris Indirect Trypanosomatidae Burmese amber Poinar (2008a) Culicidae Culiseta sp. Poinar and Brown (2012) Hemiptera Reduviidae Triatoma dominicana Indirect Trypanosomatidae Dominicsssan amber Poinar (2005c) Torirostratidae Torirostratus pilosus Direct Fe concentrations ? Yixian Formation Yao et al. Littlewood porphyrins Culex malariager Indirect Plasmodiidae Dominican amber Poinar (2005a. Indirect Plasmodiidae Burmese amber Poinar and Telford (2005).b) Phlebotomidae Palaeomyia burmitis Indirect Trypanosomatidae Burmese amber Poinar and Poinar (2004a. 16 Table 2 Body fossils of haematophagous vectors Taxonomy Species Haematophagy Parasite Source References Arachnida Ixodidae Cornupalpatum burmanicum Indirect Rickettsial-like cells Burmese amber Poinar (2015b) Amblyomma sp. (2014) Torirostratidae Flexicorpus acutirostratus Direct Fe concentrations ? Yixian Formation Yao et al.

The oldest evidence for the presence of fungi parasitic on animals derives from the Cretaceous period (Sung et al. 2014b. gut contents or coprolites of fossil parasitic invertebrates (Wappler et al.. 2013. 2013). but can also be induced by viruses. 2014).The Importance of Fossils in the Evolution of Parasites 17 (Perrichot et al.. at least at higher taxonomic levels (Dentzien-Dias et al. Host associations with dinosaurs and pterosaurs have been suggested for stem-group fleas (Huang.. Fossilized galls can also be important sources of information on planteparasite interactions (Knor et al.. Huang et al. 2014. Archaeological exam- ples frequently allow species level identifications of helminth eggs (Dittmar et al. 2013. Huang. 2013. sandflies (Phlebotominae. 2012). is less strict. nematodes and mites (Knor et al. 2013. including blackflies (Simulidae). Diptera can be traced back to the PermianeTriassic... as well as other remains found alongside. 2013) or verte- brate hosts (McConnell and Zavada. fungi can also be vicious pathogens of animals and plants (Sexton and Howlett. 2015b). 2013. 2012. the characteristic response of the host to a fungal parasite can also be preserved (see Section 4.. 2013.. 2014. 2008). 2014a. Blood-sucking is inferred to be ancestral in this group and members of various lineages are important vectors (Poinar.. have allowed parasite remains to be confidently attributed to major host groups. but a novel molecular study suggests that the earliest fleas appeared in the early Cretaceous era and had a strong as- sociation with mammals. 2012. 2014. 2014). Sometimes. 2015). 2006). 2011). 2008). Nevertheless. compare Table 2). Finding direct evidence of Jurassic or Cretaceous fleas associated with host remains would be the smoking gun to resolve this issue..2). Labandeira and Currano. 2015). bacteria. Da Silva et al.. whereas the Jurassic stem-group forms are only distantly related (Zhu et al. The earliest evidence for Metazoa parasitizing a plant is nematodes found within early land plants (Poinar et al. Psychodidae) and mosquitoes (Culicidae). The relationship between hosts and other haematophagous insects.. Nagler and Haug. 2004. Leckey and Smith. 2008).. 2015). although several extinct families of putative stem- group Siphonaptera have been reported from the Jurassic and Cretaceous pe- riods (Gao et al. Ticks are also important vectors for Spirochaetes and Ricketsiales. 2013). Hugot et al. Note that galls are often caused by parasitic insects.. Greenwalt et al. fungi.. Bed bugs and their close relatives can probably be traced back to the Eocene (Engel. which are also important vectors. Even when isolated from their hosts. which might have been already the case since the Cretaceous period (Poinar. Direct evidence for both haematophagy and their vectors is only known from Diptera (Greenwalt et al. . 2015).

which is more or less consistent with the origin of their final hosts (extant shorebirds). 2015. 2015) and (?bopyrid) isopod swellings in decapods (Weinberg Rasmussen et al.. Taylor.2 Trace fossils and pathologies Various invertebrate hosts including arthropods. Klompmaker et al. Todd and Harper. 1959.. molluscs. 2009. Huntley and De Baets. 2015). 1976. However.. 2001. crustacean arthropods (Madsen and Wolff. it cannot be ruled out that they were made by another type of closely related parasite or organism with similar behaviour in the geological past. 2009) as well as borings in octocorals related to the presence of ascothoracid barnacles (Voigt. Huntley. 2015). these traces or pathologies are believed to be so character- istic that they are interpreted to represent the oldest fossil evidence for particular lineages in the fossil record. Hess. Timothy J. Ruiz and Lindberg. 1985. 2015). even in the case of such model systems. 2003. 1989. which is evidence of an infestation or association with parasites (Boucot and Poinar. 2005. Huntley and De Baets. and can be confidently traced into the Eocene (Ruiz and Lindberg. deformations in echinoderms attributed to myzostomid annelids (Welch. 2015. 1965. which are now extinct or where pathological reactions are not yet documented in extant hosts.18 Kenneth De Baets and D. Particularly in such cases. 2010. 2011. 2012. 2010. including castration of fossil decapods by rhizocephalan barnacles (Feldmann. 1989. Radwa nska and Radwa nska. 2015). 2015a. echinoderms and various colonial organisms can contain traces or pathologies in their skeleton. However.. Donovan. 2007. igloo-shaped concretions e attributed to . Boyko and Williams. 2015a. 2014. Littlewood 3. Huntley and De Baets. Todd and Harper. Ituarte et al. Other (now extinct) culprits can be sus- pected when the record of these structures is not so continuous and shows major stratigraphic gaps (Boucot and Poinar.. 2010) or eulimid gastropods (Neumann and Wisshak. 2008. 2005. For example: shell pits have been confidently linked with gymnophallid flatworms in extant bivalves. The most convincing palaeontological model systems are those where both extant and fossil parasiteehost interactions are compa- rably well studied such as the gymnophallid-induced pits and igloo-shaped shell concretions in bivalves (Campbell. 2014). Parry et al. which makes it possible to interpret the type of relationship between them. compare Klompmaker and Boxshall. Williams and Boyko. 1998. In some cases. trace fossils and associated pathol- ogies can not only provide direct information on the behaviour of the par- asites but also the response of the host.. De Baets et al. 2011. Radwanska and Poirot. 1967). 2010). Klompmaker and Boxshall. De Baets et al.

The Importance of Fossils in the Evolution of Parasites 19 gymnophallids in extant bivalves (Ituarte et al. 2005).. 2001. Furthermore. 1985. although their interpretation becomes more difficult if no modern analogues are available (Owen. 1985). offer less confident evidence for the presence of parasitic lineages in the fossil record than in body fossils. 2011). but as long as no parasite remains are found associated with them. Other au- thors have argued that a neutral interaction is absence of an interaction. Traces which are reminiscent of nematode borings in foraminifer tests (Sliter. Parasite-induced pathologies have also been reported from hosts that are now extinct or no longer affected.and cyst-forming myzostomids: Summers and Rouse.. De Baets et al.. Pathologies. Lozouet and Renard. Babcock. 1971) have been reported from Cambrian and Ordovician trilobites (Babcock. 2015b). are believed to have radiated sometime between the Cretaceous and Eocene periods (Smith. 2002). 2015b). Zapalski. 2014). their attribution to parasitic flat- worms remains highly speculative at best (De Baets et al. 2007). it is still debated whether these traces in trilobites were made during life or post- mortem (Owen... although this might be more a problem concerning the definition of parasitism rather than its recognition (Tapanila. 1980. which is not restricted to fossil associations. have also been reported from the Silurian (Liljedahl. therefore. 2015a) as shorebirds (Char- adriiformes). which are sometimes not that well-investigated. 1998. 2015). unless demonstrated otherwise. 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.g. 2011. Such traces are usually compared with known responses to parasites by extant hosts.. 2008. 2011). which is not consistent with extant parasiteehost associations (De Baets et al. Some authors like Tapanila (2008) have suggested that fossil studies should assume that a symbiosis is neutral (commensal). but no conclusive assignment to nematodes as culprits can be made without direct fossil evidence for associated nematodes. 2007. . De Baets et al. 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. and by extrapolation it has been assumed that the same culprits were responsible in the past. their present day definitive hosts. This can be further complicated by the fact that extant phylogenies indicate that pathology-inducing lineages might have evolved more than once (e. Baumiller and Gahn. when no parasitic remains are found associated with these traces. gall. Many palaeontologists also point out the difficulty of defining an inter- action as being parasitic. 1985).

for example. Zapalski (2011) has. 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. Character- istic skeletal pathologies in terrestrial vertebrates (e. while a certain positive effect for the parasite can be inferred. therefore. 1975) caused by digenetic trematodes or trabecula-like bone lesions in cetacean whales (Littlewood and Donovan.20 Kenneth De Baets and D. 2003) and enlargement of the frontal sinuses accompanied by bone lesions in mustelids (Rothschild and Martin.. Johnson and Sutherland. often most readily recognized in specimens with sparse traces or pathologies (De Baets et al. which can occasionally also be found in the fossil record.g. 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.. 2006. and is therefore unfit for empirical science. borings) or structures as being made in vivo.. Littlewood which cannot be proven. such inter- pretations rely on identifying the traces (e. Timothy J. 2013). 2003) or cavities in the mastoid bone of humans (Oyediran et al. 2011. (2009) studied erosive lesions in tyrannosaurs and attributed them to Trichomonas gallinae- like protozoans. Donovan. Pos- itive or negative effects can be detected or inferred based on comparisons with extant interactions. 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. One spectacular example is the death-grip scars found on Eocene .g. because the possibility of making a type II error is very high. Identifying traces or pathologies of fossil parasites can potentially also be performed by demonstrating a negative influence or effect on growth. 2002. In some cases. argued avoiding commensalism as a null hypothesis in palae- oecology. 2008). Some parasitic unicellular pathogens might leave characteristic traces or pathologies in their hosts. 2007.g. 2001. borings by foraminifera in marine echinoderms and bivalves (Neumann and Wisshak. because they are reminiscent of similar pathologies in extant birds caused by this parasite. Wolff et al. growth deformation or pathology) can be shown to be asso- ciated with these structures. 2015). 2003.. the host performs activities or exhibits behaviour induced by the parasites. body size and/or morphology of their hosts. and especially on those with external shells or exoskeletons. Of course. Studies have focused particularly on invertebrate hosts. This can be most convincingly demonstrated when a host response (e. Unicellular eukaryotes can also leave character- istic traces in their hosts. Beuck et al. 2006) caused by cestodes.

De Baets et al. This can be particularly relevant to predict the future response of parasiteehost systems to global change. Huntley and De Baets.. Such data can only rarely be obtained by looking at body fossil records of parasiteehost as- sociations. or at least characteristic. 2002. Baumiller and Gahn. 2014) and body size (Ruiz. although there are some pathologies which are believed to be diagnostic. Baumiller and Gahn. with some rare exceptions where both the host and the parasite have fossilizable skeletons (Lozouet and Renard. 2015). The link between the prevalence of parasites and pathologies. 2015. Klompmaker et al. Pathologies have their own problems as they are sometimes hard to assign to a certain lineage of culprits. Huntley and De Baets. Huntley and De Baets. 2014). the nature of the relationship and their effects might be context dependent (Bronstein. 1991. which can be tracked over millions of years (Brett. 1978. for parasitism. Trace fossils can give unique information on the behaviour and prevalence of the parasites and track the response of their host through geological time. 1994. the temporal and spatial record of parasite- induced pathologies in their hosts can be much more continuous than the parasite body fossil record. 2011. 2015.. 2015.The Importance of Fossils in the Evolution of Parasites 21 leaves. 2015b. This includes direct information concerning prevalence and virulence of this relationship.. Klompmaker and Boxshall. 2009). emerging fungal spores can be released into the wind from an elevated position. echinoderms. the fungal infection Ophiocordyceps forces ants to hold onto tips of leaves so that after the death of the ant. 2015. 2002) or where multiple similar taphonomic windows (e. particularly in molluscs. Irrespective of this problem. amber) exist.. 2012). 2014. colonial organisms and others with fossilizable skeletons (Donovan. Daskin and Alford. 2010).. Ruiz and Lindberg. 1998.. Klompmaker and Boxshall. as their record can be more continuous (less patchy) than that of body fossils which only fossilize in exceptional conditions. 1989. 2015). within pop- ulations and particularly individual hosts. 2015). Furthermore. Various preservation. as well as environmental factors such as sea-level and climate change (Huntley et al. and their possible relationship with host evolution including diversity (Klompmaker et al. This can provide valuable quantitative data on various aspects of parasitee host interactions. De Baets et al. might not be straightforward and has only rarely been investigated in extant hosts. where studies have suggested that parasites might be more prone to (co)extinction (Dunn et al. Taylor.g. interpreted to have been made by ‘zombie’ ants infested by fungi (Hughes et al.. collection and taxonomic biases can and should be accounted for in quantitative analyses of fossil .

. which have so far mainly focused on less specific (pred- atoreprey) interactions (Kelley et al. Jouy-Avantin et al. although the term is often also used for desiccated.. 2015).. 2013)... 2014.. However. 2003. Coprolites can therefore be an important additional source of ancient parasitism supplementary to amber. to helminths (Gonçalves et al. 1991. Leles et al.. 1992. Frías et al. Dentzien-Dias et al. 2010. where the record is heavily biased towards arthropods and their terrestrial parasites. 2005. Klompmaker and Boxshall. 2006. coprolites are found in isola- tion. Littlewood antagonistic interactions (Huntley and De Baets.. 2014). 1993.22 Kenneth De Baets and D... Huntley and Kowalewski. 2013).. 2007) rather than parasiteehost interactions. 1999. Timothy J. Schmidt et al. 1992. Wood et al. Savinetsky and Khrustalev. and. Poinar and Boucot. for example.. 2013). 1990). 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. more recent faeces from archaeo- logical sites (Ferreira et al. 2013b). Invertebrate coprolites might also have ... 2012). in the case of more recent specimens. 2006. more quantitative data and analyses on existing model systems are required. 2015. 1992. 2012). but particularly nematodes (Ferreira et al.. where the identity of the producer can only be inferred from their morphology and content (Poinar and Boucot.. Hugot et al. influence the invasion of molluscs by parasites on various organizational levels (Cheng and Combes.. Wood et al. To further progress in the field of quantitative palaeopathology in deep time. Various environmental factors can. 2003.3 Coprolites Coprolites are usually defined as fossilized (permineralized) faeces. 2014) and various groups of parasitic flatworms (Schmidt et al.. 2006. 1991. Palaeopathologies with a more continuous fossil record have the potential to be used to model the influence of parasite prevalence and virulence on the evolution of their hosts and how they are modulated by environmental parameters on longer time-scales. Hunt et al. Poinar and Boucot. 3. 1992. including acanthocephalans (Noronha et al. to parasitic fungi and plant remains (Sharma et al. by aDNA analysis (Wood and Wilmshurst. which makes it possible to confidently identify their origin and therefore the host taxon of the fossil parasites. In ideal cases. coprolites are still associated with their producer. Reinhard and Bryant. Da Silva et al. Coprolites have yielded fossil and archaeological evidence for para- sitic organisms (Table 3) ranging from coccidia or other protozoans (Ferreira et al.. as well as the need to identify additional modern and/or fossil analogues of already identi- fied parasite-related pathologies. 1994). 2013. most frequently. Dentzien-Dias et al.

(1993) Ascaridomorpha Eggs Triassic Cynodont Da Silva et al. (2014) Oxyurida Eggs Triassic Cynodont Hugot et al. (2013b) Pachyornis elephantopus) Helminths Platyhelminthes Cestoda Egg þ developing Permian ?elasmobranchs Dentzien-Dias et al. (1992) Cryptosporidiidae aDNA (Cryptosporidium) Holocene Moas (Dinomis robustus. (1999) Schistosomatidae Schistosome-like eggs Holocene Ground sloth Schmidt et al. (1992) (Nothrotheriops shastensis) Nematoda ? Larvae Pleistocene Hyenid Ferreira et al. (2013) embryo Trematoda Eggs Cretaceous Archosaur (?dinosaur) Poinar and Boucot (2006) Dicrocoelidae Eggs Pleistocene Mammal (?bear) Jouy-Avantin et al. Wood et al. (2014) (Continued) 23 . (1992) (Nothrotheriops shastensis) Eimeridae Oocysts (Eimera) Holocene Deer Ferreira et al. 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.

Dinornis. Megalapteryx) Trichocephalida Eggs (Trichuris) Pleistocene Hyenid Ferreira et al. (2012) taylorii) habroptilus) . Littlewood Lice Body remains Holocene Humans Fry (1977) Fungi Plant-parasitic fungi Spores Cretaceous Archosaur (?dinosaur) Sharma 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. Pachyornis. (2013b) (Anomalopteryx. Timothy J. (2008) Kenneth De Baets and D.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. (2005) Plants Root-parasite Pollen (Dactylanthus Holocene Kakapo (Strigops Wood et al.

In other cases.. 2006. 1991. or can be destroyed dur- ing the extraction or preparation methods. 2013).g. 2003). as demonstrated by reports of a putative trypanosome from faecal droplets found in association with a fossil triatomine in Dominican amber (Poinar.g. 2005c). 1999. 2013) or Mesozoic periods (Poinar and Boucot. Gonçalves et al. 1952.The Importance of Fossils in the Evolution of Parasites 25 the potential to reveal past parasite infections. thin sectioning. Tomographic methods might help to reveal additional details of fossils trapped in amber as well as help to discover parasites in coprolites or other ancient remains which can be destroyed during the traditional destructive . 2006. 2014)... which are body fossils. Gonçalves et al. Some of these coprolites range back to the Palaeozoic (Zangerl and Case. 2003. parasite eggs have often been found in coprolites or fossilized faeces. Hugot et al. dissolution/rehydration methods) and classical imaging methods leaving little chance for further study. Ara ujo et al. particularly in archaeological sites (Bouchet et al. 1976.. 1998) or Eocene mammal hair in Baltic amber (Voigt.. making computer tomography particularly important to identify parasites for older (fossil) samples. 2009). samples need to be rehydrated to extract DNA) and restricted to younger (archaeological) samples due to the rapid deterioration of DNA/RNA. parasite eggs have been reported associated with Cretaceous fossil feathers (Martill and Davis.. Da Silva et al. 2013b.. Egg remains are usually considered trace fossils. but they can occasionally contain remains of developing embryos (Poinar and Boucot. they can also be found in Quaternary sediments. 2015). As some of these eggs can be quite resistant to decay. Interestingly. which are trace fossils themselves. Traditional methods of parasite recovery from coprolites. Sequencing of aDNA might successfully detect very small and/or fragile parasites that may not preserve intact in coprolites.. Protozoa remains have also been reported from the abdominal region of Miocene Tapir remains (McConnell and Zavada. Nagler and Haug. Dentzien-Dias et al. or other ancient samples. This method is however also destructive (e. Jouy-Avantin et al. 2013) as well as in termites preserved in amber (Poinar... 2003.. 2015) or computed tomography.. although most are known from the Cenozoic. or have been missed or destroyed because of techniques designed to reveal structures of the hosts to which they are associated. Remains of fossil parasites have typically been revealed through destruc- tive preparation (e. can be combined with aDNA techniques (Wood et al. 2015). particularly the Quaternary era (Ferreira et al. Ara ujo et al. 2014. Dentzien-Dias et al.

4. Siveter et al.26 Kenneth De Baets and D. but were usually received with a certain degree of scepticism (Boucot. but their useful- ness depends on the contrast between the fossils and the matrix. 2015). 2015) as well as on parasite body size changes (Fugassa et al. 1976). Various methods can yield high-resolution reconstructions of microscopic remains or struc- tures in larger fossils including mCT-scanning or phase-contrast synchrotron tomography (Donoghue et al. Duan et al.. perhaps to place them in extant phylogenies (Faulwetter et al. 2). the coprolite producers. 2003). Poinar.. In archaeolog- ical studies. 2012)... Parasitic remains in fossil coprolites have been reported for a long time (Zangerl and Case. 2006. Dentzien-Dias et al. 3D structure and morphology or association in coprolites or other ancient re- mains (Dunlop et al. particularly in marine and terrestrial coprolites (Table 3) as well as in amber fossils (Tables 1. 2015. These could even provide supplementary information on the morphology and content of the coprolites. Garwood and Dunlop. 2005. Littlewood preparation processes. Timothy J.. Complex life cycles . MOLECULAR PERSPECTIVES ON PARASITE PHYLOGENY AND EVOLUTION Historically. but also to quantify their original position. 2006.. 2014). 2012. 2006. as well as give indications about possible predatoreprey relationships and parasite load. It could potentially be used to study the presence of developing embryos (Donoghue and Dong. Additional data are required to quantitatively study these aspects on longer (palaeontological) timescales as the parasitological coprolite studies are still quite patchy in space and time. 2013). which could make it possible to more confi- dently identify their host. high degrees of reduction or apparent simplification... Mitchell. Parasites often demonstrate high degrees of specialization compared with their free-living relatives. 1990.. Computed tomography can not only be relevant to identify and characterize parasite re- mains. specialization and/or conver- gence in morphology related to their parasitic lifestyle. for many taxonomic groups of parasites. coprolites can be quantitatively studied to establish changes in biogeographic distributions and habits of their hosts (Ara ujo et al. Sutton et al. Donoghue et al. 2014). 2008). which have been suggested to be present in some fossil eggs attributed to helminths based on traditional imaging methods (Poinar and Boucot. morphologically based systematic schemes and phylogenies have been difficult to resolve even in the light of additional sampling or analysis. The potential of these windows into parasite evolu- tion has become clear in the last two decades by multiple new discoveries. 2013..

2001.. Hartikainen et al.. 2007).. Okamura and Gruhl. as long as one can properly deal with biases and spurious signal related to long-branch attraction.. (host) contamination and other issues arising from a purely molecular approach (Edgecombe et al. 2014). Okamura et al. but most authors now agree that they belong within the Annelida based on molecular analyses (Parry et al.. 2013. 2015a. Acanthocephala (thorny-headed worms) were occasionally compared to priapulids (penis worms) based on morphological evidence (Conway Morris and Crompton. Summers and Rouse. 2015 for a review). The discovery of Chromera velia. which illustrate that the relative importance of particular gene regions needed to disentangle phylogenetic . are now considered to be closely related to fish lice based on molecular evidence (Sanders and Lee. Myxozoa are now considered to be cnidarians based on molecular evidence (Jiménez-Guri et al. 2008). with other taxa has been attributed to host contamination (Jiménez-Guri et al. 2014).. 2012). the first photosynthetic apicomplexan with a fully functional plastid. might also provide a powerful model to study the evolution of parasitism in Apicomplexa... 2014. although there are some exceptions (Laumer et al. 2015. long considered to be a separate phylum. 2003. For example... molecular studies have had a considerable impact on the assignment of some parasite groups within the broader context of metazoan evolution (Zrzavý. but might also be responsible for wrong assignment of various groups of extant parasites. 2015). De Baets et al. The phylogenetic position of myzostomids has also been long debated. indicating that the plastid of this coral symbiont shares its origin with the apicoplasts (Moore et al. Wey-Fabrizius et al. 2015).. Oakley et al. Edgecombe et al. 2010. 2011). Contamination is not only relevant for aDNA (Shapiro and Hofreiter.. 2013). Most recent molecular studies with greater coverage indicate a particular route to para- sitism within Platyhelminthes and a closer relationship between cestodes and trematodes (Lockyer et al. On the other hand. pentastomids. 2014. Previously erro- neous assignment of Myxozoa. including the vermiform Buddenbrockia. Also. see Littlewood and Waeschenbach. 2015. Okamoto and McFadden. Molecular methods have the potential to resolve many problems where morphology has been problematic. but are now aligned with Rotifera within the Syndermata (Weber et al. 2011). Egger et al..The Importance of Fossils in the Evolution of Parasites 27 involving multiple hosts or even a single host can consist of morphologically distinct ontogenetic stages making homology assessment and the identifica- tion of shared features even more difficult (Brooks and McLennan... 2007. 1993). Molecular analyses indicate that it is the closest relative to apicomplexan parasites. 2008. sampling. 1982).

Since their initial application. Cladistic studies. 2009. 2003). have yielded some controversial hypotheses as to the or- igins and development of ontogenetic sequences (O’Grady. whereby distantly related lineages are incorrectly inferred to be closely related because both lineages have under- gone a considerable amount of change. Littlewood relationships still need to be better understood. The use of fossils in molecular clocks has changed in the last decades (Parham et al.. The evolution of complex life cycles is a major research question. with vertebrate defin- itive hosts argued to be the plesiomorphic condition for stem group neoder- matans (Littlewood et al... 2014. molecular clocks still need age constraints from the fossil record or other lines of evidence to provide calibration points for at least one or more nodes in a calibrated phylogeny (Ho and Phillips. with ever more sophisticated models accommodating large genomic datasets. 2015). the determination of free-living sister groups and the inference of ancestral life history strategies are key to determine the origins of parasitism and the evolution of complex life cycles. 2014). who demonstrated that only the fast- evolving quartile of their transcriptomic dataset supported the Platyzoa. molecular clock methodologies have undergone major developments (Bromham and Penny. parasitic flatworms (Lockyer et al. Ho. 2003. This theory has since been confirmed by Egger et al. A recent molecular study (Struck et al. In para- sitic flatworms (Neodermata). Warnock. complex parasite life cycles appear to have initially evolved by the addition of intermediate hosts. 2014) and nematodes (Dorris et al. (2015). 2014. fossil vertebrates may yet hold the key to verifying or at least supporting this claim. Sister-group relationships within and between parasite lineages. Timothy J.. however. rate variation and the uncertainties of multiple types of calibration points (Parham et al. which groups Acantho- cephala and Platyhelminthes among various free-living taxa.. W€ orheide et al.. 2002. Nevertheless.. W€ orheide et al. with two main mecha- nisms proposed (Parker et al. Blaxter. 1999. Blaxter and Koutsovoulos. 2003. 1999). Hipsley and M€ uller. or downward incorporation by addition of intermediate hosts. 2012. is probably an artefact of long-branch attraction. 2014). 1985).28 Kenneth De Baets and D. myzostomid annelids (Summers and Rouse. or the application of parsimony principles to infer ancestral life cycles. 2014). 2015): upward incorporation by terminal addition of hosts.. Wey-Fabrizius et al. 2012. the scenarios are inferred from molecular phylogenies of extant taxa. Ho. 2015). This has been shown for acanthocephalans (Near. 2014) also indicates that the Platyzoa.. in the absence of phylogenetic artifacts. 2015) . molecular studies can be used to investigate the origins and radiations of parasitic lineages.. Importantly.

Arcila et al. 2015). 1974) and bivalves (De Baets et al. 2013.. Finally. there are also those that have characterized complete biomes (Rawlence et al. 2015a).g. Wood et al. parasitic relationships might have already existed in the Precambrian.. 2015). Kodan- daramaiah. Based on extrapolation of extant host-associations. Ronquist et al. Hipsley and M€ uller.The Importance of Fossils in the Evolution of Parasites 29 including their implementation as probabilistic time priors (Ho and Phillips.. 2015a). 2015. 2011. aDNA techniques have made it possible to obtain pathogen DNA from dated ancient parasites or host remains (Dittmar. detection and characterization of bacteria entombed in dental calculus (Warinner et al. Cano et al.. for example. Warnock et al. Although many of these studies have been targeted in their approach..... How- ever. 2000) as well as in Silurian echinoderms (Franzen. advances in molecular techniques have provided additional advances in unravelling past events. Additional indications for parasitism are also found in other Lower Palaeozoic groups like Ordovician graptoloids (hemichordates) (Bates and Loydell. 2014) has opened up new avenues in palaeomicrobiology... methods using other types of age evidence like geological calibrations (e. 2011). 2012.. 2011a. 2015) and tip calibrations integrated among their living relatives by combing molecular and morphological evidence (Pyron. 2009. and the discovery of subfossil coprolites (Santiago-Rodriguez et al. 2006.1 Molecular clocks The ancient origin of parasitism is suggested by the deep-branching position of various parasitic lineages within the tree of life as well as the extrapolation of extant parasite host associations. 4. 2013a. Since the assignment of Cambrian . Bos et al. 2011. vicariance events) or host calibrations lag behind in their development and leave them heavily scrutinized (Goswami and Upchurch. for which the fossil constraints are better than they are for unicellular organisms. This is corrob- orated by the earliest sign of parasitism by an unknown metazoan parasite in Cambrian brachiopods (Bassett et al. In prokaryote and unicellular eukaryote.. Hofreiter et al. although the exact identity of the culprits is unknown. although so far no direct fossil evidence has been found.. 2014). 2009. For metazoan par- asites. the origin of parasitic flatworms and some lineages of parasitic nematodes have also been estimated to lie in the CambrianeOrdovician (Littlewood. Wood et al. Poinar. 2010. 2015). 2014). parasitism must have evolved at least for some groups during or slightly before the Cambrian explosion in the marine realm. 2013b. 2004) and body fossil remains of various pentastomid taxa from the CambrianeOrdovician (Castellani et al..

Littlewood Cambroclavida (a group of enigmatic.. been suggested that symbiotic/parasitic relationships in dinoflagellates and Api- complexa might have extended back in evolutionary time to the earliest or- igins of Metazoa. Brasier and Ant- cliffe. although their systematic affinity is still unclear (Littlewood and Donovan. 2013). Conway Morris. Parasitism-like life history patterns probably first evolved in the sea. 1981). However.30 Kenneth De Baets and D. It has. calibrating molecu- lar clocks to test such hypotheses remains a challenge (Bensch et al. 2001). which means that either as parasites or symbionts.. 2008). Noronha et al. these protists have been interacting with the metazoan immune system since their inception (Okamoto and McFadden. Ediacaran fossils like Dickinsonia have occasionally been compared with Spinther (Wade. In other cases it is less clear as the earliest . So far no direct unequivocal evidence for metazoan parasites has been discovered in the Precambrian. Timothy J. 2008). In some cases this might have been true. many could have already evolved towards parasitism in the Precambrian.. The earliest metazoan helminth remains are circlets of hooks from Middle Devonian fishes (Upeniece.. the earliest confidently assigned ancient acanthoceph- alan remains are eggs derived from Quaternary archaeological sites (Fry and Hall. 1984) is unsubstantiated (Kou- chinsky et al. although the exact systematic position of Dickinsonia remains highly controversial (Retallack. as indicated by nematode remains in early diverging land plants from the Early Devonian (Poinar et al. viruses and various other unicellular to multi- cellular eukaryotes have evolved before this time. 2012).. 2013). De Baets et al. 1994). Considering that bacteria. 2003.. 2010). This comparison proved to be superficial at best and they are now often interpreted to be more basal metazoans (Xingliang and Reitner. Sperling and Vinther. phosphatized. 2006.. Rota-Stabelli et al. 2008). 1969. no evidence for a parasitic relationship of Dickinsonia with other taxa could be evidenced. 1972. A parasitic mode of life of Dickinsonia would be rather absurd too as it would mean the presence of hosts which would have to be considerably larger than Dickinsonia. The discovery that the closest relative of parasitic apicomplexans is a coral symbiont might suggest that modern parasites may have started out as mutualistic metazoan symbi- onts before turning to parasitism (Moore et al. 2005b). 2008). although both plants and nematodes might have colonized the land considerably earlier based on molecular clock estimates (Clarke et al. 2011. More importantly. 2007. therefore. an annelid parasite of sponges (Rouse. which have remained unnoticed in the fossil record. but it is unclear if parasites closely tracked the terrestrialization of their hosts. 2015a).. hollow spine-shaped sclerites) to Acanthocephala (Qian and Yin.

particularly the root. 2012. These have been shown.. 2007) or probability functions that express some predefined perception of the degree to which fossil minima approximate the true time of divergence (Ho and Phillips. 2005. 2013a) allow fossils to be integrated into divergence time studies among their living relatives. Further- more. which have evolved convergently from terrestrial ancestors (Sudhaus.. 2011. when crit- ically evaluated. as the latter can lead to selection of congruent. Benton and Donoghue. 2009).. Nevertheless. 2014).. to yield . Although para- sitism evolved in the sea.. bacteria. Wood et al. using combined morphological and molecular datasets and evolutionary models. Mitchell. rather than using posteriori selections methods. 2015.. erroneous calibrations (Warnock et al. The latest tip-calibration or total ev- idence dating methods (Pyron. but most studies apply phylogenetic bracketing (M€ uller and Reisz. Mello et al. however. although deeper nodes. 2015) which can put important constraints on shallower nodes in phylogenies. Heath et al. which evaluate congruence through cross-validation. 2006. the summary above shows that the body fossil record offers confident minimum constraints for various lineages of parasites. The direct record is largely restricted to more recent Quaternary sites. 2014).. Nowak et al. as is the case for various groups of nematodes parasitizing shallow marine to intertidal taxa. in phylogenies are more crucial for dating (Warnock et al. 2013. 2013. using this premise to constrain molecular clocks might be dangerous in particular cases. 2013) or soft-bodied helminths (De Baets et al. 2014). but molecular clocks might be an alternative to dating important events without relying on recent evidence of parasiteehost associations or the evolutionary history of their hosts. The fossil record can only provide minimum constraints on the origin of parasitism... How- ever. 2011. However. 2010). various groups of terrestrial vertebrates (archosaurs.. 2015a) is not straightforward. 2015). particularly archaeological sites (Ara ujo et al.. synapsids) were already parasitized in now extinct lineages leading up to currently infested host taxa (Poinar and Boucot. Frías et al.. these calibration points should be screened and selected a priori. most authors agree that multiple calibration points implemented faith- fully across a phylogeny are ideal in achieving accurate and precise divergence estimates.The Importance of Fossils in the Evolution of Parasites 31 fossil evidence for terrestrial parasitism in these lineages considerably predates the presumed origin of their host taxa (e. vertebrates or arthropods).. Da Silva et al. Ronquist et al.g. 2012. The calibration of molecular clocks in pathogens with a poor fossil record like viruses. Various methods have been developed to estimate diver- gence times based on the stratigraphic distribution of fossil data (Wilkinson et al. protozoa (Bensch et al.

Their fossil re- cord remains are rare in time and space due to their restriction to sites of exceptional preservation.. Molecular clocks constrained by other types of evidence (e.. 2015a). host or biogeographic calibrations have not received the same scrutiny and refinement as fossil calibrations (Kodandaramaiah.32 Kenneth De Baets and D. De Baets et al. 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. the body fossil record of parasitic forms is even richer (at least less poor) than that in their free-living relatives. 2005. 2011). 1981. Furthermore. 2012.. but can potentially still be valuable to place con- straints on the evolution of these groups as a whole. In these cases. skeletal responses to parasitism are still comparatively poorly studied. Computed tomography will be important to reveal additional details of the morphology and structure of putative body fossils. 2003. Argulidae). 2013. De Baets and Donoghue.. 2015a) and Nematoda (Poinar. 2011. or supplementary ways. 2001. It therefore probably makes more sense to avoid using them to constrain molecular clocks directly. Keupp. Héritier et al. Such solutions potentially lie in the host fossil record or biogeo- graphic events. partic- ularly in extant taxa (Zibrowius. 2015a. Unfortunately. Parham et al. body fossils or geological events) could how- ever be used to test the appearances of these skeletal responses. Interestingly. Problematically. 2011a. 2012. 2015) and their per- formance needs to be more extensively tested. Myxozoa. which will make it possible to assign them more accurately to extant lineages. De Baets et al. which can be used to put constraints on early nodes in molecular clocks. Unfortunately. Littlewood unexpectedly old age estimates of clades (Arcila et al. 2014). Klompmaker et al.. Ituarte et al. 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. such as amongst Platyhelminthes (Poinar. In some soft-bodied helminths.. . 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. 2015). In the absence of reliable body fossils.. this is not always the case. the fossil record does not yield body fossils or other re- mains for multiple lineages of unicellular pathogens or soft-bodied metazoan parasites (e. it is therefore necessary to look for and select suitable alternatives.g.. but not necessarily closely related. which have left a footprint of divergence among evolutionary lineages.g.. the nearest free-living relatives have a good fossil record. to constrain the molecular clock (Bensch et al. In some cases. Timothy J.

. 2010. All factors considered. As they are currently implemented. pathological). Parasitologists often extrapolate extant parasiteehost or biogeographic relationships to estimate the evolutionary origin of parasites (Mejía-Madrid. which takes into account these factors (Warnock. Not only does the fossil record provide direct and indirect evidence for the presence of certain parasite lineages. tectonic episodes are protracted and might have different impacts on lineages depending on their ecology. for example. Biogeographic distributions of their hosts and potentially that of their parasites might also have differed considerably in the past. Hipsley and M€ uller. Some exceptions have been suggested in parasites but these still need to be tested. 2014). Likewise. ancestral state reconstruction of host associations and life cycles (host use and complexity) from phylogenies. 2014). 2001. Hipsley and M€ uller. Although some of these hypotheses do stand the test of additional sampling of extant or fossil forms. 2007). the cestode Nesolecithus and the nematode Nilonema have an apparent Gondwanaland origin with their present day distribution in Africa and South America (Gibson et al. These limitations can be partially overcome or at least controlled like fossil calibrations. which is not always. which can introduce a factor of circularity when testing hypotheses of evolutionary changes in parasiteehost associations or biogeographic distribution (Trewick and Gibb. Biogeographic dating often relies on geochronologically or otherwise geologically dated events. we should prefer to have an . 2011. Castellani et al. Furthermore. Kodandaramaiah. 2011. Crisp et al. 2014).. Caution should be always taken as the fossil record also yields evidence of parasitic lineages and parasiteehost associations which are now clearly extinct (Upeniece. 2014). biogeographic calibrations and their age evidence are rarely if ever justified. by implementing them in the most conservative way as proba- bilistic constraints that span an interval of time.. assumptions should be at least consistent with the fossil evidence and robust molecular clock estimates of their hosts. 2006. Chen et al. but it can also provide evidence for infection intensity. Therefore. host response (developmental. Santos and Gibson.. 1987. novel (potentially extinct) host associations and parasite life cycles. 2013 for a review) or more rarely to cali- brate molecular clocks. the case as they might have been modified or even reset by subsequent events. or even rarely. combined with calibra- tions can inform the interpretation of body fossils and inferred chronologies (Zhu et al. they often assume the biogeography of living or- ganisms is a faithful reflection of ancestral distribution.The Importance of Fossils in the Evolution of Parasites 33 2012.. 2011. Poinar and Boucot. Upeniece. others do not if quite different host associations or biogeographic distribu- tions are recovered. 2011. 2015).

Hibbett and Matheny. 2010. 2009. viruses or symbionts. Lee et al. and their long unchanged history is inferred such that they cannot be referred to as genomic ‘fossils’ as such.. too (Cerveau et al. Things may be even more complicated as evi- dence of HGT may have occurred between various types of endosymbiotic bacteria (Duron. 2015). 2013). than a precise timescale that lacks the necessary accuracy (De Baets et al. Some of these transfers retain an apparent parasitic role (Kidwell and Lisch. 2001) or become integrated into biochemical pathways that are functionally important in lineages that become parasitic (Alsmark et al. Gifford. 2011. 2013). Interrogation of genomes has made it possible to identify horizontal transfers of genetic elements (HGTs) in the deep history of living organisms. Comparison of such genomic signatures between species provides a means of determining their origins. Katzourakis. for example. Thézé et al.34 Kenneth De Baets and D... There is no physical ‘fossil record’ of these viruses or signa- tures (Katzourakis and Gifford. Koutsovoulos et al.2 HGT and ‘parasitic DNA’ Even for groups where no fossil biomolecules have been found. There is increasing evidence that HGTs have left genomic signatures of other more highly organized symbi- onts like bacteria in their metazoan host genomes. 2012. 2013) or viruses within their hosts (Niewiadomska and Gifford.. further evidence of historical hoste parasite interactions will undoubtedly arise from future genomic studies of both hosts and parasites. parasites can leave footprints in their hosts’ genomes (Gilbert and Feschotte. 2014). diversification and change through time. 2013). Littlewood accurate timescale that might lack precision.. 2010.. methods have been developed. although an understanding of the role of HGT in eukaryotes is still in its infancy (Hirt et al. typically revealing ‘hosteparasite’ interactions over prehistoric or geological timescales. 2011.. Katzourakis. 2013. 4.. 2015). Silva et al. Koutsovoulos et al. but are expected to become more commonly detected in multicellular .. which can compare the relative molecular rates of groups to test the hypotheses of co-divergences (Loader et al. 2014). Timothy J. 2011. 2007.. HGT events are common in prokaryotes and many microbial eukary- otes... However. 2013). 2010. Thézé et al. 2014). HGTs are the transfer of DNA between two nonvertically related individuals belonging to the same or different species (Sj€ ostrand et al. Loss-Oli- veira et al. Even if no suitable cali- bration points can be found. 2012. 2013. 2015a). Studies have focused particularly on ancient viruses (Gilbert and Feschotte. Herniou et al...

Dittmar. 2014.b. (2013) showed the pattern of HGTs retained after parasite diversification are likely to be functionally important for the parasites (e. Davis and Xi (2015). By explicitly modelling the evolution of genes present in genomes. Richards et al.. 2013b. HGTs are important in revealing which evolutionary lineages were concurrent and when speciation (or broader divergence) events took place. Further interrogation will reveal lineages of parasites with genomic signatures of their long-associated histories with their host groups. this evidence will provide indications as to when particular lineages came into contact with one another. revealing the need to be wary of technical artifacts and gene conservation is- sues before claims of HGT can be verified (Wijayawardena et al. With microbial phylogenies. Wood et al. There is increasing evidence that the role of HGTs in eukaryote evolution is important. 2014. FUTURE PERSPECTIVES Various new advances in ancient biomolecule detection and charac- terization (Briggs and Summons. 2015). 2014) including aDNA (Dittmar.. 2014.. Sz€ ollTsi et al. 2014a.. . 2012). 2014) offer many new prospects and perspectives in palaeoparasitology. novel development in molecular clock methodologies (Parham et al. 2009.g. and it does not seem overly speculative to predict that signatures from hosteparasite interactions will be found in more genomes. Wijayawardena et al. particularly in the evolution of resistance. validated against the groups’ good microfossil record. but the success of these leads in revealing accurate records of historical interactions depends on greater study. W€ orheide et al. (2011). palaeoproteomics (Hofreiter et al.The Importance of Fossils in the Evolution of Parasites 35 eukaryotes as more is known about their genomes (Andersson. (2012) provided a chronologically ordered phylogeny for cyanobacteria. 2014. Hofreiter et al. 2010). (2013). for example.. Alsmark et al.. thus showing that their methods can reveal and use HGTs as a source of information on timing (or at least chronology) of evolutionary events. 2015) and new possibilities for the critical evaluation and nondestructive analysis of 3D fossil structures by computed tomography (Cunningham et al. there is strong evidence that multiple HGT events have promoted the plant parasitism ability in some nematodes (Danchin et al. in kinetoplastids and apicomplexans). schistosomes) have been discredited...g. 2012. 5. Sutton et al. Similarly. and vice versa. 2005). Ho. In turn. Focusing on microbial eukaryotes. Shapiro and Hofreiter.. 2015). Some recent claims of HGT in multicellular parasites (e.

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while the earliest fossil vertebrate-parasitic nematodes are from Upper Triassic coprolites.2 Mexican amber nematodes 75 7. 53 .2 Rock fossils 54 2.3 Coprolites 55 3. Stages in the Evolution of Nematode Parasites of Invertebrates 79 10.2015. stone and coprolites dating from the Palaeozoic to the Holocene. OR 97331. The earliest parasitic nematode is a primitive plant parasite from the Devonian. Poinar. j ISSN 0065-308X http://dx. Fossil invertebrate-parasitic nematodes first appeared in the Early Cretaceous. Volume 90 © 2015 Elsevier Ltd.03. 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.1 Baltic amber 60 6. Nematode Parasites from the Pleistocene and Holocene 77 8. Media for the Study of Fossil Nematodes 54 2.1 Nematode parasites of humans from the Pleistocene and Holocene 78 9. Department of Integrative Biology. Nematode Parasites from the Early Cenozoic 60 5.1 Dominican amber nematodes 65 6. CHAPTER TWO The Geological Record of Parasitic Nematode Evolution George O. Oregon State University.002 All rights reserved. Corvallis. Jr. Nematode Parasites from the OligoceneeMiocene 65 6. Advances in Parasitology. Introduction 54 2. Nematode Parasites from the Pliocene 77 8.1016/bs.doi.1 Amber 54 2. Palaeozoic Parasitic Nematodes 55 4. along with views on the origin and evolution of nematodes and their hosts.edu Contents 1. Origin of Nematode Parasites of Vertebrates 81 11.org/10.apar. USA E-mail: poinarg@science. Specific examples of fossil nematode parasites over time are presented. Parasitic Nematode Body Fossils from the Mesozoic 55 5. vertebrates and plants based on fossil remains in amber.oregonstate.

the great majority of which are forest living arthropods (cf. even if they have not completely finished their development. 2. Iturralde-Vincent and MacPhee. 40e50 mya (Larsson.54 George O. Jr. Amber-containing parasitic nematodes extend from the early Cretaceous (130e135 mya) to the Miocene (15e20 mya). Baltic amber. 2001). While some nematodes have been preserved in fine-grained cherts dating back to the Devonian. 2003) and Leb- anese amber. which makes them extremely difficult to locate. (2006) and Poinar (2011). 2003). Using this method. decompo- sition after death is quite rapid. Burmese amber. fossilized resin (amber) and coprolites have been the most use- ful media for studying the evolution and early hosts of parasitic nematodes. from microbes to vertebrates (Poinar. The urge of parasitic nematodes to escape from hosts that become entrapped in tree resin. 1992). and sclerotized structures that could be fossil- ized are microscopic.1 Amber Amber is fossilized tree resin that preserves a wide range of organisms. 1992). Iturralde-Vinent. 1990. Geological ages mentioned here are based on Gradstein et al. 97e110 mya (Cruickshank and Ko. 1996. 2001). 1. Mexican amber at 22e26 mya (Poinar. While parasitic forms can reach up to several metres in length (Yeates and Boag. 130e135 mya (Poinar and Milki. (2012). Poinar. . Dating of amber deposits is usually based on fossils in the surrounding bedrock. Preservation appears to be the result of inert dehydration and fixation by natural plant products in the orig- inal resin. Poinar. INTRODUCTION The body fossil record of parasitic nematodes is limited by their small size and soft bodies (Littlewood and Donovan. 1978). 2006). MEDIA FOR THE STUDY OF FOSSIL NEMATODES 2. 2011).2 Rock fossils Nematode remains in sedimentary deposits mostly occur as compression fos- sils with only the body outline and external ornamentation evident. 2. Taxonomic groupings of nematode categories follow treatments of De Ley and Blaxter (2004). provides most of our fossil records of parasitic nematodes. Eyualim-Abebe et al. Dominican amber has been dated at 20e45 mya (Cepek in Schlee. The occurrence of parasitic nematodes in fossilized resin is frequently associated with the habits of their hosts.

. 2014) can reveal the presence of vertebrate- parasitic nematodes. The next oldest member of this group is the 130 mya mermithid. sclerotized parts such as onchia and spicules. 2006. it can be difficult to distinguish between actual nematode parasites and microbotrophic nematodes that entered the dung after it was deposited (Poinar. 1983). Paleoxyuris cockburni Hugot et al. PALAEOZOIC PARASITIC NEMATODES The only Palaeozoic body fossil of a parasitic nematode is the Early Devonian Rhynie Chert plant-parasitic nematode. 2014. This type of permineralization has provided us with the earliest record of parasitic nem- atodes from the Early Devonian Rhynie Chert (Poinar et al.g. in some fine-grained sedimentary deposits known as Lagerst€atten. and occasionally even portions of the alimentary and reproductive systems (Poinar. In some rare instances where silica and other dissolved minerals impreg- nate rocks.. Eggs. Ancient dung samples also are one of the best resources for establishing early records of human nematode parasites (Gonçalves et al. Their presence provides the earliest evidence of a symbiotic association between terrestrial plants and animals and repre- sents an early stage in the evolution of plant parasitism by nematodes and their presence on land. (1994) from Early Cretaceous Lebanese amber. 2011) can be found. (2014). 2008). Hugot et al. nematodes inside can be preserved in amazing detail.3 Coprolites Analysis of lithified coprolites dating back millions of years (e. PARASITIC NEMATODE BODY FOSSILS FROM THE MESOZOIC The oldest animal-parasitic nematodes have recently been found in Triassic cynodont coprolites in Brazil... . 2003). Palaeonema phyticum Poinar et al. 2014) and desiccated dung of more recent ages (Poinar. These include a 240 mya ascarid. 3. The single specimen was coiled up in the body cavity of an adult midge (Chironomidae: Diptera) (Figure 2). Cretacimermis libani Poinar et al. Ascarites rufferi Da Silva et al. Da Silva et al. Poinar and Boucot. However. Aglao- phyton major Kidson & Lang. 4.The Geological Record of Parasitic Nematode Evolution 55 However. juveniles and adults were present in the stomatal chambers of the Early Devonian (396 mya) land plant. 2. (2008) (Figure 1). (2014) and a 240 mya old oxyurid.

Aberdeen.56 George O. 2008 surrounded by cortical cells of Aglao- phyton major in Devonian Rhynie Chert. Figure 1 Palaeonema phyticum Poinar et al.. Jr. . Figure 2 The mermithid. 2006 emerging from a biting midge in Early Cretaceous Burmese amber (Ron Buckley amber collection) (Scale bar ¼ 1 mm). Cretacimermis protus Poinar and Buckley. Poinar. Scotland (Scale bar ¼ 59 mm).

pro- vides the earliest record of mycetophagous nematodes. Adult males and females. as well as resistant juvenile stages were present. beginning with invertebrates and then expanding their host range to vertebrates. The adults of C. Figure 3 The thelastomatid. Features of the fossil nematodes resemble those of the extant snail parasite. together with mycelium. 1987). 1930. A sibling species of C. as occurs in extant members of the family (Hunt. . Mid-Cretaceous Burmese amber contains both plant and animal nema- tode parasites. Cretaciaphelenchoides burmensis Poinar (2011). While the origin of oxyurids could extend back to the Silurian based on the earliest fossils of their millipede hosts (Wilson and Anderson. Vanderburgh and Anderson. 2004). but it is likely that molluscs were the original host of Cosmocercoides spp. dukae live in the intestinal tract of the snail. 2003). Oxyurids may be the first nematodes to form parasitic associations with terrestrial animals. Paleothelostoma tipulae Poinar (2011) (arrow) adjacent to its tipulid host in Early Cretaceous Burmese amber (Scale bar ¼ 251 mm). A small population of the fungal-feeding aphelenchoidid. 1960). The nematodes could have been carried to the site by wood-boring insects. 1993). when they first invaded insects is unknown.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. Extant craneflies are common hosts of thelastomatids (Poinar. A snail in Burmese amber with juveniles of Palaeocosmocerca burmanicum Poinar (2011) adjacent to its mantle cavity provide early evidence of the family Cosmocercidae. The thelasto- matid. dukae occurs in the rectum of frogs and toads (Harwood. Such hoste parasite associations still occur today (Poinar and Poinar. 1975). Paleothelastoma tipulae Poinar (2011) adjacent to a cranefly in Burmese amber (Figure 3) establishes the earliest fossil record of this group in inverte- brates. Cosmocercoides dukae (Anderson. and second stage juveniles and third stage infectives occur in the mantle cavity.

Cretacimermis protus Poinar and Buckley (2006) parasitized biting midges (Ceratopogonidae) of the genera Atriculoides Remm and Leptoconops Skuse (Poinar and Monteys. 2008) (Figure 5). The Burmese amber mermithid. Mermithid nematodes emerging from insects also occur in Burmese amber. Entomopathogenic nematodes. . Two specimens of Cretacimermis chironomae Poinar (2011) were asso- ciated with an adult chironomid midge. An analysis of an dinosaur coprolite from the Early Cretaceous Iguan- odon shaft in Belgium revealed ascarid eggs. Jr. Figure 4 Proheterorhabditis burmanicus Poinar (2011) (arrow) adjacent to its beetle host in Early Cretaceous Burmese amber (Scale bar ¼ 152 mm). date back to the Early Cretaceous with Proheterorhabditis burmanica Poinar (2011) and its rove beetle (Staphylinidae) host in Burmese amber (Figure 4). birds and reptiles.58 George O. show that mermithid parasitism of the Chironomidae occurred in Laurasia and Gondwanaland in the Early Cretaceous. for example those whose infective stages carry symbiotic bacteria in their gut and release them in a potential host. 2005). The egg of Ascarites priscus Poinar and Boucot (2006) (Figure 6) still had its outer mammillated surface and contained a developing juvenile nematode. Poinar. Extant species of Leptoconops feed on the blood of mammals. Rod- shaped bacteria similar to those associated with extant species of Heterorhab- ditis occurred in the fossil rove beetle. as well as Creta- cimermis lebani from Lebanese amber. it is likely that the females also fed on vertebrate blood (Szadziewski and Poinar. While the genus Articulicoides is now extinct. These specimens.

. Cretacimermis protus Poinar and Buckley. Megalosaurus from the Bernissant Wealden Iguan- odon locality in Belgium (Scale bar ¼ 11 mm). 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.The Geological Record of Parasitic Nematode Evolution 59 Figure 5 The mermithid.

but Heydenius antiqua (von Heyden) was found protruding from the body of a long-horned beetle (Coleoptera: Cerambycidae) in German brown coal strata (von Heyden. . Sliter (1971) found nematodes living within borings in the tests of the foraminifera Rosalina globularis d’Orbigny and Bolivlina doniezi Cushman and Widkenden off Southern California and felt that the borings were made by the nematodes rather than by some other invertebrate.1 Baltic amber A wide range of parasitic nematodes occur in Baltic amber. Additional studies are needed to verify the abil- ity of specialized groups of nematodes to bore through the shells of foraminifera before fossil tests with bore holes can be used to establish the presence of marine nematodes. Myce- tophagous parasites include a reproducing population of the aphelenchoidid. 1866) is now considered a collective species for all mermithids parasitizing chironomid midges in Baltic amber (Figure 7). Jr. Palaeoaphelenchoides balticus Poinar (2011) that were probably feeding on fungi on the resin-producing tree. Poinar. as shown by Heydenius formicinus Poinar (2002) emerging from a winged male of Prenolepis henschei Mayr in Baltic amber (Figure 8). especially as parasites of the family Chironomidae. Nematodes that occur in extant foraminifera tests provide a challenge to both biologists and paleontologists.60 George O. It is unusual to find nematodes in coal deposits. NEMATODE PARASITES FROM THE EARLY CENOZOIC 5. Sliter (1971) used identical borings in bathyal and neritic Cretaceous foraminifera to determine the distribution and abun- dance of marine nematodes. Extant ants are known to host a number of mermithids and this parasitic association dates back at least to the Eocene. There are many extant nematodes that live in the tunnels of bark beetles and develop on fungi in the insect galleries. 1943). 5. A number of mermithids occur in Baltic amber. the absence of diagnostic characters prohibits further identification. showing that mermithid lineages were parasitizing Coleoptera by the Eocene. Later. The first one described in 1866. other nematodes recovered from forami- nifera tests were identified as Syringonomous typicus Hope and Murphy (1969). Heydenius matu- tinus (Menge. 1860). Smithsoninema inaequale Hope and Tchesunov (1999) and an unde- scribed species (Myers. While there may be several genera and species involved.

in Baltic amber the first fossil record of a mermithid parasite of a hemipteran. with the only records coming from Ireland (Helden. . 1866): one completely emerged and the second still in the body cavity of their chironomid midge host in Baltic amber (Scale bar ¼ 53 mm). 2002 emerging from a male winged ant (Prenolepis henschei Mayr) in Baltic amber (Scale bar ¼ 640 mm). Heydenius brownii Poinar (2001). Hemipteran hosts of mermithids are rare today. 2008). Heydenius formicinus Poinar.The Geological Record of Parasitic Nematode Evolution 61 Figure 7 Two specimens of Heydenius matutinus (Menge. With a fossil record extending back to the Early Permian Figure 8 The mermithid. was found protruding from the body of a planthopper (Fulgoroidea) (Figure 9). Also.

A third parasite line- age was represented by Tripius balticus Poinar (2011) of the family Sphaeru- lariidae. Figure 9 The mermithid. Heydenius sciarophilus Poinar (2011) (Figure 10) and another a tetradonematid. Several different lineages of parasitic nematodes have been found to attack sciarid fungus gnats (Diptera: Sciaridae) in Baltic amber. emerging from an achiliid planthopper in Baltic amber (Scale bar ¼ 2. Poinar. Other dipterous hosts of mermithids in Baltic amber were gall gnats (Cecidomyiidae). Palaeotetradonema sciarae Poinar (2011).6 mm). . One was a mermithid. 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 life cycle of the fossil was prob- ably similar to that of the extant species. Several nematodes were still inside the body cavity of the adult host while others had emerged (Figure 11). Tripius sciarae (Bovien). (Rasnitsyn and Quicke. 2001. hemipterans could have been ancient terres- trial hosts for mermithids. Jr. Poinar.62 George O. Heydenius brownii. 2002).

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). . Howardula helenoschini Poinar (2003) that parasitized scuttle flies (Phoridae). Figure 12 Two specimens of Heydenius cecidiomyae Poinar (2011). a parasite of a gall gnat in Baltic amber (Scale bar ¼ 575 mm). emerged (Figure 12). Another parasite lineage of Diptera was represented by the allantonematid. There are no reports of extant gall gnats parasitized by mermithids.

Extant phorid flies are parasitized by Howardula nematodes globally (Richardson et al.. A micro- filaria of Cascofilaria baltica Poinar (2011. Poinar. Blackflies (Simuliidae) and biting midges (Cera- topogonidae) are the most common biting insects in Baltic amber. 1975. obviously having just exited from the host’s body cavity (Figure 13). Jr. in Baltic amber (Scale bar ¼ 347 mm). suggesting that the fly had taken a blood meal shortly before falling in the resin. 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. The nematodes normally leave the fly host via the intestine or reproductive system (Richardson et al. Disney.. Triphleba sp.. Hematophagous flies in Baltic amber also were associated with vertebrate nematode parasitic lineages.. 1994). Howardula helenoschini Poinar (2003) (arrow) emerging from a phorid fly. Figure 13 Specimens of the allantonematid. This represents the oldest fossil record of a filarial nematode. helenoschini could be detected through the host’s abdomen. 2012) was adjacent to a blackfly with a swollen abdomen. The lemon-shaped parasitic female of H. Poinar.64 George O. 1977. a worldwide genus infecting mammals and vectored by blackflies. helenoschini were clustered at the posterior tip of the fly’s abdomen. Five specimens of H. The microfilaria falls within the size range of those of extant Onchocerca spp. Still additional insect hosts of mermithid nematodes in Baltic amber include a moth (Lepidoptera) parasitized by Heydenius podenasae Poinar . 1977) and that is probably the route used by the five fossil nematodes.

NEMATODE PARASITES FROM THE OLIGOCENEeMIOCENE 6. an adult caddis fly. (Phasmatodea: Phasmatidae) parasitized by Heydenius phasmatophilus Poinar (2012) (Figure 15).4 mm). A second lineage was a member of the family Tetradonematidae.1 Dominican amber nematodes One of the major host groups of nematode parasites in amber from the Dominican Republic is ants and there is evidence that three lineages of para- sitic nematodes were involved. A mermithid lineage is represented by Heydenius myrmecophilia Poinar et al. (2012). 6. (2006) that had recently emerged from a species of the ant genus Line- pithema Mayr. Triaenodes balticus Wichard and Barnard. 2005) parasitized by Heydenius trichorosus Poinar (2012) in Baltic amber (Scale bar ¼ 1. Myr- meconema antiqua Poinar (2011). This species was represented by a mass of . 2005 (Trichoptera) parasitized by Heydenius trichorosus Poinar (2012) (Figure 14) and a phasmatid.The Geological Record of Parasitic Nematode Evolution 65 Figure 14 Adult caddis fly (Triaenodes balticus Wichard and Barnard. and Heydenius araneus Poinar (2000) from a crab spider (Tho- misidae) (Figure 16) is the earliest record of nematode parasitism of spiders. Balticophasma sp. Spiders were also parasitized by mermithid nematodes in the Baltic amber forest.

(Phasmatodea: Phasmatidae) parasitized by Heydenius phasmatophilus Poinar (2012) in Baltic amber (Scale bar ¼ 2. Figure 15 A phasmatid. The life cycle of this group is especially fascinating and unique.1 mm).66 George O. .). 1803. When females of M. Jr. eggs (Figure 17) that had escaped through a hole in the gaster (abdomen) of a species of Cephalotes Latreille. neotropicum have matured and the body cavity of the ant is filled with eggs. a parasite of Cephalotes atratus (L. The fossil probably had a life cycle similar to the extant Myrmeconema neotropicum Poinar and Yanoviak (2008). the color of Figure 16 The spider mermithid. Poinar. Balticophasma sp. Heydenius araneus Poinar (2000) adjacent to its clu- bionid spider host in Baltic amber (Scale bar ¼ 2 mm).

dominicanus was probably similar to that . the Allantonema- tidae. Cephalotes ants are also hosts to a third parasite lineage. A separate lineage of allantonematids. The infected ants stand on stems and raise their abdomens high in the air. The ingested nematode eggs hatch in the larval guts and the juveniles penetrate into the insect’s body cavity. the eggs of M. Worker ants collect and feed the infested bird droppings to their brood. It appears that this complicated life cycle was established already some 20e30 million years ago. the host’s gaster changes from black to a shiny red.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). A female fly was heavily infected and large numbers of juve- niles and second-generation female nematodes were adjacent to the host (Figure 19). Mature juveniles of Palaeoallantonema cephalotae Poinar (2011) were emerging from a worker of Cephalotes serratus in a piece of amber (Figure 18). The bright red abdomen resembles ripe berries that are relished by birds. neotropicum pass thought the bird’s digestive tract and are deposited in the droppings. A similar hosteparasite association occurs with an undescribed allantonema- tid and workers of Cephalotes christopherseni in Peru. The life cycle of P. When a bird ingests an infected ant. represented by Palaeoparasitylenchus dominicana Poinar (2011) parasitized drosophilid fruit flies in the Dominican amber forest.

in Dominican amber (Scale bar ¼ 24 mm).68 George O. Another mermithid lineage attacked scavenger flies Figure 19 Parasitic juveniles of Palaeoparasitylenchus dominicanus Poinar (2011) emerging from a drosophilid fly in Dominican amber (Scale bar ¼ 432 mm). of the extant species. . Two juvenile specimens of Heydenius psychodae Poinar (2011) had completely emerged from an adult moth fly (Figure 20). Cephalotes serratus Vierbergen & Scheve. Poinar. Parasitylenchus nearcticus Poinar et al. (1997) from Eastern North America. Jr. Moth flies (Diptera: Psychodidae) were also attacked by mermithid nematodes in the Dominican amber forest. Figure 18 Detail of a specimen of Palaeoallantonema cephalotae Poinar (2011) from the ant. There appears to be no record of mermithids parasit- izing extant moth flies.

The life cycle of P. The fossil shows that life cycles . (Diptera: Scatopsidae). The latter has a mycetophagous cycle that occurs in mushrooms also invaded by fungus gnats. Another fly group in the Dominican amber that was parasitized by mer- mithid nematodes was milichids (Diptera: Milichidae). Heydenius psychodae Poinar (2011). There are no extant records of mermithids from this family of flies. dominicanum may have been similar to that of the extant Iotonchium californicum Poinar (1991). Fungus gnats of the family Mycetophilidae are common in Dominican amber. The mermithid. which become a secondary host. while additional juveniles are in the amber surround- ing the host (Figure 21). The swollen female nematode and a number of juveniles remain in the body cavity of the fossil fly. Iotonchid nematodes have evolved a complex life cycle alter- nating between insects and fungi. Five specimens of Heydenius scatophilus Poinar (2011) were adjacent to their scatopsid host in Dominican amber. and one representative was parasitized by a member of the Iotonchi- dae lineage. The Dominican amber Paleoiotonchium dominicanum Poinar (2011) probably had a similar dual host life cycle.The Geological Record of Parasitic Nematode Evolution 69 Figure 20 Two specimens of the mermithid. Hey- denius dipterophilus Poinar (2011) had completely emerged from its milichid host in Dominican amber. with their moth fly host in Dominican amber (Scale bar ¼ 800 mm). There appears to be no report of mermithids infecting extant scavenger flies.

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. Poinar. dominicana was placed in the Parasitodiplogaster clade. rounded lip region and elongate tail. however. which is a phoretic stage. Strictly mycetophagous nematodes of aphelenchoidid lineages have also been described from Dominican amber. lack of a stylet. The allantonematid. 1991). The long. Many of them were dauer (resistant) juveniles. thus providing indirect evidence of fig trees in the ancient forest. 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). Palaeoallantonema apionae Poinar (2011) was parasitizing an apionid weevil. and numerous individuals of the diplogastrid. Some 60 specimens of the aphelenchoidid Crypt- aphelenchus dominicus Poinar (2011) were associated with an adult platypodid beetle. Also in Dominican amber are nematode parasites of herbivorous insects. Figure 21 Parasitic juveniles of Paleoiotonchium dominicanum Poinar (2011) inside the body cavity of a mycetophilid fungus gnat in Dominican amber (Scale bar ¼ 75 mm). S. an extant genus that parasitizes figs wasps in Africa and Mesoamerica (Poinar. The stylet-bearing Bursaphelenchus similus Poinar (2011) probably originated from a gallery belonging to an adjacent platypodid beetle. slender. Synconema dominicana Poinar (2011) were adjacent to a fig wasp (Hymenoptera: Agao- nidae) (Figure 22). Jr. A third lineage was represented by numerous individuals of Oligaphe- lenchoides dominicanus Poinar (2011) feeding on a large mat of adjacent fungal hyphae. stylet-bearing adults . Based on their attenuated head. Fossil-parasitic nematodes of higher plants are extremely rare. 1979. Poinar and Herre.70 George O.

Figure 23 Population of the plant nematode. . Extant anguinids can withstand desiccation and survive for years in dried seeds. while another is some distance away. One large specimen is adja- cent to its moth host (Figure 25). Another species of stylet-bearing plant-parasitic nematode in Dominican amber was the anguinid. One interesting lineage of aphelenchoidids in Dominican amber is the Acugutturidae Hunt (1993).The Geological Record of Parasitic Nematode Evolution 71 Figure 22 Parasitic stages of Synconema dominicana Poinar (2011) emerging from a fig wasp in Dominican amber (Scale bar ¼ 545 mm). and males with a C-shaped terminus align the species with members of the Aphelenchoididae. It apparently had been feeding within and then attempted to escape from a seed that fell in the resin. Palaeoanguina dominicana Poinar (2011) (Figure 24). Extant representatives are ectoparasites on the external surface of insects. especially moths. Several specimens of Seto- nema protera Poinar (2011) belong to this family. Oligaphelenchoides maximus Poinar (2011) in Dominican amber (Scale bar ¼ 857 mm).

72 George O. and apparently transfer from moth to moth during mating. especially noctuids. Figure 24 Juvenile female of Palaeoanguina dominicana Poinar (2011) in Dominican amber (Scale bar ¼ 128 mm). Extant species of this family occur on six families of moths. . While the high rate of mermithid parasitism of chironomid midges in Eocene Baltic amber was previously noted. mermithid parasitism of this host group also occurs in Dominican amber as exemplified by Heydenius Figure 25 The ectoparasitic nematode Setonema protera Poinar (2011) (arrow) adja- cent to its moth host in Dominican amber (Scale bar ¼ 245 mm). Several additional specimens are attached to the moth’s abdomen. Jr. Poinar.

1984 inside the body cavity of a Culex mosquito in Dominican amber (Scale bar ¼ 348 mm). Other mermithid lineages. nematode parasites also occurred inside the host. such as Heydenius dom- inicus Poinar (1984) (Figure 26) parasitized mosquitoes. neotropicus Poinar (2011). Foleyella duboisi (Witenberg and Gerichter. Heydenius lamprophilus Poinar (2011) was parasitizing an adult firefly (Coleoptera: Lampyridae) in Dominican amber (Figure 28). Nematodes also parasitized sand flies. .The Geological Record of Parasitic Nematode Evolution 73 Figure 26 A specimen of Heydenius dominicus Poinar. Heydenius saprophilus Poinar (2011) had been parasitizing a wood gnat (Anisopodidae) (Figure 27). 1944). Palaeoallantonema dominicana Poinar (2011) (Figure 29). A second filarial nematode adjacent to another adult mosquito was described as Cascofilaria parvus Poinar (2011). The nematodes resemble the infective stages of the extant frog para- site. A female sand fly of the genus Lutzomyia was parasitized by Palaeoallantonema phlebotomae Poinar (2011). A few fossil blood-sucking flies were found vectoring filarial parasites in Dominican amber. another group of bloodsuckers in the Dominican amber forest. Members of Foleyella infect tree frogs (Leptodactylus spp. One female mosquito was adjacent to an infective and pre-infective stage of the filarial nematode. Aside from those adjacent to the sand fly. It is thought to represent an infective stage juvenile but could not be further identified. Saprophagous flies were also attacked by mermithids in Dominican amber. and a rove beetle (Staphylinidae) was sur- rounded by 44 juveniles of the allantonematid parasite. The host range of mermithid nematodes in Dominican amber is amazingly broad and also includes predatory beetles. 1999).) in South America and Eleutherodactylus tree frogs have been found in Dominican amber (Poinar and Poinar. Cascofilaria dominicana Poinar (2011).

. 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).74 George O. described as Chalcidonema paradoxa Poinar (2011) were tentatively placed in the Aphelenchoididae (Figure 30). Two individuals were projecting from the body of the wasp and one was still inside the wasp. The nematodes. Jr. One interesting record of parasitism unknown today involved several nematodes that had emerged from a parasitic wasp (Hymenoptera: Pteroma- lidae). Poinar. Figure 28 Heydenius lamprophilus Poinar (2011) from a lampyrid beetle in Dominican amber (Scale bar ¼ 914 mm).

2 Mexican amber nematodes The Mexican amber forest was in large part similar to that of the Dominican amber forest with similar insect genera but different species. females. Since the wasp larvae develop as internal insect parasites. showing that the forests were separated long enough for speciation to occur. it is possible that the nematodes were also parasitizing the same host and entered the wasp larva. One of the most spectacular nematode parasites in Mexican amber was a population of the aphelenchoidid.The Geological Record of Parasitic Nematode Evolution 75 Figure 29 A group of parasitic juveniles of Palaeoallantonema dominicana Poinar (2011) adjacent to their rove beetle host in Dominican amber (Scale bar ¼ 233 mm). Males. 6. . eggs and juveniles were present. Oligaphelenchoides atrebora Poinar (1977). along with fungal hyphae Figure 30 Stages of Chalcidonema paradoxa Poinar (2011) (arrows) associated with a chalcidoid wasp in Dominican amber (Scale bar ¼ 471 mm).

that served as their food source (Figure 31). Also present were nematopha- gous fungi that had parasitized several individuals of O. 1986) (Figure 32). one interesting species was the tetratonematid.76 George O. Palaeotetradonema Figure 32 Thick hyphae of a nematophagous fungus inside a specimen of Oligaphelen- choides atrebora Poinar. Few parasitic nematodes have been recovered from Mexican amber. Jr. however. 1977 in Mexican amber (Scale bar ¼ 176 mm). 1977 in Mexican amber (Scale bar ¼ 9 mm). Poinar. . Figure 31 A reproducing population of Oligaphelenchoides atrebora Poinar. atrebora (Jansson and Poinar.

1900). (1993). 1972). in extant populations of K. Strongylus edentatus (Looss.000-year-old ground squirrel (Citellus sp. while all extant cases of horsefly parasitism by mermithids are in larvae (Poinar. the hosts are still extant. The oldest records of various vertebrate parasite lineages are presented below. Didilea ooglypta Tang et al. 2000). 1966). rupestris at the same location (Ferreira et al. Whipworm (Trichuris Roederer) remains date from 30. Horse pinworm eggs (Oxyuris equi Schrank) can be used to place horses at ancient locations (Jansen and Over. NEMATODE PARASITES FROM THE PLIOCENE An interesting Pliocene nematode parasite is the mermithid.000-year-old eggs in coprolites of the caviid rodent. Poinar and Lane..81 mya to 11. Pinworms of the genus Syphacia Seurat were recovered from fossilized remains of a 10. 8. 1991).) (Dubinin. tabanae was emerging from an adult horsefly. The horsefly was identified as the extant Tabanus sude- ticus Zeller.500 BP to 3300 BC. Palisade worms. 1962. NEMATODE PARASITES FROM THE PLEISTOCENE AND HOLOCENE Several vertebrate-parasitic nematodes have been reported from deposits in the Pleistocene that extends from 1. These nematodes are widespread and reproduce in the caecum and colon of horses today (Anderson. Kerodon rupestris. Heydenius tabanae Poinar (2011) emerging from an adult horsefly (Diptera: Tabanidae) in sedimentary deposits in Germany dated at about 2. which occurs in the intestine of rodents worldwide. 7. were recovered from the intestine of a mummified Late Pleistocene horse (Dubinina. 1978).The Geological Record of Parasitic Nematode Evolution 77 phlebotomae Poinar (2011) that attacked a phlebotomine sand fly. In most cases.000e12. 1985). 1985. The authors suggested that climate change was responsible for the disappearance of Trichuris sp.500 BP and the Holocene from 11.5 million years (Grabenhorst. 1948). It is interesting that H. The fossil worms closely resemble the extant species Syphacia obvetata (Rudolphi). Placement in the Tetradonematidae was based on the structure of developing ova in one specimen that was similar in size to ova in the extant sand fly tetrado- nematid. . in Brazil.

1996).000  180 years from Rampart Cave. Klicks. 1889. Egyptian mummies have been an excellent source of human nematodes. However. 1982). these records are not old enough to shed light on the origin of nematode lineages in humans. Rarely it is possible to obtain molecular evidence of parasites from sub- fossilized remains. 1957).000-year-old ascarid eggs from the Pleistocene (Bouchet et al. Agamofilaria oxy- ura Schmidt et al. contained eggs of an oxyurid considered to be Parapharyngodon sceleratus (Travassos. Eggs and larvae of most gastrointestinal parasites have been obtained from coprolites. in Argentina produced elliptical bodies that are thought to be nematode eggs (Ringuelet. latrines and mummies (Gonçalves et al. Arizona contained first stage juveniles of the oxyurid.78 George O. Jr. 1992.. Poinar. especially those ‘natural mummies’ that were preserved with all their organs intact.. (1992) and a strongyloid. Reinhard and Ara ujo. 2003. 2008). 1923) that infects the extant lizard. (2013) reported extracting ancient nematode DNA from four moa species in New Zealand. Wood et al. Some rare fossil nematodes have been obtained from remains of extinct animals such as coprolites from a 1.. 8. 1998).. Mylodon listai Ameghino. Tropidarus torquatus (Ara ujo et al. they do provide important information on the types and geographical distribution of human nematode parasites. Reinhard. Tri- chostrongylidae and Trichinellidae were identified in the moa coprolites. cesspits. While the earliest evidence of human nematode parasites are 30. Nine-thousand-year-old coprolites from a Brazilian iguaniid. (1992). Tropidarus sp.000-year-old boluses of the extinct ground sloth.5-million-year-old extinct Hyaena Bris- son. Strongyloides shastensis Schmidt et al. Using these markers and microscopic analysis.1 Nematode parasites of humans from the Pleistocene and Holocene The search for human nematode parasites by anthropologists and archaeol- ogists falls under the discipline of paleoparasitology or archaeoparasitology (Taylor.. The nematode juveniles could not be identified. nematode representatives of the Heterakoidea. 1999). 1955. 1762. 1990.000e24. Pages from the Papyrus Ebers . 1993). Sandison and Tapp. We know very little about how humans acquired their 138 species of nematode parasites (Crompton. but they could have belonged to either Ancyclostoma or Toxascaris since both genera para- sitize extant hyaenids (Ferreira et al. An analysis of dried 10. Shasta Ground Sloth (Nothrotheriops shastensis) boluses dated at 10.

The Geological Record of Parasitic Nematode Evolution 79

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.

9. STAGES IN THE EVOLUTION OF NEMATODE
PARASITES OF INVERTEBRATES
Nematode parasitism of animals probably first originated in invertebrate
marine hosts with the ‘aphasmidians’ and later on land with the ‘phasmidians’.
It is likely that nematodes arose in the sea as free-living microbotrophs in the

80 George O. Poinar, Jr.

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.

10. ORIGIN OF NEMATODE PARASITES OF
VERTEBRATES
The earliest fossil vertebrates were in shallow, near shore Cambrian
and Ordovician deposits. There is no evidence of their presence in fresh-
water deposits prior to the Early Devonian (Carroll, 1988). In the Silurian
seas, nematodes probably parasitized the primitive-jawed acanthodians

82 George O. Poinar, Jr.

as well as elasmobranchs and the ancestors of coelacanths based on present-
day host records (Poinar, 2011).
It is likely that oxyurids were the earliest nematode parasites of terrestrial
vertebrates, and their antiquity has recently been demonstrated with the dis-
covery of P. cockburni Hugot et al. (2014) in a 240-million-year-old cyno-
dont coprolite (Hugot et al., 2014). There is quite a time lapse to the
next oldest record of vertebrate pinworms in Holocene and Pleistocene de-
posits (Jansen and Over, 1962, 1966; Poinar, 2014).
However, the ascarid lineage may be just as ancient since the Triassic fos-
sil, A. rufferi Da Silva et al. (2014) dates from the same time period and same
host as P. cockburni (Da Silva et al., 2014). The next oldest fossil ascarid par-
asites are the Early Cretaceous A. priscus and A. gerus recovered from an
dinosaur coprolite (Poinar and Boucot, 2006).
The three records of filarial nematodes in amber establish this nematode
lineage in the Cenozoic and show what types of insect vectors were trans-
mitting these parasites. The next oldest records of vertebrate parasitism are
30,000-year-old eggs of A. lumbricoides from human coprolites (Patrucco
et al., 1983) and 30,000-year-old whipworm eggs from coprolites of a caviid
rodent (Ferreira et al., 1991).
The question regarding the original host of heteroxenous parasites (those
using an invertebrate as an intermediate host and a vertebrate as a final,
developmental host) has been debated for years. These nematodes, exempli-
fied by the Spirurida, actually have two infective stages, one for the inver-
tebrate and the other for the vertebrate. Did these heteroxenous
nematodes evolve first in vertebrates with invertebrates becoming second-
arily infected by ingesting eggs in faecal material? Or were invertebrates
parasitized first and the vertebrate cycle was established when the latter hosts
were eaten? Evidence for the invertebrate first theory is that (1) some of
these parasites can complete their entire development in the invertebrate
host and (2) invertebrate hosts appeared in the fossil record before those
of vertebrates.
Unfortunately, the fossil record of nematodes is too sparse to answer this
question; however, estimated dates of the origin of vertebrate- and inverte-
brate-parasitic nematode families can be inferred from the earliest fossil re-
cord of their host group or molecular clock estimates. Regarding the
family Spiruridae Railliet and Henry, 1915, the earliest vertebrate host
group appears in the Cretaceous while the earliest fossil record of an inver-
tebrate host group is in the Carboniferous (Poinar, 2011).

The Geological Record of Parasitic Nematode Evolution 83

11. ORIGIN OF NEMATODE PARASITES OF PLANTS
Plant parasitism evolved independently in at least four terrestrial line-
ages, the Enoplida, Triplonchia, Dorylaimia and Rhabditida (Poinar, 2011).
Plant-parasitic nematodes may have existed in the Silurian or even Ordovi-
cian since the earliest known fossils are from the Devonian (Poinar et al.,
2008). There is no evidence yet of any marine lineage of plant-parasitic
nematodes. Those plant-parasitic nematodes found in the sea are terrestrial
lineages that invaded littoral and sublittoral habitats. These include the
tylench genera Halenchus Cobb (Fortuner and Maggenti, 1987), Hirschma-
niella Luc & Goodey (Luc, 1987) and the aphelench species Aphelenchoides
marinus Timm & Franklin and A. gynotylurus Timm & Franklin (Timm
and Franklin, 1969).
The most primitive higher plant parasites are members of Aphelenchi-
dae, Tylenchidae, Paraphelenchidae, Neotylenchidae and Paurodontidae,
whose lineages could well extend back to the Silurian with early fossil
records of fungi (Taylor et al., 2015). Siddiqi (1983) supposed that tylenchid
plant parasites originated from algal-feeding lineages while Paramonov
(1962) and Maggenti (1971) felt they developed from mycetophagous
lineages.
The oldest aphelench fossil is the Early Cretaceous C. burmensis followed
by the Eocene P. balticus (Poinar, 2011). The above species represent free-
living mycetophages that are probably the primitive aphelench trophic stage.
Just when aphelenchs shifted their diet to higher plants is not known, but the
Dominican amber Oligaphelenchoides maxima is considered to represent an
aerial parasite with a biology similar to some extant Aphelenchoides spp.
The fossil Palaeoanguina dominicana that was developing in a seed in Domin-
ican amber is further evidence of obligate parasitism of aerial portions of
plants. This species probably had a life cycle similar to some extant members
of the genus Anguina Scopoli (Fortuner and Maggenti, 1987).

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.

elasmobranchs and primitive marine fish as hosts based on extant parasitee
host associations (Poinar, 2011). Since their fossil record is so sparse, deter-
mining the evolutionary clocks of the many lineages of parasitic
nematodes, each of which evolved independently, is difficult. However,
the minimum longevity of some nematode orders and infraorders can be
determined by body fossils (Figure 33), and time constraints on other lin-
eages can be inferred with molecular clock methodologies. However,
morphology and molecular methods do not always match. For instance,
some molecular clock studies place the origin of ascarids in the Jurassic
(Blaxter, 2009), but this is clearly incorrect since ascarid body fossils occur
in the Triassic (Da Silva et al., 2014). Since most nematode families have
multiple hosts, the earliest fossil of the most primitive host can be used
to estimate the possible date of origin for various nematode groups (see
Poinar (2011)). Using fossil host records, the earliest animal-parasitic nem-
atodes would have been members of the marine families Benthimermithi-
dae, Tetradonematidae and Leptolaimidae, whose invertebrate host groups
extend back to the Cambrian. The earliest terrestrial animal parasites would
be Thelastomatoidea, Rhigonematoidea and Ransomnematoidea that
parasitized millipedes, which have a body fossil record dating back to the
Silurian (Wilson and Anderson, 2004). The first vertebrate parasites would
have used elasmobranchs and primitive marine fish as hosts (Poinar et al.,
2014). The earliest higher plant parasites, which could have evolved
from mycetophagous lineages as far back as the Silurian could have been
lineages of Aphelenchidae, Paraphelenchidae, Neotylenchidae, Paurodon-
tidae and Tylenchidae (Poinar, 2011). With so many different lineages of
nematode parasites, it is only natural to assume that parasitism has evolved
convergently and independently in multiple lineages of nematodes. Ac-
cording to recent molecular studies (e.g. Blaxter and Koutsovoulos,
2015), plant parasitism has evolved at least three times, animal parasitism
has arisen at least ten times across a wide range of invertebrates and five
times in vertebrates hosts within the three nematodes subclasses. However,
many additional origins of parasitism could be proposed based on firm
morphological data. Sudhaus (2008, 2010) used morphological characters
to show that there are at least 20 independent origins of insect parasitism
by nematodes.
We look forward to the discovery of additional nematode fossils associ-
ated with identifiable host remains (including coprolites) that will help us to
better understand the origin and evolution of nematode parasitism of verte-
brates, invertebrates and plants.

The Geological Record of Parasitic Nematode Evolution
Figure 33 Minimum longevity of nematode orders and infraorders based on body fossils. Numbers refer to mya (million years ago).

85

86 George O. Poinar, Jr.

Molecular clock methodologies are extremely important, and together
with morphology, the two disciplines complement each other very well.
Together they can show relationships between extant lineages, perform
ancestral host reconstruction with phylogenetic dating analyses and deter-
mine when various lineages might have appeared in geological time (Sung
et al., 2008; Poinar et al., 2011).

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

Constraining the Deep Origin of
Parasitic Flatworms and Host-
Interactions with Fossil Evidence
Kenneth De Baets*, 1, Paula Dentzien-Diasx, Ieva Upeniece{,
Olivier Verneaujj, #, **, Philip C.J. Donoghuexx
*Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€ urnberg, Erlangen, Germany
x
Nucleo de Oceanografia Geol ogica, Instituto de Oceanografia, Universidade Federal do Rio Grande,
Rio Grande, Brazil
{
Department of Geology, University of Latvia, Riga, Latvia
jj
Centre de Formation et de Recherche sur les Environnements Méditerranéens, University of Perpignan Via
Domitia, Perpignan, France
#
CNRS, Centre de Formation et de Recherche sur les Environnements Méditerranéens, Perpignan, France
**Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa
xx
School of Earth Sciences, University of Bristol, Life Science Building, Bristol, UK
1
Corresponding author: E-mail: kenneth.debaets@fau.de

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,

sometimes referred to as the cercomer theory (Lockyer et al. Subsequently. 2007. Laumer et al. primitive parasitic flatworms (Neodermata) were probably ecto- parasitic with a simple life cycle on vertebrates (Park et al.. Hahn et al. probably first a crustacean intermediate host in Cestoda and a mollusc intermediate host in Trematoda (Park et al... 2001). Littlewood. 2007).. 2003a). Wey-Fabrizius et al. the sis- ter-group relationship between Monopisthocotylea and Polyopisthocotylea based on morphological data (Boeger and Kritsky. where a sister-group relation between Mon- ogenea and Cestoda. with the crustaceans as subsequent inter- mediate hosts adopted by the Cestoda groups after the ancestral cestode diverged from the monogeneans (mollusk first hypothesis). Littlewood et al. 2010). and between these taxa and Trematoda was postulated.. However. Justine. 1997... The closest free-living relatives of helminths are also important in con- straining divergence times in their evolutionary history (Littlewood et al. 1989. One hypothesis (Littlewood et al. it has been proposed they added an intermediate host to their life cycle. This differs from previous hypotheses (Brooks. Another hypothesis (Cribb et al. Egger et al. However.. and that the vertebrates were involved in the life cycle of the common ancestor of the Monogenea þ Cestoda clade as independent initial hosts apart from that of trematodes. 2003a... This led to two now probably outdated hypotheses of interpreting the life cycle evolution of Neodermata (Park et al.. Perkins et al.. 2014.. 1998. 2014.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 95 1989). Based on recent results employing mitoge- nomic data.e. 2007) before switching to a blood diet (Perkins et al. the monophyly of Monogenea i. 1997.. 1999b. Park et al. 2006). 2010. the phylogeny of . 2013) indicate a sister-group relationship between cestodes and trematodes (rather than between Mono- genea and Cestoda) with one possible exception (Laumer and Giribet. Near. 2001) suggested that the association of common ancestor of the Trematoda with molluscan hosts was primitive (acquiring its subsequent vertebrate hosts indepen- dently). is not always sup- ported by molecular phylogenetics (Mollaret et al. 2013. 1999a) suggested that proto-neodermatan first acquired an endoparasitic association with vertebrates and that independent adoptions of invertebrates by the Trematoda (molluscs) and Cestoda (crustaceans) as well as ectoparasitism in Monogenea were subsequent acquisitions (verte- brate first hypothesis).. Lockyer et al... most recent molecular-based analyses (Mollaret et al.. 1999a). 2007) and engaged in epithelial feeding (Perkins et al... 2003a) either. Interestingly. 2015). Lockyer et al. 2002. although no clear morphological characters support this arrangement. 2015) and those including alter- native data such as microRNAs (Fromm et al. 2010)..

Telford et al. Philippe et al. 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.. 2007. 2009) such as the Acoela (Ruiz-Trillo et al. 2011) and Xen- oturbella (Bourlat et al.. 2013) or remain associated with their hosts (Upeniece. 2013). 2006. Hejnol et al.. which can be isolated (Poinar and Boucot. Weber et al.. We consider whether these rare fossil finds are at least consistent with coevolution of parasitic flatworms and their hosts. 2001. 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. 2002. 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. but also on the relation- ships within this grouping. 2010. 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. platyhelminths have often been grouped in the Platyzoa (Cavalier-Smith.. Dentzien-Dias et al.. 2011) or (2) more commonly occur as characteristic . 1999. which have convergently evolved a parasitic lifestyle with larval stages and have been shown to be closely related with free-living Rotifera (Near. It remains unclear whether Platyzoa is a clade or an artificial grouping generated by systematic error and long-branch attraction artefacts (Edgecombe et al. 2014)...96 Kenneth De Baets et al. 1998) together with various other taxa including Acanthocephala... 2006.. 2011. 2. 2002. since subsequent studies have not only disagreed on the membership of the phyla. Struck et al. Mwinyi et al. Wallberg et al.. 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.. 2013.. free-living flatworms has proven even more problematic (but see Littlewood and Waeschenbach. Wey- Fabrizius et al. Willems et al. major environmental changes or key ecological or evolutionary events in the evolution of their hosts. Furthermore. 2003). ASSESSMENT OF THE FLATWORM FOSSIL RECORD Fossil evidence for parasitic flatworms can be derived from (1) rare exceptionally preserved body fossils. 2003.

Littlewood and Donovan. f)). while in placoderms (A. 2011) might even indicate that they belong to different groups . 2011) are the oldest potential body fossil evidence for parasitic flatworms. one isolated circlet was found close to a specimen of a clam shrimp (Figure 1(g)) and two other circlets were found associated with another crustacean arthropod (Mysidacea: Figure 1(e)). 2001. lack of hard parts and the residence within the host and/or isolation from their hosts (Conway Morris. which have the potential to be traced back in the fossil record (Ruiz and Lindberg. Huntley and Scar- poni. However. c. 2. 2011. 1996. Huntley.. 1999. Littlewood and Donovan. Upeniece (2001. they are associated with the gill regions. 2003. 2011) discovered about 77 cir- clets. The rarity of fossilized parasiteehost associa- tions and the fact that culprits of traces or pathologies in the skeletons of their hosts are often hard to identify can make it difficult to infer parasiteehost associations from the fossil record. 2015). Huntley et al.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 97 traces or skeletal pathologies in their (intermediate) hosts. Ituarte et al. Cestoda) and Acanthocephala to attach themselves to their hosts. which were mostly attached or closely associated with fossil gnathos- tomes (16 juveniles of the antiarch placoderm Asterolepis ornata. Ruiz.. it is the only direct evidence for the presence of such associations in the geological past. 1998. 2011). 2012. 2003. Huntley and De Baets.1 Devonian fossil hook circlets Circlets of fossil hooks described from the Devonian of Latvia (Upeniece. The length of infested fishes varies between 1 and 4 cm (Figure 1(a) and (d)). 2011). Huntley and Scarponi. 2014. and in the abdominal region near the scapula (Figure 1(d) and (f)). In acanthodians (L. strongly sug- gest a parasitic nature (Upeniece. Todd and Harper. but the hooks are too large to indicate parasitism based on the size of the crustaceans. Nevertheless. e. Differences in morphology and their location on the host body (Upeniece. Upeniece. 2001. 2007. The location of these remains in fossils of their vertebrate hosts (Figure 1(b) and (c)) and their similarity to the hooks of parasitic helminths. 1989. near the fin spines. 2001. De Baets et al. gaujicus). although their exact affinity remains the sub- ject of debate (Upeniece. 1991. 2011). 1981.. Several of them were infested with 2e9 parasites (7 hook circlets can be counted in the specimen figured in Figure 1(b)). Most authors agree that they are the remains of parasitic helminths. 2005. ornata) their location is not so well determined (see Figure 1(a)). Parasite body fossils are scarce due to their small size. These are reminiscent of hooks which are used by Neodermata (Monogenea. 27 specimens of the acanthodian Lodeacanthus gaujicus: Figures 1(b. 2015.

Figure 2). 2011) (Modified from Upeniece (2011) unless otherwise stated. (a) (b) (c) (d) (e) (f) (g) Figure 1 Fossil helminth remains in Middle Devonian gnathostomes (Upeniece. (c) Close-up on the hook circlet found associated with L. (d) Locations where helminth remains were found in juvenile and adults of the . (b) Multiple fossil circlets of parasitic helminth hooks (marked with ellipses in (a)) found inside the acanthodian Lodeacanthus gaujicus. specimen LDM 270/ 33.98 Kenneth De Baets et al. gaujicus. 2001.): (a) Locations where hel- minth remains were found on juveniles of the placoderm Asterolepis ornata. 3. 2001. LDM 270/18c (Upeniece. Pl.

gaujicus. Light grey circles. squares e possible endoparasites. 2001. indicates that at least some of them represent Monogenea (Combes. Poulin (2005). present even in basal extant Cestoda like Gyrocotylidae (Xylander. (g) fossil hooks found near a clam shrimp. gaujicus (No 12e23). although the larvae of Cestoda can also have radially arranged chitinous hooks for attachment. This holdfast organ is only fully evaginated after death and resembles the ‘introvert’ of Rotatoria. 2005). ornata (No 1e11). but this does not necessarily rule out a monogenean affinity. Liepa (Lode) pit. No. She noticed that the hooks with ‘handles’ typically occur in the abdominal region of acanthodians and placoderms. cestodes and acanthocephalans). Upeniece. 17). for ex- ample. The elongated tube- like body of acanthocephalans typically possesses a thorny proboscis. which is an anterior retractile organ bearing a large number of hooks (Bush et al. Upeniece (1999. which is characteristic for early divergent monogeneans (Boeger and Kritsky.02e0. 2005) and Amphilinidea (typically 10). (e) Schematic drawing of circlets of fossil hooks (Modified from Upeniece (1999). The circular arrangement of the bilaterally symmetrically located hooks.) found in juveniles of placoderm fish A. suggestive of a close affinity with endoparasites such as Acanthocephala or Cestoda. 2011) suggested that at least two morphological groups are presented in both species of fish: hooks with a ‘handle’ and hooks without a ‘handle’.g. Larval forms of Cestoda typically bear hooks. monogeneans) and endoparasites (e. which might further corroborate a similarity to early divergent parasitic flatworms. with the exception of traces of the disc outline. Dark grey circles.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 99 of parasites (Upeniece. LDM 270/4a. (f) Fossil hooks found in juvenile acanthodian body near the scapula (see also Figure 1(e). 2001). Upeniece (2011) observed that small-sized acanthodians possessed small hook systems. traces of cuticular disc as well as the maximum number of 16 hooks. Kinorhyncha and Nematomorpha larvae (Taraschewski. 2011). 1993). and in/on crustacean Mysidacea (No 24). Interestingly. in juveniles and adults of acanthodian L. squares e possible ectoparasites.g. while larger acanthodians exhibited the greatest range in size of the hook systems. which can be retained in the adult forms = acanthodian L. These might indicate that parasites might have spent all their life in one host. could demonstrate an evolutionary trend towards decreasing body size in extant ectoparasitic Monogenea. 2001). further hampers a more precise taxonomic assignment. The hooks are also considerably larger (length: 0. while this was less clear for derived endoparasitic flatworms (Digenea). All speci- mens derive from the Middle Devonian.40 mm) than those of extant flatworms. . Priapulida. The lack of fossilized soft body parts. including ectoparasites (e..

Petit and Khalloufi. 2012. such as in Amphilinidea (Rohde. 2011.. 2003). 1999. However. 2012). 2005. their composition (element analysis) and the three-dimensional structure using computer tomography can be particularly useful for disen- tangling phylogenetic affinity as it did for the elements of the now-extinct conodonts (Purnell and Donoghue.. Upper Devonian (Upeniece. the characteristics of these (Luksevics et al. Luksevics et al. Middle Devonian (Mark-Kurik et al. Interestingly. 1997. although no conclusive evidence for a parasitic flatworm infestation was found (De Baets et al. 2005). Whatever the exact taxonomic affinity of the parasite hook circlets. A reinvestigation of these attachment structures with particular focus on taphonomy. . the minimum age assigned to the GivetianeFrasnian boundary (382.. 2005). 2013). 2015). 2001). 2001). Mark-Kurik and P~oldvere. 2012). 2014). which may be armed with hooks arranged in one or more circles (Bush et al. 2012) are insufficient to attribute them to partic- ular group of parasites confidently. Luksevics et al. This corresponds with at least 381..7 Ma  0... some Cyclophylli- dea have a dome-shaped structure at the end of the scolex. although we cannot entirely exclude the possibility that they belong to a now-extinct lineage of parasites. while others like Trypanorhyncha can have a scolex with four retractable tentacles bearing hooks (Caira and Reyda. Poinar. or even rule out potential other causes. Murdock et al.. Famennian) gnathostomes to cestode and trematode infestations. 2005). Derived Cestoda have a specialized attachment device (the scolex) that has a highly variable morphology and may have hooks: Diphyllidea typically possesses a scolex bearing a dorsal and ventral set of apical hooks (Caira and Reyda. 2012. they also overlap temporally with the presence of blister pearls in Devonian ammonoids (Rakoci nski. 2012. 2011. Luksevics et al. 2011.. Most au- thors agree that the fossil circlets of hooks probably belong to platyzoan hel- minths (Upeniece. they remain the oldest direct evidence for the presence of helminthegnathostome and helminthevertebrate association in the fossil record (Boucot and Poinar. 2010). Age: The finds of the Lode Formation were described initially as Early Frasnian. 2010. which might also have been caused by parasitic flatworms. 2001. Jurina and Raskatova. Goudemand et al. 2009) and other pathologies like skin lesions (Petit.9 Ma.100 Kenneth De Baets et al. It is common practice in geolog- ical and paleontological studies to use Ma for ‘Million years ago’. 2013.8 Myr: Becker et al. (2009) attributed various skeletal pathologies from Mid- dle (Givetian) to Upper Devonian (Frasnian. the rostellum. although most authors now assign this to the Upper Givetian.. while XX Myr is often used to refer to a duration of XX million years.

Liljedahl. 1983). shell burrowing organisms and inorganic particles (G€ otting.. 2015). However. Todd and Harper. 1985. 1985.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 101 2. 1979. Molecular clock es- timates usually place the origin of shorebirds in the Cretaceous (Paton et al. which these authors traced back to 6400 years in the Holocene. Figure 2(d)). Baker et al. 2012. The earliest fossils that can be confidently assigned to extant lineages of charadriiform birds are stem-group representative of Alcidae from the Upper Eocene of North America (Mayr. Conway Morris. although some forms also infest humans as final hosts (Lee and Chai. Su- perficially. 2007. although older charadriiform-like fossils have been reported from the Lower Eocene of Denmark (Bertelli et al. 1974.2 Silurian blister pearls and calcareous concretions in bivalve shells As (blister) pearls and volcano. Pearls and blisters can. 2001. 2001. Huntley et al. The earliest known fossil blister pearls from the Silu- rian (Kríz. 2001. 1994. 1985. although this might be based on the incorrect .. 2011). which typically have shorebirds (Char- adriiformes) as final hosts (Ching. Huntley and Scarponi. Ituarte et al. 2005. 2005). 1979.to igloo-shaped calcareous concretions (Campbell. be caused by a variety of irritants. 2011) might already indicate the presence of derived parasitic flatworms in the Silurian. Lauckner. other pathologies are believed to be more characteristic for particular lineages of parasitic flat- worms such as Gymnophallidae including shell pits (Ruiz and Lindberg. 1983).. 1983. 2005) demonstrated a link between igloo-shaped concretions and gymnophallid digenean flat- worms. 1991.. 1979. 1981. 2005. but the Paleozoic occurrence of this structure is not consistent with extant host associations of Gymnophallidae. This is not straightforward since it has been demon- strated that the remains of soft-bodied helminths can be destroyed during the pearl formation process (Lauckner. 1989. 2007). their first occurrence in the Silurian (Kríz. (2001. Ituarte et al.to igloo-shaped concretions can be induced by intermediate stages of parasitic flatworms (G€ otting. Figure 1(e). Geyer et al. Ituarte et al... Figure 2(aec). however. 1985. Boucot and Poinar. Huntley and De Baets. 2015. 2001).. 2014.. 2011). 1995). 2003. 2015) and volcano. 1937. Campbell.. however. 1985. Ruiz. Huntley. also been reported from the Upper Silurian (Liljedahl. 2010) are therefore not character- istic for parasitism unless parasitic remains can be found inside of them (De Baets et al. Huntley and Scarponi. including other parasites. Rouse. 2010. Liljedahl. Combes. 2011. 2005. 2013). Huntley and De Baets. similar igloo-shaped concretions have. 1994) and earliest known free pearls from Triassic (Kutassy. De Baets et al. 1974. Lauckner. 1994.

note the noncalcified area around the anterior end of the larva (photo: Cristian Ituarte. (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.). (2005). refigured from Ituarte et al. compare Todd and Harper (2011).102 Kenneth De Baets et al.). refigured from Ituarte et al. (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). . 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.). (2005). (2005). Photo courtesy of Jon Todd. (a) (b) (c) (d) (e) Figure 2 Shell structures (igloo-shaped concretions. (a) Metacercaria lodged in live position into an igloo-shaped calcareous covering of Gaimardia trapesina (MLP 5659) from Beagle Channel in Ushuaia. (b) Scanning electron micrograph of a left valve of Cyamiomactra sp. (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. shell pits) which have been linked with gymnophallid trematodes (Digenea) in extant and fossil bivalves.). refigured from Ituarte et al.

2. (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).. smooth shelled and with a small operculum (polar swelling) suggesting that they are nonerupted eggs (Figure 3(c) and (d)).7 Ma (Melchin et al.. 2012. Ksepka et al. personal communication 2014). 2014). It was identified as a shark coprolite by its spiral structure and fossil content (Dentzien-Dias et al..45  0. 2012).. Todd and Harper. Mayr.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 103 placement of fossil taxa (Dyke and Van Tuinen.. 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. 2004. 2004. which was isolated from its host and forms part of a set of more than 800 coprolites of different shapes and sizes found in a geograph- ically restricted area (Dentzien-Dias et al. (2012) for the Gr€ otlingbo bentonite at the nearby locality H€ orsne 3. 1994). 2011. 2013). 2015). Shell pits have so far been traced back only to the Eocene (Ruiz and Lindberg.. Huntley and De Baets.3 Permo-Carboniferous egg remains in shark coprolites The earliest confident record of parasitic flatworms with complex parasite life cycles are eggs attributed to Cestoda from the Rio do Rasto Formation (Dentzien-Dias et al. 2013). although we cannot rule out the possibility that gymnophallids. The eggs occur in a cluster (Figure 3(b)) and are ovoid. which has been correlated with M€ ollboss 1 (Jeppsson et al..18  0. 1994) with similar behaviour.35 Myr obtained by Cramer et al. 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. 1985.4796 Myr. Thomas et al. 2011) and/or other methodological artefacts (cf. 1985. which has been assigned to the Middle to Late Permian (Holz et al. The eggs vary little in size within the cluster. 2012. or closely related (now potentially extinct) taxa or their ancestors. The eggs were obtained from a coprolite (Figure 3(a)).. The top of the Pristiograptus dubius parvus e Gothographus nassa graptolite biozone has been dated to 428. yielded an minimum age of 427. Jeppsson et al. The morphological features . 1989. Most eggs are filled with pyrite and one egg is suggestive of containing a developing larva (Figure 3(c) and (d)). This is consistent with UePb age of 428. which is more or less consistent with the pres- ence of gymnophallideshorebird associations (Figure 2). 2006) and probably accounts for some of the sil- ification of the strata there (Mikael Calner. ranging from 145 to 155 mm in length and 88e100 mm in width. 2013). had different life cy- cles and host associations in the past. 2010).

. which has yielded the cestode eggs. The coprolite should therefore be older than the Guadalupian (Capitanian)eLopingian (Wuchiapingian) boundary dated to at least 259. before destructive thin section analysis. Abbreviations: C ¼ capsule or shell. I ¼ inner envelope. Op ¼ operculum. S ¼ somatic cells. of these eggs (operculum. M ¼ oncospheral membrane. 2012). (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. which has also yielded a variety of vertebrate faunas (Dentzien- Dias et al. (c) Cestode egg with a developing embryophore. O ¼ outer envelope. where verte- brate faunas indicate a Guadalupian (Late WordianeCapitanian) age (Cisneros et al. The locality is located near Posto Queimado. which is typical of modern tapeworm eggs deposited in mature segments or proglot- tids. H ¼ putative developing hooklets. 2012. (b) Thin section of the coprolite part con- taining parasite eggs clustered in. 2012). Dias-Da-Silva. egg shape and size: Figure 3(c) and (d)) as well as their deposition together in an elongate arrangement (Figure 3(b)).4 Myr: Henderson et al.104 Kenneth De Baets et al. (2013). P ¼ putative polar thickening.. 2012). (d) Partial reconstruction of egg in (c) with interpretations of the observed structures. . corroborates their cestode affinity..8  0. E ¼ embryophore (ochosphere). Age: The coprolite derives from the upper member of the Rio do Rasto Formation.): (a) Picture of the spiral heteropolar coprolite from the Rio do Rasto Formation.4 Ma (259.

. 1990. However. However. 2013). 2003. dunkeri . theropod coprolites are rare (Hone and Rauhut. Combes. 2010). 2.... 1976. Age: The Cobelodus aculeatus specimen with the putative cestode eggs derives from the Stark Shale. but the latest discovery of cestode eggs in a Permian shark coprolite (Dentzien-Dias et al. The producers of these coprolites (and therefore also hosts of the parasites) are still debated (Chin et al. 2012) can therefore be used as minimum constraint. Rosscoe and Barrick. 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. 2011).. particularly when compared with coprolites of aquatic verte- brates (Chin. which also includes the Stark Shale (Rosscoe. Strictly speaking. It was assigned to the Westphalian D by Zangerl and Case (1976) without any in- formation corroborating this assignment. Dentzien-Dias et al. Baele et al.. it could extend range of cestode eggs in shark coprolites by an additional 40 Myr. Pending reinvestigation of this fossil. 2001) or other parasitic helminths. 2002) such as crocodylians in contemporary deposits (Hunt et al. which largely corresponds with the Kasimovian (Falcon-Lang et al. 2012). as it is based on the co-occurence of a single metarsal in the same deposits. this coprolite should be called a cololite as the fossilized faecal remains were found lodged within its producer (Hunt et al. 2008. Both Bertrand (1903) and Poinar and Boucot (2006) pre- sented arguments that they could have been produced by theropod dinosaurs (as opposed to crocodiles). An age older than the Kasimoviane Gzhelian boundary (303. Nebraska.. the core black shale member of the Dennis Formation of the Missouri Series. 2013). Poinar. The Missouri series form part of the local Missourian stage. 2013) illus- trate that their interpretation as helminth eggs cannot be excluded. 1998. 1976. Combes.6 Ma according to the 2012 Geological Timescale: Davydov et al. This metatarsal was originally assigned to M.4 Cretaceous egg remains in terrestrial archosaur coprolites The oldest fossil evidence for Trematoda is an egg which was recovered from an Early Cretaceous isolated terrestrial vertebrate coprolite found near Bernis- sart in Belgium (Poinar and Boucot. 2001) within a Carboniferous coprolite are still controversial (Boucot.. near Fort Calhoun.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 105 Older reports of potential cestode eggs (Zangerl and Case. 2006). Their seemingly precise assignment to ‘Megalosaurus’ dunkeri is therefore questionable. further analyses of the morphology and the arrangement of these spherical bodies are necessary to confirm their assignment to cestodes (Zangerl and Case. 2012).

Ruiz and Lindberg. see review by Huntley and De Baets. Never- theless. 2009. 2001. M0r and the basal part of M0n. Studies on pathology have focused on invertebrate intermediate hosts (Ruiz and Lindberg. 2001. 2005). Age: The fossil-bearing strata are now more precisely dated to be of Late Barremian to Early Aptian age (Yans et al. Yans et al. 2005).7 Ma. Huntley and De Baets.. 2014. 1989. although superficially similar structures might also be caused by other digenetic trematodes such as Lep- ocreadiidae (Ituarte et al. 1985. 2001. Schnyder et al. 2011). 2011.. 2007. This yields an approximate minimum age for these strata of 125. 2012).. 1989. (2012). 2012). Eocene (Todd and Harper.. These characteristic pits have been reported throughout the Cenozoic from the Eocene to the Holocene (Johannessen. 1989. 2006). Huntley et al.106 Kenneth De Baets et al. . but its morphology is only sufficient to assign it to theropods at best (Pascal Godefroid. 2014. Ruiz. Age: The oldest precisely dated shells (Venericor clarendonensis) with pits derive from subdivision B2 of the London Clay. Huntley et al.. corresponding with the upper part of magnetochron M1n.. Further support could come from the distribution of volcano-shaped (Campbell. 2011). which have been traced back to at least 6240  70 years BP in the Holocene (Ituarte et al. These pits have been commonly linked with Gymnophallidae (Ruiz and Lindberg. Todd and Harper. 2012.. Berggren and Aubry (1996) assigned this unit to upper calcareous nannofossil zone NP11.. they are believed to be characteristic for gymnophallid trematodes (Campbell. or a more conservative age of 125.. it remains the oldest evidence for trematodes in terrestrial predatory archosaurs (Poinar and Boucot. Huntley and Scarponi. Huntley and Scarponi. 2007. 2005.. Huntley. the age assigned to the base of the Tethyan Deshayesites deshayesi ammonoid biozone (Schnyder et al. 2015. Huntley.. 2001. 2009) by Ogg et al. 2015). Figure 2(e).. Ituarte et al. 1991.9 Ma according to the 2012 Geological Timescale (Vandenberghe et al. Huntley and De Baets. 2011). 1973. 2015). Todd and Harper. which corresponds with a minimum age of 53. (now Altispinax dunkeri). 1985) to igloo-shaped calcareous concretions (Ituarte et al. 1989. 2012. personal communication 2014). 2005. Despite a certain degree of variability in these structures in extant bivalves. Todd and Harper. Ituarte et al.5 Eocene shell pits in intermediate bivalve hosts The oldest evidence for the presence of Gymnophallidae might lie in the Eocene in the form of characteristic shell pits found in their intermediate bivalve hosts (Ruiz and Lindberg. 2. the age attributed to the top of magnetochron M0r by Ogg (2012).93 Ma. 2005).

Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 107 2015). mostly from archeological sites (see Gonçalves et al.. They could not be assigned to a partic- ular genus.000 years BP for Cestoda. Searcey et al. including genera and species. 2003.. 2012) and could potentially be found in the fossil record (cf. 2003 for a review. 1999) during a cold and dry climatic period (Lumley et al. 1984). 2002. Johnson and Sutherland. 2013. limb malforma- tions e including supernumerary limbs and bone bridges e can have various other causes. The age assignment used in archeological publications can be a bit confusing.. 2014). Age: The coprolite (H13 HEN5 1526) derives from an archeological layer at the Caune de l’Arago cave (Tautavel. although some pathologies in vertebrate intermediate hosts have also been linked with parasitic flatworms.. Beltrame et al. The best examples are probably the teratological limb malformations in North American amphibians. the brown colour and the presence of an operculum) is characteristic of dicrocoelid flatworms. which makes this the oldest direct evidence for the presence of dicrocoelid flatworms (Digenea: Dicrocoelidae). The morphology of the eggs (asymmetrical shell. They can provide upper constraints for the earliest appearance of various taxa of Cestoda and Trematoda. 2001. which these authors attributed to Ursidae based on its morphology and associated fossil finds. which starts at the 1st of January 1950 reflecting the fact that radiocarbon dating became practicable around that time and also antedates large-scale nuclear weapons testing altering the global ratio of carbon isotopes (Taylor. Nevertheless. . 2012). with possible ages up 6368 years BP for Trematoda and ages up to 10. 2004. Ara ujo et al.. 2. 1999).6 Eggs remains in a Pleistocene mammal coprolite The oldest Quaternary flatworm evidence is derived from an isolated Mid- dle Pleistocene mammal coprolite ( Jouy-Avantin et al... Lunde and Johnson. 2002.. 2014). although their dimensions are reminiscent of Dicrocoelium and Eurythrema based on egg measurements.. Stopper et al. 2003. 2. Pyrénées-Orientales.7 Holocene evidence for parasitic flatworms from ancient remains Other Quaternary parasitic flatworm fossils and subfossils derive from the Holocene. Koprivnikar et al. 2014. John- son and Chase.. Before Present (BP) stands for a timescale.. France) and could be dated to a minimum age of 550.000 years BP (Jouy-Avantin et al. Fr€ obisch et al. meaning their interpretation is not always straightforward (Blaustein and Johnson. which have been linked with the trematode Ribeiroia on several occasions (Johnson et al.

We herein use the dates mentioned in the orig- inal publications to avoid confusion. haematobium were one of the earliest to be discovered in Egyptian mummies. 2001). Archeological publications often use BC (Before Christ) and AD (Anno Domini). Dicrocoelium can be traced back to 3384e3370 BC (Dommelier Espejo. Anoplocephalid remains which could be more specifically deter- mined as Monoecocestus can be found in rodent coprolites dated as old as 6700  70 years BP (Sardella et al.. Hundred years BP is 100 years before 1950 (i. According to Gonçalves et al. 1990) and Schistosoma ova in another contemporary mummy (Reyman et al. 2010). The record of ano- plocephalid cestodes can be traced back to at least 8920  200 years BP based on eggs founds in coprolites attributed to humans (Fugassa et al. 2003). The oldest free-living flatworm body fossils derive from ... the year AD 1850). and as Clonorchis sinensis could be traced back to a mummy from Chu Dynasty (475e 221 years BC) with an age of at least 2171 years BP (Wen-yuan et al.. 2012).108 Kenneth De Baets et al.. 2003) and Taenia eggs from an Egyptian mummy attributed to about 3200 years BC (Reyman et al. Remains of the Cestoda Diphyllobothrium pacificum can be traced back to about 10. 2013). 1985). Note that age assignment might change or differ according to the dating methods used (Iles. trematodes (Fasciola as well as Opisthorchioidea) can be traced back to at least 5400  40 to 5230  40 years BP (Roever-Bonnet et al. The earliest reports of Hymenole- pis were dated approximately from 4000 to 2000 years BC (Gonçalves et al.8 Free-living flatworms The body fossil record of free-living flatworms is also of little help as it is poorer or even more patchy than the fossil record of parasitic flatworms (Poinar.5 Ma. 1977). 1977). which might range from about 6368 years BP to the 694  30 years BP. ancient DNA of echinostomatid trematodes was extracted from coprolites of the extinct ratite bird Megalapteryx from New Zealand (Wood et al.. Recently.000e4000 BP according to Reinhard (1992).. Schistosoma can be traced back to 3200 years BC based on the discovery of Schistosoma haematobium antigen in the shin tissue of an Egyptian predynasty mummy (Deelder et al. 2010). 1980). Eggs of S. although the exact evidence for such an age were not discussed in this paper. 1979).. the difference between BP and AD becomes negligible. 1984). 2. At ages older than about 0.e. coincident with the time of their extinction (Wood et al. We recommend using the most conservative age estimates using reliable methods.. (2003)..

Acanthocephala) and free-living taxa (Wey-Fabrizius et al. 1984). Palij et al. 1979. and those of flatworm egg capsules from Qua- ternary lake sediments (Frey. Poinar. Conway Morris. 2007). Harmsworth. Even Dickinsonia was assigned to flatworms at one point (Palij et al.. Knaust. Otsuka and Sugaya. Elicki and Wotte... 2008.. but could also have been produced by other taxa with similar behav- iour (Buatois et al. 2007. 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. Erwin et al. 2002. 1968. Various Permian to Triassic trace fossils have also been attributed to turbellarians including Polycladida and Tricladida (Alessandrello et al. 2000. 2007). 2006. although they cannot be confidently assigned to the phylum (Conway Morris. 2013). 2012). 2011). These fossils considerably post-dated divergence time estimates for free-living flat- worms derived from molecular clock studies. 1997. Brasier and Antcliffe. 1988. 2003). 2000. Gray. 1964. 2010). Older molecular clock studies place the origin of (free-living) Platyhelminthes deep in the Precambrian (Hausdorf. 1985). Kouchinsky et al. Curvolithus has also been attributed to flatworms (Seilacher. Erwin et al. 2004. which has also been followed in some recent classifications (Amin. 1979... a group currently containing both parasites (Platyhelminthes. 2004. Sperling and Vinther. The assignment of Cambrian fossils (cambroclaves) to the Acan- thocephala as suggested by some authors (Qian and Yin. 2003) and calcareous nodules of Miocene age (Pierce. 2012). is highly question- able and widely rejected (Conway Morris et al.. 2003). These problematic Cambrian organisms can be classified as Lophotrochozoa at best (Kouchinsky et al. but more recent relaxed molec- ular clock studies place their origins between the latest Precambrian (Edia- caran) and the early Cambrian (Douzery et al. The oldest parasitic flatworm fossils are therefore not only important for putting constraints on free-living flatworms. Fedonkin. 1975. but also on the presence of Platyzoa in the fossil record.. 1981). The taxonomic position of Dickinsonia has been heavily debated (Retallack. 2013). 2011).. 1981. 1960. 2010). Compare Conway Morris and Crompton (1982) and Near (2002) for further speculations and hypotheses on the origin and evolution of parasitism towards . 1998).. Knaust. 1988). 2003. 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.. 2010). Labandeira.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 109 Eocene Baltic amber (Poinar.. 2008) and this taxon is often inter- preted as one of the earliest divergent metazoans (Xingliang and Reitner. Some Ediacaran fossils have occasionally been related to free-living flatworms (Allison.. Peterson et al.

2003).. 1993). This considerably predates the oldest gener- ally accepted fossil evidence for parasitic flatworms. which parasitize vertebrates today and might have done in the past. some dating back to 9500 years BC according to Fry and Hall (1969). 2001. Littlewood and Donovan. Many studies on extant flatworms have focused on the hook elements of particular groups (Vignon and Sasal. 2011. 2014). derives from Dominican amber deposits (Waggoner and Poinar. but the fossil record indicates that other groups like pentastomids. a putative reinvestigation of these fossils could be used to constrain the evolutionary history of this entire group. Castellani et al. 2006). the oldest accepted record of Rotifera. 2003) have suggested that the Middle Devonian hook circlets might belong to a platyzoan helminth. This may suggest that parasitic flatworms evolved in basal gnathostomes (Littlewood. Consid- ering that multiple authors (Upeniece. 2010. 2010. 2001. (1994) for Cestoda. the free-living relatives of Acanthocephala. 3. . Waloszek et al. If we map the fossils of parasitic flatworms on their host phylogenies (Figure 4). Donoghue and Keating.. 2005. 2001). With the exception of highly derived taxa. 1996. 2003). The oldest confidently assigned Acanthocephala re- mains have been reported from archeological sites (Gonçalves et al.. which would lie somewhere around the Cambriane Ordovician based on the host fossil record (Friedman and Sallan.110 Kenneth De Baets et al. 1994. INTERPOLATING OR EXTRAPOLATING EXTANT PARASITEeHOST RELATIONSHIPS AND THE ASSUMPTION OF PARASITEeHOST COEVOLUTION Analysis of the range of current parasiteehost associations has often been used to infer the evolutionary origin of parasitic organisms (Littlewood and Donovan. Informa- tion and illustrations of these helminth structures can also be found in comprehensive systematic treatments: Yamaguti (1959). Iturralde-Vinent. 2006)... Maas and Waloszek. which is not the case for all parasites (Figure 5). 1994. Schmidt (1986) and Khalil et al. 2011) or taxa (Shinn et al. were already around at this time (Walossek and M€ uller. 2003). parasitic flatworms do not parasitize hagfishes or lampreys (Littlewood. Furthermore. Pentastomids mainly parasitize terrestrial vertebrates today (Christoffersen and De Assis. the rise of the Acanthocephala. 2012. Yamaguti (1963a) for Monogenea and Yamaguti (1963b) and Golvan (1969) for Acanthocephala. Walossek et al. 2011). Vignon. they are at least consistent with extant parasitic flatwormehost associations. which is now more confi- dently dated to the Miocene (Iturralde-Vinent and MacPhee. Sanders and Lee.

but in the CambrianeOrdovician (Walossek and M€ uller. Waloszek et al.. 2015). Walossek et al.... 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. but the Figure 5 Comparisons of the consistency between extant and fossil host ranges of parasitic flatworms and pentastomids. Recent discoveries of Silurian pentastomids associated with ostracods even further extend the host gap between fossil and extant pentasto- mids (Siveter et al.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 111 Figure 4 Fossil finds of putative flatworm fossils discussed in the text mapped on their host phylogeny. 2010). 2011). Host phylogeny was modified from Goudemand et al. . 2010. 1994. which was modified from Donoghue and Smith (2003) and Rowe (2004) taking into account new phylogenetic hypotheses summarized in Donoghue and Keating (2014). Turner et al.. (2011). they are found in marine deposits and there were no terrestrial vertebrates to serve as hosts at this time. Their morphology indicates a parasitic lifestyle. 2005. 1994. 2013). Castellani et al..

exact host of these marine forms is still unknown as they were not found directly associated with their hosts.. 2015). 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. Turner et al. This might suggest that in- vertebrates might have been the initial hosts in the marine realm. Dentzien-Dias et al. making it conceivable that these small pentastomids represent adults that spent their entire life cycle on small fish-like vertebrates (Sanders and Lee. 2010. 2011. Some have suggested their hosts might have been conodonts (Walossek and M€ uller. In the case of intermediate hosts. The range of the host gap between Cambrian and extant pentastomids (Figure 5) might therefore depend on the systematic position of conodonts. it might also be hard to identify the final host without finding remains of the putative parasite associated with them. Fossils of potential hosts might be common or present in the same layers. if ostracods are the final hosts as suggested by these authors and if no host switching occurred between the Cambrian and the Silurian. where the fossil evidence is often pathologies or traces. 2013. appointing a poten- tial host remains within the realm of speculation. although without direct evidence for a parasitic relationship (attached or found within well-preserved body fossils of their hosts). 2002). but also for parasite remains found in isolated coprolites not confidently assign- able to precise host taxa (Jouy-Avantin et al.. Donoghue and Keating. the CambrianeOrdovician fossil pentastomids resemble larvae of modern forms that can infest fish. Poinar and Boucot. Interestingly. putative pentastomid remains were recently also reported from ostracods within the Silurian Herefordshire Lagerst€atte (Siveter et al.or crown-vertebrates (Blieck et al. Predatoreprey relationships might provide a clue (Ruiz and Lindberg. it is hard to be certain of the identity of the culprits since various organisms with similar behaviour can produce similar traces. probably either stem.. which further increases the host gap between extant and fossil pentastomids.112 Kenneth De Baets et al. 2002. Walker and Brett. age in itself might .. 2010. Murdock et al. However.. of which tooth-like remains have been commonly found in these deposits. 2010). 2011).. which is still debated. but direct evidence for predation from one taxon on another is rare in the fossil record too (Brett and Walker. 1999. 2006. Furthermore. 2014). Nevertheless.. 1989. Thus. De Baets et al. 2013). 2011). Goudemand et al. pentasto- midehost associations from the Cambrian and Ordovician lagerst€atten would be necessary to further test this hypothesis.. Interestingly. Most authors agree that con- odonts are chordates. 1994).

1993. hosts assignable to taxa they currently parasitize were not around yet. Although the hosts of CambrianeOrdovician pentastomids remain speculative. 2010) used the parasitic flatworm fossil record as a calibration. Huyse and Volckaert. Thus. molecular clocks still need to be calibrated to obtain absolute age estimates... 2010.. Zietara et al. .. 1994.b. Light and Hafner. 1992.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. Hipsley and M€ uller. Most authors agree that the fossil speci- mens can only directly provide a well-justified minimum constraint for the origin of some particular lineages. Olson et al. 2009a.. which is not that straightforward among parasite groups with a patchy fossil record. Other studies have relied on molecular substitution rates derived from other studies (Despres et al. Page et al.. although it relied on the Upper Devonian and Carboniferous putative flatworm fossils.. they must have had different intermediate and/or final hosts at that time. 2014). Parham et al.. 2006). Badets et al.. However. 2012). a cophylogenetic approach has been used (Hafner et al. Only one study (Perkins. 2005).. Héritier et al. respectively. 2007). 2015). 2002. Benton et al. 2011. Waltari et al. 1998.. 2002. 2002. According to Parham et al. Due to the lack of well-preserved spec- imens in parasitic flatworms. 1995). 2011. is still debated (as discussed above). most molecular clock studies have relied on the host fossil record to inform divergence estimates (Verneau et al. 4. which may in turn pro- vide a robust evolutionary timescale for apparent cospeciating symbiotic species when the timescale of the host lineage is (comparably) well con- strained (Moran et al. 2010. Badets et al. 2007. so they must have had additional parasiteehost associations in the past which are now extinct. 2009.. More rarely biogeography (focusing on vicariance events) has been invoked to constrain molecular clock estimates of parasitic flatworms (Zietara and Lumme. 2007. The best practice for using fossils for molecular clock calibration has been discussed and reviewed extensively (Donoghue and Benton... 2014). (2012). Martínez-Aquino et al. which is even more problematic (Papadopoulou et al.. whose taxo- nomic assignment to Monogenea and Cestoda. MOLECULAR CLOCK STUDIES Molecular clock (timetree) methods for calibrating phylogenies have the potential to be useful to discriminate evolutionary scenarios in parasite evolution or hosteparasite associations (Hypsa.

as the substitution rate is var- iable and unknown. phylogenetic analysis that includes the specimen(s). (2) availability of apomorphy-based diagnoses of the specimen(s) or an explicit. 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. since the origin of parasitism falls outside the calibration interval a priori (Warnock et al. 2014).9 Ma) deposits might further narrow this . Warnock et al.4 Ma as discussed above)... which would be only Permian (>259. to constrain the evolutionary history of the host (and the parasite). This would yield quite large confidence intervals (cf. Alterna- tively. 2011 for this node) and the earliest certain appearance of parasitic flatworms in the fossil record.. For example. if the origin of parasitic flatworms occurred during the early evolution of gnathostomes as suggested by Littlewood (2006). and the oldest fossil assignable with confidence to the crown group (as the minimum). (3) explicit statements on the reconciliation of morphological and molecular data sets.114 Kenneth De Baets et al. Donoghue and Keating. 2012).7 Ma) or Middle Devonian (>381. 2011 for this node) and the earliest well-dated fossils that can be confidently assigned to crown-group gnathostomes deriving from Ordovician (w421. 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... 2012 for Parasitiformes). 2011). up-to-data. reinvestigation of putative flatworm trace or body fossils from Upper Silurian (>427. at least one point calibration or maximum constraint is required to calculate the substitution rate and absolute diver- gence times (Warnock et al. but such estimates would be more honest and accurate (closer to reality) than seemingly precise estimates which are argu- ably inaccurate. 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.. (5) reference to a published radioisotopic age and/or numeric timescale with details on its selection.8 Ma: Benton et al. Divergence time estimation is not possible with minimum constraints alone. 2009. Furthermore. therefore. this would mean they originated bet- ween the Cambrian (643 Ma: oldest confidence intervals of Erwin et al. (4) specification of the locality and stratigraphic level (to the best current knowledge) from which the calibrat- ing fossils are derived. 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.

2000) have suggested a younger.. 2013) and Trema- toda in archosaur hosts (Poinar and Boucot.. which is so far not contradicted by finds of older remains of S. Furthermore. multiple inaccu- rate calibrations might be consistent. which might indicate that schistosomes only colonized Africa around 15e20 Ma (Lawton et al. Diphyllobothrium. 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. And ujar 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. Fasciola. Dicrocoelium. 2012).. Furthermore.. 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. consistent calibrations may be . 2011). The fossil record also provides constraints on the origin of Cestoda in shark hosts (Dentzien-Dias et al. 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). Monoecocestus. a recent study by Mello et al.. More recent studies (Snyder and Loker.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 115 time interval in the future. 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. 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..g. The oldest fossil evidence for schistosomes are antigens deriving from a 3200 BC Egyptian mummy. 2003b). 2013) might also provide additional constraints in such studies. Direct dating of samples yielding ancient DNA (Wood et al. Most authors agree that multiple.. Parham et al. 2003). the fossil record provides upper constraints on the origin of Gymnophallidae in the form of characteristic pathologies. which can result in erroneous rejection of more reasonable calibrations. well-justified calibrations are the best approach to obtain the most robust and accurate molecular clock estimates (Warnock et al. 2011). ancestral Asian origin somewhere in the Miocene. Taenia). In some cases. dicrocoelid flatworms derived from eggs in coprolites as well as several genera and even species from archeological sites (e. In some cases. 2006). mansoni in archeological sites of South America (Gonçalves et al. 2014) as these only verify consistency (Clarke et al.. Schistosoma. 2011. However. 2005...

Biogeographic calibra- tions as they are currently implemented are problematic (Goswami and Upchurch. 2013) the continental break-up of superconti- nents. because older events might have led to similar distribu- tions (pseudo-congruence) or younger events might have altered their dis- tributions (pseudo-incongruence. Parham et al. Kodandaramaiah. Warnock et al. Even for some of the classical examples of groups with current distributions congruent with vicariance.. and introduce an aspects of circularity (Crisp et al. 2012. 2011.. It assumes that the current parasiteehost associations did not markedly change through geological time. 2014). but ultimately more accurate divergence estimates (Warnock et al. 2007. 2012) as discussed above. one could resort to the use of biogeographic events or calibrations related only to the host fossil record. 2012. Nevertheless. In highly host-specific lineages with simple life cycles like the .. see Donoghue and Moore. 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. Most importantly. 2014). calibration should be implemented in the most conservative way. Warnock. particularly in groups which are estimated to range several hundred million years into the past (e. 2012). making it harder to establish whether biogeographic barriers were coincident with speciation events. the pentastomid example we discussed above). Hipsley and M€ uller. De Baets and Donoghue. Using hosts also leads to circular reasoning when employing them to investigate hypotheses of parasiteehost coevolution. 2003). which might result in less precise.. respectively. 2011. 2014) or postdate (Friedman et al. redundant by definition. Having taxon-area relationships consistent or inconsistent with biogeographic events. which is not necessarily true.. 2014). and they should be implemented more con- servatively. actually occurred (De Baets and Donoghue. 2015). causal to a given speciation event. It should be established when a certain barrier. Furthermore. 2011). does not necessarily mean that these clades diversified at the same time as these events. Using the fossil record of hosts also introduces an aspect of circularity in addition to other considerations related with fossil calibrations (Donoghue and Benton. In the absence of a suitable fossil record. 2010.116 Kenneth De Baets et al.g. since they fail to correct for changes in rate varia- tion (Clarke et al. studies have demonstrated that divergence might predate (Murienne et al. such as onychophorans and cichlids.. there remains an assumption that biogeographic distri- butions have not changed significantly in geological time..

(2011) also suggested that some dates might be consistent with the break-up of the supercontinent Gondwana. Qiao and Zhu. 2007. 2013. Furthermore. 2009a. 2010) or host switching (Hafner and Page. Badets et al.b. which have been around for many hundreds of millions of years. 2009). have made them an ideal model to test the use of constraints from biogeog- raphy and the host fossil record (Bentz et al. although this event must have happened at the latest by about 419 Ma (Zhu et al. 2006... In the case of lineages or parasitee host associations. 2002. 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. 1995). The oldest stem-group lungfish is generally considered to be Diabolepis (Friedman. 2006. molecular studies with greater taxonomic coverage have particularly focused on biomedically or economically important taxa such as Schistosomatidae (Lockyer et al. 2015). 2001. 2009). Orélis-Ribeiro et al. Poinar and Boucot. Héritier et al. Verneau et al. 2013). making it hard to infer past biogeographical distribution or parasiteehost associations. 2011. 2003b. 2001. To better . host range changes and extinction might contribute significantly to missing taxa.. Taxon sampling can play a large role in tree reconstruction and interpre- tation with respect to biogeography (Trewick and Gibb. 2009). although this needs to be further tested with additional sampling. 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). 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). Badets et al. from extant data alone. but for groups with common host switches and/or complex life cycles this approach might be less suitable. 2006..Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 117 Polystomatidae (Figure 6).. However. 2011.. Verneau et al. Wood et al. Badets et al. 2001. 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. (2002) used 425 Ma to calibrate the split between Actinopterygii and Sarcopterygii (Figure 6)... 2014) or particular lineages with a high host specificity such as Polystomatidae (Bentz et al.. it might work well. while one of the oldest ingroup lungfishes might be Westollrhynchus (Qiao and Zhu.. 2011)..

(2001. The divergence between the European Polystoma species (i. nodes 1e3) were deduced from historical biogeographical scenarios suggested by Bentz et al. Eurasian and African Polystoma from their closest South and North American relatives (nodes 1 and 2) was constrained between 65 and 56 Myr. Figure 6 Ultrametric tree of neobatrachian polystomes inferred from MULTIDIVTIME (Modified after Verneau et al.).e. The divergence of the lineage associating Metapolystoma. 1992) and possible dispersal to Eurasia via Beringia. Polystoma gallieni) and the lineage grouping Metapolystoma and African Polystoma was constrained between 25 and 5 Myr. reflecting the . 2006) and Badets et al. (2009b). Calibration points (black rectangles. reflecting vertebrate exchanges between the two Americas in the Paleocene (Gayet et al..118 Kenneth De Baets et al. (2011).

estimates of the divergence time of lineages as well as external sources of evidence such as climate. 1988.. 2007.g. i. Nevertheless.. According to Verneau et al.. Bentz et al. although some could also belong to Acantho- cephala or more derived flatworms (Cestoda). focusing particularly on evolutionary important taxa which have putative fossil records (e. geography. Bromham. 1998) or within and between lineages of parasites and/ or hosts (Thomas et al. When no appropriate constraints are available.. hypothetically corresponding to a separation of the western and eastern components of Gondwanaland. 5.e. 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. it is essential to sample as many distinct lineages of parasites as possible as well as their free- living relatives. the root prior was set at 160 Ma (sd  5 Myr).. although the presence of = hypothesized ages of dispersal routes between Eurasia and Africa (Rage. some of which are most reminis- cent of extant Monogenea. 2014). 2012). 2010). Divergence time estimates (see Verneau et al. 2009).Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 119 understand the evolutionary history using molecular methods. Furthermore. CONCLUSIONS AND FUTURE PROSPECTS The earliest fossil evidence for the presence of helminths falls in the Middle Devonian in the form of hooks. Madapolystoma (see Du Preez et al. Gymnophallidae. (2009b). basal Monogenea. . novel prob- abilistic approaches make it possible to incorporate in biogeographic infer- ence. 2011). Finally.. Hibbett and Matheny. which can bias the results of such studies (Hipsley and M€ uller. corresponding to an initial divergence separating Asian and Australian polystomes from all other neobatra- chian polystomes (Badets et al. relative rates of uncali- brated molecular clocks can be used to test the support or reject the temporal congruence of parallel distributions or parasite-host evolution (Loader et al. 2009b) are reported for two nodes that are relevant for understand- ing the origin of the new Malagasy genus. it should be kept in mind when interpreting the results that the rate of molecular evolution might be significantly different between parasites and hosts (Page et al. 2010.. their fossil record or ecolog- ical tolerance (Sanmartín. 2012). Ces- toda) or reliable geological constraints derived from biogeography or the evolutionary history of their hosts. 2006. The oldest secure record of parasitic flatworms with complex parasite life cycles lies in the Permian which can be confidently assigned to cestodes. Loss-Oliveira et al. 2001).. 2009.

2003. chemical sample preparation. A comparative analysis of hook elements of acanthocephalans and parasitic flatworms (Monogenea.. 2013) and it could therefore be used to constrain the evolu- tionary origin of flatworms and other Platyzoa..55 Ma in the Middle Pleistocene. 2003) and Platyzoa in general (Conway Morris and Crompton. Various extant genera and species have been described from younger archeological sites (Gonçalves et al. 1992). 2011. would benefit from CT-scanning technologies to characterize their 3D- morphology and structure in a nondestructive way and potentially reveal additional details or fossils which otherwise might be destroyed by the sam- ple preparation process (e. 1982. igloo-shaped concretions reminiscent of those caused by gymnophallid trematodes in extant bivalves might already indicate the presence of derived parasitic flatworms with complex parasite life cycles in the Late Silurian (>428 Ma). Wey- Fabrizius et al. Furthermore. 2006). not consis- tent with evolutionary history of current gymnophallid hosts (shorebirds). Only rarely have studies been performed to assess the evolution of these structures over larger scales. which are believed to have appeared somewhere between the Cretaceous and Eocene. which can be confidently attributed to archosaurs (potentially theropod dinosaurs or crocodylians). Several putative flatworm fossils need additional study to confidently assign them to a certain lineage of flatworms including pla- tyzoan helminth hooks in Middle Devonian gnathostomes. Araujo et al. These Silurian occurrences are. The earliest evidence for dicroelid trematodes (Jouy-Avantin et al. see Malmberg (1990) for Monogenea. . thin-sectioning. Huntley and De Baets. Remarkably. however.g. Todd and Harper. Ces- toda) in a new molecular phylogenetic framework would therefore be in order to more confidently assign the fossil hook circlets to a certain clade or phylum. the study of eggs as well as hook circlets. The first evidence for terrestrial parasitic flatworms and trematodes was found in the form of eggs within a Lower Cretaceous coprolite (Poinar and Boucot. 1989. the fossil record of parasitic flatworms in considerably better than that of free-living flatworms (Poinar. which is a rather controversial study for different reasons (Gusev. 2015).. which is more or less consistent with the presence of their final host in the fossil record.120 Kenneth De Baets et al. e. resedimentation procedures). 2014). which is now largely done with destructive methods and in two dimensions.g. Characteristic pits in bivalves shells indicative for the presence of digenetic trematodes (Gymnophallidae) appear already in the Eocene (Ruiz and Lindberg. putative cestode eggs in a Carboniferous shark coprolite and eggs in a Cretaceous archosaur coprolite.. 1999) falls at about 0.

Novel methods like exper- imental decay studies or computer tomography might provide additional insights into the phylogeny. 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. 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.Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 121 Fossil evidence can only provide minimum time constraints and is not avail- able for all lineages of parasitic flatworms. 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. Steve Ross- coe (Hardin-Simmons University). 2013).. 2006. For calibrations based on the evolutionary history of parasites or their hosts. Upper Devonian. London) are thanked for pointing us to literature with the latest stratigraphic assignment of the Silurian. Riga). 2001. Carboniferous. for calibrations based on biogeographic events.. Poinar and Boucot. Cretaceous and Eocene flatworm fossils. Pascal Godefroit (Royal Belgian Institute of Natural Sci- ences. which can be characteristic for certain lineages. respectively. Brussels) and Jon Todd (Natural History Museum. 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. We therefore advise implementing such calibrations in the most conservative way. However. Characteristic pathologies might also put constraints on the evolutionary history of parasitic flatworm. Ervıns Luksevics (University of Latvia. Dentzien-Dias et al. 3D-morphology and ecology of such fossils. Jon Todd (Natural . ACKNOWLEDGEMENTS Michael Calner (Lund University). Interpolations based on parasiteehost associations or biogeographic events can potentially be used to supplement fos- sil constraints. circularity in testing hypotheses should be avoided and caution should be taken when multiple host-switching events are sus- pected. where the sampling and fossil record might be comparatively better. 2003. 1985. Ituarte et al. 2005). 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. particularly their attachment organs or their eggs (Littlewood and Donovan. Several recent discoveries indicate that exceptionally preserved gnathos- tomes or their coprolites might yield additional finds of parasitic flatworm fossils.

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1 General aspects 142 2.1016/bs.2015.2. Insect Parasitism s.1.3 Fossil representatives 160 Advances in Parasitology.1 General aspects 146 2.1 Neuroptera (Mantispidae) 159 4.str.2.2 Diptera 152 3.09.2.1.lmu.1. e Neuropteroida 159 4. Functional Morphology Group.) e Paraneoptera 142 2.1 General aspects 159 4. Insect Parasitism sensu stricto (s.2 Phylogenetic inference of appearance and molecular estimations of early 160 evolution 4.1.1 Phthiraptera 142 2.2 Insects in the fossil record 140 2.3 Fossil representatives 146 3.1 General aspects 148 3.doi. Introduction 139 1. e Antliophora 147 3.1. Planegg-Martinsried.2 Phylogenetic inference of appearance and molecular estimations of early 146 evolution 2. 137 . Volume 90 © 2015 Elsevier Ltd.1 Insects as parasites and hosts 139 1.2 Hemiptera 146 2.2 Phylogenetic inference of appearance and molecular estimations of early 153 evolution 3.apar.2. Haug1 Department of Biology II.2 Phylogenetic inference of appearance and molecular estimations of early 143 evolution 2.2. Germany 1 Corresponding author: E-mail: jhaug@bio.1 Siphonaptera 148 3.1 General aspects 152 3.3 Fossil representatives 149 3.3 Fossil representatives 145 2.1. Joachim T. CHAPTER FOUR From Fossil Parasitoids to Vectors: Insects as Parasites and Hosts Christina Nagler.2 Phylogenetic inference of appearance and molecular estimations of early 148 evolution 3.str.1. University of Munich (LMU). j ISSN 0065-308X http://dx.1.2.org/10. Insect Parasitism s.de Contents 1.003 All rights reserved.1. str.3 Fossil representatives 154 4.

2.2 Phylogenetic inference of appearance and molecular estimations of early 162 evolution 4.1 General aspects 175 7.1 Nematoida 174 7.3 Fossil representatives 173 7.3 Fossil representatives 175 7.3 Fossil representatives 179 8.3 Fossil representatives 171 6. Parasitoids 163 5.2 Phylogenetic inference of appearance and molecular estimations of early 174 evolution 7.1.2 Phylogenetic inference of appearance and molecular estimations of early 166 evolution 5.3 Fossil representatives 176 7.1 General aspects 172 6.2.2 Strepsiptera 169 5.2 Coleopterida (Coleoptera.2 Phylogenetic inference of appearance and molecular estimations of early 181 evolution 8.1 General aspects 177 7.1. Plant Parasitism (versus Phytophagy) 172 6.3.2 Mites 175 7.2.2.2. Conclusion 182 .3.1.3 Fossil representatives 162 5.2.2.1 General aspects 179 8.3 Fossil representatives 167 5.1 General aspects 163 5.3.1.1 Hymenoptera 163 5.3 Fossil representatives 182 9.3 Pseudoscorpions 177 7.1 General aspects 174 7.1 General aspects 169 5. Insects as Vectors 179 8.138 Christina Nagler and Joachim T.2 Phylogenetic inference of appearance and molecular estimations of early 178 evolution 7. Insects as Hosts 174 7.2 Phylogenetic inference of appearance and molecular estimations of early 176 evolution 7.2 Phylogenetic inference of appearance and molecular estimations of early 173 evolution 6.1. Meloidae) 161 4.1.2.2. Haug 4.2 Phylogenetic inference of appearance and molecular estimations of early 170 evolution 5.1 General aspects 161 4.

but also includes parasitoid. Considering that over 60% of all insect species have been proposed to be parasites (Price 1980). it has been estimated that only about 20% of all existing insect species have been described so far (Grimaldi and Engel. For a comprehensive view on fossil parasitic insects. 2005). it has been proposed that as many as two-thirds of all species are para- sitic. where several lineages independently evolved a parasitic lifestyle. we discuss here different aspects. 2005). Ectoparasitism and especially haematophagy occurs.1 Insects as parasites and hosts Insecta is often considered to be the largest animal group comprising over half of all metazoan species (Mayhew.Insects as Parasites and Hosts 139 10. at least in their larval stages. This propensity towards parasitism is also reflected within insects. functional morphology and a direct com- parison of fossil and extant species. . 2003). protistan. The fossil record can report this behaviour with direct (parasite associated with its host) or indirect evidence (insect with parasitic larva. isolated parasitic insect. 1. INTRODUCTION 1. Parasitoidism is an important feeding strategy for different wasps and relatives (Hymenoptera). such as mantid lacewings (Mantispidae) and blister bee- tles (Meloidae) are endoparasites or kleptoparasites. Ectoparasitism has been suggested to have evolved not less than 30 times in different insect groups (Grimaldi and Engel. Also. pathological changes of host).000 parasitic insect species in the modern fauna (although one could ask how reliable these estimations are). The high abundance of parasitism in the fossil record of insects can reveal important aspects of parasitic lifestyles in various evolutionary lin- eages. While parasites (in the strict sense) do not kill their host. Numerous insects are also the host for other parasitic insects or meta- zoans. including phylogenetic systematics. midges (Diptera). 2007). we could estimate that there should be at least 600. in fleas (Siphonaptera). Parasitic behaviour ranges from parasitic habits in the strict sense. Outlook 183 Acknowledgements 184 References 184 Abstract Within Metazoa. lice (Phthiraptera). Insects can also serve as vectors for numerous metazoan. some beetles (Coleoptera) and bugs (Hem- iptera) (Pe~ nalver and Pérez-de la Fuente 2014. parasitoids do (Kathirithamby. bacterial and viral diseases. phoretic or kleptopara- sitic behaviour. Other insects. for example. Lukashevich and Mostovki. 2009).

Often we also see parasitoids that have parasitoids as host. However. .. They also are hosts to a plethora of bacteria. 400 ma). 2002) and existed definitely since the Triassic (250 ma. Engel and Grimaldi. Parasitism in insects originated several times (Labandeira. Molecular estimations argue for an even earlier origin (e. 2005). see below). but many serve as hosts also for other insects. which occurs in several insect groups. based on possible insect coprolites (Labandeira.g. coleopterans. However. Definitive and more complete insect body fossils have been described from the Carboniferous (350 ma) and they already appear quite diversified at that time (e. Other putative Devonian insects tend to be rather fragmentary (e.g. 250 ma and many minor modern extant insect groups (‘families’) find their origins in the Cretaceous. a phenomenon known as hyperparasitoidism (Kathirithamby.. Misof et al. (2013) rejected this interpretation and interpreted it as ‘poorly preserved Devonian arthropod’ based on a reinvestigation of the specimen. ca. Haug but also for twisted-wing ‘parasites’ (Strepsiptera) and occasionally also for other insects. The oldest fossil evidence for arthropod parasitism in general is provided by pentastomids from the Cambrian (495 ma. The oldest body fossil that was interpreted as an insect is a single specimen of a supposed insect nymph from the Late Devonian. While parasites are usually significantly smaller than their hosts. 1990). 2014a). 120 ma (Grimaldi and Engel. 2012). another important parasitic mode (in the widest sense) is plant parasitism. Yet. hemipterans. Plasmodium and Dengue virus use insects as vectors. 2014).140 Christina Nagler and Joachim T.g. Besides parasitoidism. 2006 and references therein). to become widely distributed (e. nematode and nematomorph worms and mites. including Trypanosoma. H€ ornschemeyer et al. In contrast to most parasites. 2004. Many major modern in- sect groups make their appearance later in the Triassic. Finally. Shear and Kukalova-Peck. no definitive insect body fossil has been found that old. viruses and protists. insects do not only act as parasites themselves. 2011 and references therein). while pentastomids are arthropods they are not insects. 2009).. 425 ma (Garrouste et al. 1. the size relation of host and para- sitoid is oddly skewed. dipterans or hymenopterans.2 Insects in the fossil record The indirect fossil record of insects dates back to the Silurian.g. parasitoids reach about the same size as their host. Castellani et al. Many notable pathogens.. e. 420 million years ago (ma).g. Poinar.

In cases where we have no closely related extant form.g. the analysis of the contents of the digestive or circulatory system might also be informative. parasites without their hosts. 1999). parasitism sensu lato. preserves soft- bodied specimens as well as organisms with a cuticle. leaf mines and asymmetric growth. This includes. fossilized tree resin. Also here inference relies heavily on comparisons with extant parasiteehost reac- tions (e. More rarely. Sivinski et al. i. which allow parasitism to be inferred in the fossil record: 1. Typical examples are mites on insects. a functional morphological com- parison to modern parasitic forms can still be a strong indicator for a parasitic lifestyle e presumably because their morphology is known to be modified directly as a result of their parasitic lifestyle. Inclusions in amber are perfect examples of this kind of preservation (e. Due to the enormous diversity of insects. Parasitism is meant here in its broadest sense. Another type of indirect evidence is the influence on morphology. 1997) providing unique snapshots of life as it was millions of years ago. Furthermore. This is especially telling (but not only) in cases of plant parasitism indicated by galls. or nematodes emerging from an insect (see below). but we tried our best to cover all major fossil examples. for example. Amber. McNaughton. In the following. 2014a).e.Insects as Parasites and Hosts 141 Parasitized and parasitic insects are preserved as fossils in rocks and in numerous occasions in amber. Lewis and Grimaldi. Also quite direct is finding isolated parasites. This type of evidence relies heavily on comparison with modern forms. 1983). 3. to an exceptionally detailed degree (Pohl et al. 2003..g. applicable to many insect groups. Rozen. a fossil flea will be as parasitic as a modern one. However. a morphological comparison to extant relatives can give clues. 4.. Poinar. In such cases. 2010. we will not be able to cover every possible fossil example insects involved in parasitic re- lationships. . it can be difficult to identify the responsible organisms for these pathologies. We can roughly distinguish four different types of fossil. 2. we consider cases where insects are hosts or vectors for other organisms. The most direct cases are parasites directly associated with their hosts. is the finding of free-living developmental stages of a parasite.. parasitism sensu stricto (traditional type of parasite). we provide examples of fossil insect parasitism in various insect groups. growth and development of the host as a reaction to parasitism. More indirect evidence for parasitism. parasitoidism (host about the same size and is killed) plant parasitism (plant is ‘forced’ to help the insect) and kleptoparasitism (a parasite taking prey or other useful material from the host.

) e PARANEOPTERA Not all insect groups are known to have parasitic representatives. 2010. The females lay large eggs and atta- ch them to the hair or feathers of their host with a special secretion (Martill and Davis. They are traditionally split into two subgroups. Due to the dependence of their life cycle to the host and their host specificity. Beutel et al. Ischno- cera and Rhynchophthirina (Johnson and Clayton. 2003). INSECT PARASITISM SENSU STRICTO (S. both being again sister groups (Light et al. and Anoplura. there seem to be no unequivocal parasitic representa- tives of Entognatha. Hence active parasitism appears to be restricted to eumetabolan insects (Paraneoptera þ Holometabola). 2005). the sucking lice (Grimaldi and Engel.. Archaeognatha.. 2003). Active parasitism occurs in Phthiraptera. Psocodea or Psocoptera (if simply accepting that Phthiraptera are psocopter- ans) is sister group to Hemiptera plus Thysanoptera.. STR. Palaeodictyoptera or Polyneoptera. Haug 2. traditionally both have been placed together in the group Psocodea. All stages (including the adults) are wingless and dorsoventrally flattened. 2003). 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). They are a model system for phyloge- netic studies including co-speciation and coevolution (Wappler et al. Odonatoptera.g. the chewing lice.1 General aspects The group Phthiraptera. Phthiraptera is most likely an in-group of Psocoptera (e. Hemiptera and Thysanoptera. As far as we could find. . Johnson and Clayton. Paraneoptera includes the groups Phthiraptera (chewing lice and sucking lice). ‘Mallophaga’.142 Christina Nagler and Joachim T.. Johnson and Clayton. 2004.1. currently comprises 4900 extant species. They posses claws for clinging to hair or feathers and have modified mouthparts for feeding (Light et al. 2014). and also in some Hemiptera. They are extremely modified for their parasitic lifestyle and behaviourally adapted for particular microhabitats on the hosts (Johnson and Clayton. 2010). The chewing lice are named for their chewing mouthparts and include Amblycera. Ephemer- optera. All phthirapterans are obligate ectoparasites of birds or mammals. 1998). 2003). Zygentoma. which are obligate ectoparasites of birds and mam- mals. Psocoptera (book lice. or true lice. 2. bark lice). Phthiraptera is a candidate for being the most special- ized group of parasites among insects.1 Phthiraptera 2.

Cretoscelis burmitica (Figure 1(a)) from amber of Myanmar (Grimaldi and Engel. Anoplurans. Johnson and Clayton.. Their ancestors most likely had simple chewing mouthparts and were free living in the nests or burrows of vertebrates. where the host of lice could be an early mammal.Insects as Parasites and Hosts 143 After hatching. show a minimal age for the entire group Psocodea to be 135 ma (Early Creta- ceous. 2003). phthirapterans develop through three nymphal stages to the adult. About 2700 feed on birds and 380 on mammals (Yoshizawa and Lienhard. 2010). The mouthparts and the head of the 550 extant species are extremely modified and adapted to the mammalian host. bird. Recent findings of troctomorphs. the sucking lice.2 Phylogenetic inference of appearance and molecular estimations of early evolution Liposcelidae. They are the sister group to Anoplura and it is likely that Anoplura evolved from a Rhynchophthirina-like ancestor (Light et al. Rhynchophthirina includes only three species. 2006). but about 12% parasitize mammals such as rodents (Grimaldi and Engel. The lice feed on keratin in hair or feathers. 2003). They are obligate parasites mostly of birds. 2010. secretions or blood.. The group Ischnocera is the largest group of ‘Mallophaga’ with approx- imately 3080 species. traditionally classified as ‘Psocoptera’ or book lice are the sister group to Phthiraptera (Yoshizawa and Johnson 2010). Later in their evolutionary his- tory.1. provides an impor- tant calibration point for the appearance of true lice. They fed directly from their hosts and developed iteratively more modified mouthparts. dependent on where on the hosts they lived and their chosen diets (Light et al.. 2005. they parasitize elephants and wild pigs. the minimal divergence time of true lice and Liposcelidae is 100 ma. 2010). parasitize only mammals. Due to a discovery of a representative of Liposcelidae in mid-Cretaceous amber of Myanmar (about 100 ma). they apparently became more dependent on their hosts and adapted from associates to parasites. Azar et al. Amblycera (traditionally classified as ‘Mallophaga’) is the sister group to all remaining phthirapterans. 2. Grimaldi and Engel (2005) estimated the evolu- tionary appearance of lice to be around 145 ma. another in-group of Psocoptera. although not parasitic itself. another feathered theropod dinosaur or a haired . All of them possess an elongated ‘rostrum’ which bears the mandibles in a 180 angle from the ‘normal’ position to break through the skin and feed on blood. 2015a). Johnson and Clayton.

(b) Saurodectes vranskyi (modified from Grimaldi and Engel (2005. Psocodea) (modified from Mey (2005). Psocodea) (modified from Grimaldi and Engel (2006. (2004). (a) Cretoscelis burmitica (Liposcelidae. at least in the Early Cretaceous (Yoshizawa and Johnson 2003). Haug Figure 1 Fossil representatives of Psocodea (Paraneoptera). The appearance of Amblycera (the earliest offshoot of Phthiraptera) has been suggested to be around 120 ma. (c) Megamenopon rasnitsyni (Phthiraptera. with the ancestral host again being an early feathered dinosaur (Wappler et al. (2011) sup- ported the notion that the early hosts of lice were feathered theropod dino- saurs. Based on molecular dating techniques. Molecular data indicate a slightly older origin of lice. Smith et al. Figure 2) with kind permission of the Royal Society). Figure 38. 2004). pterosaur. Figure 1 with kind permission of Eberhard Mey). Figure 1(a) with kind permission of the Royal Society). Psocodea) (modified from the fossil pictured in Wappler et al.12) with kind permission of Cambridge University Press and David Grimaldi).. (d) Psittacobrosus bechsteini (Phthiraptera. which would be more or less .144 Christina Nagler and Joachim T.

2004). Yet. (2006) proposed that Saurodectes vrsanskyi is neither a phthirapteran nor could be assigned to any other insect ‘order’. The . 2010). 1998). Anoplura supposedly appeared in the Late Cretaceous (77 ma) and soon after the CretaceousePalaeogene boundary (before 65 ma). but Mey (2005) emphasized its importance and suggested a reinvestigation of the material.g. fossils of Phthiraptera are rare. Rasnitsyn and Zherikhin (1999) described Saurodectes vrsanskyi (Figure 1(b)) from the Zaza Formation of Baissa (130 ma). they radiated and adapted to different mammalian in-groups (Smith et al. (2004) considered this discovery has very little systematic value. 2005.1.Insects as Parasites and Hosts 145 congruent with the fossil record. Grimaldi and Engel (2005) stated that it is an ‘ectoparasite with phthirapteran affinities’ and later (Grimaldi and Engel.. it is likely also a mite. Representatives of Liposcelidae have been found in nests of birds. To date. 2004). shed fur and feathers (Grimaldi and Engel.3 Fossil representatives Due to the close connection between these ectoparasites and their hosts. its systematic attribution was based on an elimination process of other insect groups. Mey. 2. 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. 2001) was also described as a putative louse. Light et al. 2003). 2005.. 2010). Megamenopon rasnitsyni is 44 million years old from the Messel Lagerst€atte in Germany and resembles modern menoponid lice (Figure 1(c)). mammals or in the plumage of birds and fur of mammals. Wappler et al. Based on molecular data.. Martill and Davis.. Cuticular remains from the Triassic of Saptura Badin (215 ma) were described as a louse by Kumar and Kumar (2001). Wappler et al. 2006. but also an exceedingly bizarre insect’. Yet. Subsequent authors inter- preted these remains as that of an oribatid mite (Dalgleish et al. 2006). Mey (2005) followed this statement. 2006) as a ‘putative louse or close relative. six possible cases have been discovered: Voigt (1952) reported louse eggs on hair in Baltic amber. 2006. The single specimen of Amblyceropsis indica from the Triassic Bagra For- mation (Kumar. Mey. probably a representative of Prostigmata (Dalgleish et al. Grimaldi and Engel (2005) and Wappler et al. Dalgleish et al. Yet.. which has been recognized by various authors. This association may have given the input to a permanent parasitism in lice (Yoshizawa and Lienhard. 2011. feeding on faeces. and interpreted it as an ischnoceran louse.. also even earlier origins have been suggested (e.

The phthirapteran eggs should be reinvestigated to clarify their system- atic position. around 110e32 ma (Otalora-Luna et al.2.2. The exact relation- ship of the hemipteran subgroups is still under discussion (Beutel et al. rasnitsyni with its last meal in it. 2. Haug specimen is likely an ectoparasite of aquatic birds. Li et al. 2015). some species are commonly known as kissing bugs (Grimaldi and Engel.3 Fossil representatives There is one questionable compression fossil ascribed to Reduviidae from the Early Cretaceous (140e120 ma) and some reduviids were discovered in Burmese (Early Cretaceous). namely. 2. They have been considered to have evolved by means of a phytophagous strategy giving way to arthropod predation and finally becoming haematophagous. 2014). Sternorrhyncha (all four groups together formerly referred to as ‘Homoptera’) and Heteroptera (Beutel et al. The newest discovery was Psittacobrosus bechsteini by Mey (2005). It seems now extinct. 2012). contain also several haematophagous species (Yao et al.. but is not really a fossil (Figure 1(d)).. rasnitsyni and P.. 2014). 2012)..146 Christina Nagler and Joachim T. To conclude: only the last two specimens. A recent finding extends the record of haema- tophagous hemipterans to the Early Cretaceous (145 ma) (Yao et al.. Coleorrhyncha. Cicadomorpha (together forming Auchenorrhyncha). Phylogenetic analyses indicate that the origin of Hemiptera lies in the Late Permian (Li et al... 2005). A prominent haematophagous group within Hemiptera is Reduviidae.2 Phylogenetic inference of appearance and molecular estimations of early evolution Their high diversity is often explained as having diverged with the radiation of angiosperms coincident possibly with their phytophagous behaviour.2 Hemiptera 2. 2. There is hence only one direct phthirapteran fossil. 2012). 2014). of M. 2014. can be assigned to Phthiraptera without any doubts. The haematophagy should have evolved at least three times in these bugs (Ribeiro et al. M.. Two other groups. Cimicidae and Polyctenidae. Canadian (Late Cretaceous) and Dominican . as in the gut of this para- sitic louse remains of feathers have been found (Wappler et al.1 General aspects Hemiptera includes Fulgoromorpha. its host is a specimen of the bird Ara tricolor found in the 1980s. 2004).. bech- steini.2.

Larvae are generally scavengers and adults feed on nectar . and below). Active parasites (in the strict sense) are known in both of the latter groups. e ANTLIOPHORA The exact relationships within Holometabola have been in flux. traditionally considered to be the sister group of Mecoptera. These form two sister groups Neuropteroidea and Mecopteroidea (based on larval morphological characters and on molecular data. 2011). we might even speculate that the elongate mouthparts in the stem species of Mecopteroidea were already used for blood sucking and ectopar- asitism could represent an autapomorphy of Mecopteroidea. Beutel et al.. Antliophorans are characterized by an elongation of the mouthparts.Insects as Parasites and Hosts 147 (Miocene) amber (Poinar and Poinar. This appears to be part of their ground pattern. While most modern mecopterids feed on flowers. 2014. Siphonaptera (fleas). (2014).. ants and bees (Hymenoptera) are the sister group to all remaining holometabolans. this source of food was not yet readily available when the group diversified. Mecopterans feeding on flowers could then represent a novelty.. has been repeat- edly resolved as an in-group of Mecoptera (e. Diptera is the sister group to Mecoptera (Peters et al. birds or avian-rafted dinosaurs with the aid of geochemical data. Whiting. similar to evolutionary changes in Diptera (see below for details). 2002.STR. The ancestor of Mecopteroidea most likely existed in the Permian already. haematophagy is a ground pattern feature for dipterans and fleas. Yet. Within Antliophora. They provided evidence for haema- tophagy on mammals. Beutel et al. INSECT PARASITISM S. As will be outlined in detail below. 3. but also some mecopterids appear to have fed on blood.. Peters et al. The monophyletic group Mecopteroidea (Panorpida of some authors) consists of Mecoptera.. Hence. This might be seen as a possible preadaptation to a blood-sucking (haematophagous) type of ecto- parasitism. Wiegmann et al. 2009). 2005. 2014. 2011. Peters et al. Most mecopterans are insects with extremely elongated mouthparts and an elongate body.g. 2014). 1992).. Labandeira. the current (more or less stable) hypothesis suggests that wasps. 2014. Poinar. Remarkable fossil representatives from the Early Cretaceous in China (145 ma) have been described by Yao et al. Diptera (together Antliophora) and Trichoptera and Lepidoptera (together Amphiesmenoptera.

1 Siphonaptera 3. see below). wingless obligate ecto- parasites. 2012b. Whiting et al.. 2008) to the mecopteran in-group Boreidae. 2012. except fleas. 2003. It is still controversial as to which fossils are indeed all part of the early evolutionary history of fleas. reduced antennae. 2012. Vransky et al. They feed exclusively on the blood of mammals (94%) and birds (6%) (Poinar. Some fossils of the Late Jurassic (150e140 ma) indicate a Mesozoic age for the sister group to the fleas (Grimaldi and Engel. 2010. 3. 2002). are laterally compressed. others are predators or even can- nibals (Grimaldi and Engel. 2012b). The systematic and phylogenetic position of some Mesozoic fossils is still not settled (Gao et al. 2010).. Interest- ingly all insect ectoparasites have a dorsoventrally flattened body. 2005).1 General aspects Siphonaptera. Like many other insect parasites. Tungidae. Poinar. 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.. It has also been suggested that Siphonaptera is either an in-group (Friedrich and Beutel 2010) or the sister group (Whiting et al. Perrichot et al. 2013a. with its species retaining numerous plesiomorphic characters.. 2014. 2002). 2000). 2012b). where it is laterally compressed. 2012b).. large claws and modified mouthparts to pierce the skin of the host and suck blood (Lukashevich and Mostovki.148 Christina Nagler and Joachim T. Certain scorpionflies from the Early Cretaceous (100 ma) have long pointed mouthparts with fine serrations. the true fleas. 2005) and that this type of fossil scorpionflies may have led to Siphonaptera (Huang et al. 3. In contrast to lice.. no wings. Despite the fact the exact origin and relationships of fleas and other scorpionflies remains partly un- clear. Rasnitsyn and Quicke. Poinar. we can still state that with the radiation of mammals in the Palaeocene and the obligate ectoparasitism of fleas. Haug (Poinar. .2 Phylogenetic inference of appearance and molecular estimations of early evolution Based on molecular studies.1. Larvae often live in or near the nest of the host and feed on host faeces.1. Rasnitsyn and Quicke. this indicates that these early mecopterans fed on blood (Boucot and Poinar. 2008). Siphonaptera radiated far more recently than other mecopteran groups (Grimaldi and Engel. Siphonaptera is considered to be monophyletic. 1997.. 2005. likely represents the sister group to all other fleas (Beutel et al. fleas do not generally spend their whole life on the host. exfoliated skin. fleas have reduced eyes.

This large ecto- parasitic insect with long.. longipes to the ‘family’ Saurophthiridae (representing an empty. 2005.. Lukashevich and Mostovki. 2003). 2013). Some extant ectoparasitic bat flies show similar body proportions and legs (Grimaldi and Engel. Rasnitsyn and Quicke (2002) supposed S. 1976). 2012. 2012b). 2012). Mesozoic flea-like fossils indicate a possible diversifi- cation of Siphonaptera at least in the Late Jurassic (150 ma) (Gao et al. 2012. Poinar. incredibilis as possible sister group to Tar- winia and Saurophthirus (see next points). see below). recent morphological study indicates that Strashilidae are highly specialized dipterans (flies) (Huang et al. Poinar. These species found in amber indicate the evolution for modern species-groups in the Middle Caenozoic (Perrichot et al. • Saurophthirus longipes (Figure 2(e)) from the Early Cretaceous Zaza For- mation of Baissa. 2005). • Extinct adult fossil specimens of Siphonaptera (Figure 2(b)) ascribed to extant genera have been found in Eocene Baltic amber and in Miocene Dominican amber (40e50 ma) (Perrichot et al. 1992)..Insects as Parasites and Hosts 149 Flea-like ancestors have been considered to have shifted step by step from pterosaurs to mammalian hosts (Gao et al. but is thought to have been unable to walk on the ground... 2012. Gao et al. 2012). 1986).3 Fossil representatives Due to the close connection between siphonapterans and their hosts. (2013a) assigned S. 2012b.. Lukashevich and Mostovski. 2003. Huang et al.. However. which would indi- cate a permanent life on the host (Grimaldi and Engel. 2012. fleas are rare in the fossil record just like lice (Lukashevich and Mostovki. central Siberia (Ponomarenko. While such clear in-group fossils are easy to recognize as such. 2013a. 3. These are thought (by Grimaldi and Engel.. 2003). 2005) to be ‘the early close relative of fleas from the . useless bracket) and supposed it to represent the closest relative to modern fleas. Lewis and Grimaldi. there are also some more challenging Mesozoic findings: • Strashila incredibilis (Figure 2(f )) from the Jurassic of Transbaikalia in East Siberia (Rasnitsyn.1. Rasnitsyn and Quicke (2002) pro- posed Saurophthirus as sister group to Tarwinia and true fleas. 1997). slender legs closely resembles certain Mesozoic giant fleas (Huang et al. • A specimen of Tarwinia australis (Figure 2(c)) and three other (similar appearing) specimens from the Early Cretaceous Koonwarra sediments of Victoria (Jell and Duncan. slender legs to grasp its host. Huang et al. It has long.

Mecopterida) (modified from Rasnitsyn (1992. Huang. Mecopterida) (modified from Perrichot et al. (2014. Mecoptera) (modified from Grimaldi and Engel (2005. (2012. Siphonaptera) (modified with permission from Macmillan Publishers Ltd from Huang et al. Siphonaptera) (modified from Rasnitsyn (1992. T. Haug Figure 2 Fossil representatives of Mecopterida (Mecopteroidea). (e) Saurophthirus longipes (Sauroph- thiridae. . (Pseudopulicidae.150 Christina Nagler and Joachim T. (b) Eospilopsyllus kob- berti (Siphonaptera. 2015). Figure 2(a))). (a) Mosquito-like scor- pionfly (Boreidae. (d) Pseudopu- licidae sp. Figure 2) with kind permission of Alexander Rasnitsyn).3) with kind permission of Cambridge University Press and David Grimaldi). (c) Tarwinia australis (Siphonaptera. (2012. Figure 12. (f) Strashila incredibilis (Siphonaptera. Mecopterida) (modified with permission from Elsevier from Huang et al. Pseudopulicidae (see below. Mesozoic’. and has some particular features that are closely related to another Mesozoic giant flea group. After a current reinterpretation of the holotype. Figure 4)). australis is a definitive early representative of the lineage to Siphonaptera. Figure 5) with kind permission of Alexander Rasnitsyn). Figure 1) with kind permission of Magnolia Press).

These specimens share some morphological characters with extant fleas. These specimens share morphological characters with extant fleas.. • Saurophthiridae. Jell and Duncan. 1986). The morphological data indicate that Pseudopulicidae (including these two) represent an early offshoot of the siphonapteran lineage (Gao et al.. 1976.. we can state that early representatives of Siphonaptera sensu lato (before the node of Siphonapetra sensu stricto) were likely parasitizing feathered dinosaurs. but are more likely early offshoots of the evolutionary line- age towards them (some may also represent other groups. 2012). but may be because at the point of their review the only known Saurophthirus was S. assuming this is not a plesiomorphic feature. This indicates a divergence of Saurophthiridae and true fleas in the Late Jurassic (Gao et al. Their habitus indicates a strict ectoparasitic lifestyle. but retain plesiomorphic features like nonjumping hind legs. Rasnitsyn. However. Also they have similar mouthparts in siphonate mecopterids. With Saurophthirus exquisitus from the Lower Creta- ceous Yixian Formation in China et al. where the mouthparts were not preserved. These giant fleas might document an early diversification towards haematophagy (Huang et al. Hence Sau- rophthiridae (including another species S. All flea-like Mesozoic fossils are definitely not true fleas in the strict sense (Poinar.Insects as Parasites and Hosts 151 • 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. This species has short and slender piercingesucking stylet mouthparts. 2013) • Pseudopulex jurassicus from the Middle Jurassic and Pseudopulex magnus from the Early Cretaceous (Gao et al. 2012). 2013a). 2013a). pterosaurs or early mammals as ecto- parasites grasping with their long legs (Gao et al.. Hence. longipes see above) resembles the true fleas more than any other Mesozoic flea or flea-like fossil. Subsequently Gao et al. Ponomarenko.. One could simply consider modern fleas (including most amber fossils) as Siphon- aptera sensu stricto. instead of discussing at which point the term ‘flea’ should be applied. but could represent an extinct lineage in early flea evolution (Gao et al. 2012). All three spe- cies were ascribed subsequently to Pseudopulicidae (see below. while using Siphonaptera sensu lato for the Mesozoic flea- like fossils plus Siphonaptera s. longipes.. Grimaldi and Engel (2005) saw no features that indicate special relationships to true fleas. 2012b).str... 2013a. adapted more for attachment than jumping (as in . Huang et al. (2013a) suggested Tarwinia þ Pseudopulicidae as sister group to Saurophthirus þ the modern fleas based on morphological characters. 1992. see above).. (Gao et al. 2012).

1 General aspects The superdiverse insect group Diptera is cosmopolitan and with 154.. but early representatives of Chironomidae from the Triassic and Jurassic were still haematophagous.. 3. 2010).2. Female frog-biting midges find their hosts by listening to the mating calls of the host frogs (De Silva and Bernal. Ceratopogonidae. Extant representatives of Culicidae are blood suckers of almost all verte- brates. Huang et al. They could have either pierced through scales or fed on the skin between the scales on nonfeathered dinosaurs (Poinar. Extant adults of Chironomidae feed on nectar and honeydew.. Haug modern forms). Azar and Nel. Species of Corethrellidae are known as frog-biting midges. 2014. Haematophagous groups within the Diptera are numerous: Phlebotominae. like midges and craneflies. The early representatives of Siphonaptera sensu lato appear not to have entangled themselves in hair or feathers. Ceratopogonidae is very species rich. with 6180 extant species (Borkent. resemble mecopterans in basic morphology. Females of groups which retain this mode have mandibles. Haematophagy is obligate for females (of blood-sucking species) to complete each gonadotrophic cycle and produce fertile eggs (Greenwalt et al. dangling legs.. with their long wings and long. Simuliidae. while more derived species feed on insects as ectoparasites (Borkent et al. Greenwalt et al. 2012). 2005). but also nonavian dinosaurs (Poinar et al.000 described species represents 10e12% of all described animal species (Lambkin et al. 2012. crocodilians. Early divergent representatives of Diptera. 2005). These tiny midges are host-specific and parasitize frogs. 2013).2 Diptera 3. 2000). Sycorinae. 2013a. Pérez-de la Fuente et al.. 105 extant and 7 fossil species are known (Borkent. 2012. 2013). 2011). which function as lancets (Grimaldi and Engel. snakes. 2012b) or they could have parasitized the membrane of the wings of pterosaurs (Gao et al. Tabanidae. lizards. Hence. like Aenne triassica from the Late Triassic of England (210 ma. 2013). Vransky et al. likely fossil hosts could have been early mammals. 2013). Muscidae and Glossinidae (Grimaldi and Engel.. Culici- dae... Rhagionidae. 2013. .152 Christina Nagler and Joachim T. Corethrellidae. 2014). Representatives of older lineages feed on vertebrates.. but have well-developed wings. Dipterans are easily recognizable as their hind wings are reduced to halteres. Representatives of Ceratopogonidae or biting midges are small. turtles. The ancestral feeding mode for Diptera is blood-sucking. Carnidae. Such forms had biting mandibles.

Psychodidae with about 3000 extant species has received special scienti- fic attention due to their medical significance. necrophagy.and nectar-feeding at the same time (Karoyli et al. 3. 2012). coprophagy. 2010).2 Phylogenetic inference of appearance and molecular estimations of early evolution Dipterans are thought to have evolved in the latest Permian to the earliest Triassic. Tabanidae) radiated and new dipteran larval types evolved. while parasitic forms evolved de novo from this strategy (Grimaldi and Engel. Cyclorrhapha and Schizophora. Hence while blood sucking and haematophagy seem to be the ancient diet of dipterans.. In the Early Cretaceous (145 ma).Insects as Parasites and Hosts 153 Simuliidae or blackflies are a group with 2100 extant species (Craig et al. leaf mining and different types of parasitism (Grimaldi and Engel.. when other insect lineages became extinct. In this period. Wiegmann et al. Hence brachycerans became one of the most dominant insect groups. the more derived brachyceran in-groups.. radiated (Lambkin et al.2. this type of diet must have been lost (but also regained) independently several times. 2010). which is thought to have evolved a predatory lifestyle. Rasnitsyn and Quicke. mammals or amphibians. 2005. Most often it was displaced by nectar feeding . dipteran in-groups evolved all kind of new diets: phytophagy. representatives of Sycorinae and Phlebotominae are parasitic blood feeders (Grimaldi and Engel. 2002). 2005)... 2012). An exception might be Rhagionidae. These larvae lived in soil. Within Psychodidae. The elongate mouthparts of the 4500 species of Tabanidae (Zhang. larval or adult predators. 2009). plesiomorphic are parasitic while derived forms have abandoned this strat- egy. 2012) are well suited for blood. 2000). Reidenbach et al. 2013. 2011. 247 ma. The claws of fossil forms indicate that early representatives of Simuliidae fed on feathered nonavian dinosaurs or early birds (Currie and Grimaldi. Species of Rhagionidae are known as water snipe flies and are a relatively small group with about 500 extant species (Zhang.g. likely due to the drying of aquatic and semiaquatic habitats. After the TriassiceJurassic mass extinction event (about 200 ma). mainly species of Symphoromyia (Zhang. 2014) and they have been considered to be the first pollinators of early angiosperms (Labandeira. About 50 extant species are parasitic on birds. In other groups. 2005). 2012). The parasitic groups Tabanidae and Rhagionidae are in-groups of Tabanomorpha (Kerr. early brachycerans (e.

3 Fossil representatives Dipteran fossils are numerous especially in amber.. 2013. 2014. 2012)... Borkent et al. A number of examples include the following: • The oldest representative of Diptera has been considered to be Grauvogelia arzvilleriana from the Middle Triassic Voltzia-Buntsandstein (240 ma) (Gall . It is supposed that the first ‘non-mandibulate’ forms occurred after the Lower Cretaceous (Azar and Nel. 2012). 3. Psychodidae has been thought to have evolved by the Triassic (248 ma) before the breakup of Pangaea (Andrade Filho et al.. Chou- fani et al. 2012). 2007. Pérez-de la Fuente et al. 2013. 2014). 2011). 2012. 2009.. Wiegmann et al. The protozoan Leishmania is supposed to have coevolved with psy- chodidans (Andrade Filho and Brazil. 2013.. 2003).2. Haug multiple times during the radiation of angiosperms in the Lower Cretaceous (Choufani et al. Culicidae (mosquitoes) should have evolved during the Middle Jurassic. 2014). 2011). Zhang. 2013).. 2012. 2003). Greenwalt et al.. Modern dipterans do not use their mandibles to chew. This interpretation is more or less congruent with a recent molecular study (Wiegmann et al. Tabanomorph-like forms are thought to be the oldest representatives of Brachycera and radiated probably 200 ma (Lambkin et al. Still all these inferences are dependent on certain relation- ship assumptions and the exact relationships within Diptera are still not satis- fyingly clarified (Beutel et al. 2013). 2009).. 2013. Fossils ascribed to Simuliidae (176 ma) and Thaumaleidae (146 ma) indicate that biting midges (Ceratopogonidae) should have evolved at the latest in the Late Jurassic (Beutel et al. 2011). based on molecular data. 300e200 ma (Harbach and Greenwalt. Borkent et al.. 2003). Ceratopogonidae þ Chironomidae is the sister group to Simuliidae þ Thaumaleidae.. Krenn and Asp€ ock. due to the less patchy geographic distribution of culicids they have been considered to have existed before the separation of Pangaea.and pollen-eating form. Azar and Nel. 191 ma (Reidenbach et al. Yet. 2013. Tabanidae (Figure 3(a)) are considered to have evolved quite recently in the Early and Middle Cretaceous (Beutel et al. Culicomorpha with Nymphomyiidae.. The earliest direct fossil evidence comes from the Lebanese amber (122 ma...154 Christina Nagler and Joachim T. It is likely that psychodidans evolved from a blood-sucking form parasitic on nonavian dinosaurs or ptero- saurs gradually to a nectar. Culicoidea and Chironomoidea are thought to represent early radiations (Lambkin et al. Azar and Nel.. since only the old lineages Sycoracinae and Phlebotominae are still parasitic (Azar and Nel.

(a) Laiyangitabanus formosus (Tabanidae.4 mm. Mantispidae (Neuroptera. (2002. (2008. Mantispidae) larva (modified from Ohl (2011. Diptera) (modified with permission from Elsevier from Zhang (2012. . Neuroptera) (modified from Engel and Grimaldi (2007. Coleopterida) (f). Figure 2(a))). Diptera) (modified from Grimaldi et al. Neuroptera) (modified with permission from Elsevier from Shih et al. (f) Epispasta abbreviata (Meloidae. (e) Mantispa styriaca (Mantispinae. Figure 1(f))). (d) Micromantispa cristata (Mantispidae. (c) Dicromantispa electromexicana (Mantispidae. (b) Burmaculex antiquus (Culicidae. Meloidae (Coleoptera. Figure 5) with kind permission of the American Museum of Natural History). Coleoptera) larva (modified with permission from Elsevier from Bologna et al. Figure 5(a))). Figure 36(b)) with kind permission of the American Museum of Natural History). (2015.Insects as Parasites and Hosts 155 Figure 3 Fossil representatives of Diptera (Mecopteroidea) (a and b). Neuropteroida) (c and e). Figure 2(b)) with kind permission from Springer Science and Business Media). Body length 10.

This statement has not been further supported. very high level of iron in the abdomen of the midge could be detected (Greenwalt et al. • One of the most spectacular findings is a modern-type mosquito. 1974... 2004). Veltz et al. 1985. Due to their abun- dance in lake sediments and their swarm behaviour. dipterans in general are very frequent in the fossil record (Grimaldi and Engel. (2002) stated that the gut of this specimen contains granular material. 2002. 2014. 2000. 2002). most fossil mosquitoes are preserved in lake or other lacustrine sediments (Briggs. 1996.. while the younger forms were most likely already feeding on nectar and other flower products. Kalugina. 2012. Azar and Nel. 2010. Due to their larvae. • Only slightly younger is the fossil of a nematoceran (mosquito-like form) in 230 ma Triassic amber from Italy (Schmidt et al. 1976. from the Kishenehn shale in Montana (46 ma). 2007. Azar et al. This is based on the reten- tion of several plesiomorphic characters that show an intermediate condition between modern mosquitoes and other midges (Harbach and Greenwalt. Jarzembowski et al. we might assume a similar mode of life for this species. Grimaldi et al. which have an obligate connection to water. 2008. 14 are preserved as compression or impression fossils (Hulden and Hulden. • Culicidae (mosquitoes) is represented in the fossil record by at least 25 species.. Poinar et al. 2015. 2013). 11 are known in amber. Grimaldi et al. only Triassic and Jurassic forms appear to have been haematophagous...156 Christina Nagler and Joachim T. Briggs. 1966). 1980. • Specimens of dipterans are the most common and most diverse forms in amber inclusions. With the aid of time- of-flight secondary ion mass spectrometry. 2013).. Yet. 2008. possibly representing a blood meal. 1993). Haug and Grauvogel. 2012). • Fossil chironomids are abundant not only as inclusions in amber but also as impressions from the Triassic to the Cretaceous (Lukashevich and Przhiboro. Grimaldi et al.. Borkent and Grimaldi.. 2013). in Spanish amber dipterans are in 38% of all biological inclusions (Delclos et al. This was interpreted as a fossilized blood meal providing a direct evidence for haematophagy in fossil representatives of Culicidae. Culiseta sp. The oldest fossil mosquito Burmaculex antiquus (Figure 3(b)) from Burmese amber (100 ma) has been proposed to repre- sent the sister group to all remaining culicids. Greenwalt et al. 2005). 2012. Some Eocene fossils have been ascribed to modern mosquito species (Harbach and Greenwalt. 2007. Kalugina and Kovalev. Ansorge. 2013). The fossils range from the Middle Cretaceous to the Oligocene. ... As haematophagy is thought to be ancestral for Diptera.

• Representatives of Psychodidae are diverse and abundant in the fossil record with 74 species (Azar and Nel. 2013. Andrade Filho et al. Choufani et al. The oldest specimen ascribed to Leptoconops... Compression fossils of biting mites are rare.. 1996. Psychodidans occur in Lower Cretaceous Burmese. Poinar.. 2004. This was used as an indication of morphological stability in Ceratopogonidae for million of years. Andrade Filho and Brazil.. Borkent. Amber specimens have been recorded from Lebanese amber (122 ma) to Dominican amber (15 ma. 2008). The oldest compression fossil is Archiaustroconops besti of Southern England from the Purbeck Limestone group (146 ma). 2008. was found in Lebanese amber (122 ma) (Borkent et al... Andrade Filho et al. Lebanese. 2011. Choufani et al. Azar et al. 2003. 2009. 2011).. which has been related to a lack of change in diet of Cerato- pogonidae during the radiation of the angiosperms (Borkent and Craig. 2015. 2002. 2015b.. 2013). 2013).. France and Spain amber (120e 135 ma) to Miocene Mexican and Dominican amber. (2) their small size and (3) their swarming behaviour (Szadziewski et al... Borkent. Blagoderov et al. 2005). 1995. 2003). and hence a presumed representative of Leba- noculicoidinae (sister group to all other Ceratopogonidae). 2005. 2011). • Archicnephia ornithoraptor from the Cretaceous amber (90 ma) of New Jer- sey is the only amber inclusion of a representative of Simuliidae known so far (Grimaldi and Engel. 2007. • The fossil record of Ceratopogonidae is one of the best known among insects with 274 fossil species (Borkent.. The oldest definitive representatives of Simuliidae are Kovalevimyia lacrimosa from the Late Jurassic of Siberia (176 ma) and a Simulimima grandis pupa from the Middle Jurassic of Siberia (Currie and Grimaldi. Ibanez-Bernal et al. This abundance is connected to (1) the close association of their habitats and resin sour- ces. Andrade Filho et al. 2014) and with countless spec- imens in all 15 major amber deposits currently known. Petrulevicius et al. 2007. 2000). 2007. Azar and Nel. Grimaldi and Engel. 2015. Pérez-de la Fuente et al. rep- resenting a single wing (Borkent et al.. 2000. Brazil and Andrade Filho. 2003. Leptoconops also has extant representatives. . 122 ma from Lower Cretaceous Lebanese amber (Szadziewski. Sontag and Szadziewski. 2000). Borkent.. 2014.Insects as Parasites and Hosts 157 • The oldest representative of Corethrellidae is Corethrella cretacea. Ansorge. 2001. 2014. but also in the Early Jurassic of Germany (180 ma) and in the Late Triassic of Virginia (210 ma. Fraser et al. Szadziewski et al.

. Petrulevicius et al.. to a predatory or nectar-feeding life- style.. Krzeminski and Krzeminska. Penalver and Grimaldi (2005) reported a swarm of specimens of Phlebotominae associated with mammalian hair from the Miocene Dominican amber. 2002) and the Cretaceous New Jersey amber (Grimaldi et al. 2011). Gallia alsatica. 2014). 2013) from Dominican amber. 2004a). The more spectacular one is the observation of nucleated erythrocytes with parasi- tophorous vacuoles in the gut of an amber-embedded sand fly (Poinar and Poinar. Baltic amber (Trojan.. 2013). Summing up. 2003).. which indicate that snipe flies were in fact still abundant and widespread (Solorzano Kraemer and Nel. 2011b. they are a well-represented group in fossil deposits. occurred first in Cretaceous amber of France and New Jersey (Azar and Salame. Snipe flies have been considered to be abundant during the Jurassic and declined during the Cretaceous (Mostovski. A recent finding from China. 2008). 2013.b. Haug 1994). Yet this behaviour is quite scattered . 2004a. 2003) and America (Grimaldi et al. 2010.. Two discoveries give direct evi- dence for the haematophagy of Psychodidae. 2012).. 2011) with 28 species (Strelow et al. 2007). 2011. numerous Cretaceous fos- sils have been found. Within the brachyceran lineages of Diptera several groups evolved parasitoidism. The oldest representatives of Tabanidae are impression fossils from the Lower Cretaceous of China (Zhang. Qiyia jurassica. However. Poinar and Poinar. 80 species have been described (Solorzano Kraemer and Nel. Their evolutionary history shows a gradual evolution from ancestral blood-feeding. an aquatic parasitic fly larva from the Jurassic (150 ma) could be a representative of the early lineage of Tabanomorpha and would support their supposedly Jurassic age (Chen et al. one of the oldest fossils among snipe flies. Azar. Strelow et al. 2005) give also more evidence for their parasitic lifestyle and func- tion as vectors in the past. Poinar. 2007. Penalver and Grimaldi. hence ectoparasitism. • Horse flies (an in-group of Tabanomorpha) have been reported from Miocene Mexican amber (20 ma.. 2005a. first representatives of Diptera are as old as the Triassic. comes from the Jurassic of France (200 ma. sometimes also with reversal to blood sucking. 2009). a more derived psychodid in-group. 2009). • Due to the close connection between the water snipe flies (Tabanomor- pha) and trees. Europe (Mostovski et al.158 Christina Nagler and Joachim T. Sycoracinae. 2005. 2004a) and two asso- ciations with the remains of their host (Vullo et al. 2015. Several indications of haematophagy (Greenwalt et al. Poinar and Telford..

They are distinct by a mantodean-like appearance e they have prominent raptorial forelegs. elon- gated ‘necks’ and well-developed eyes (Grimaldi and Engel. the parent group named Neuropteroida (Beutel et al.1 Neuroptera (Mantispidae) Within Neuroptera.Insects as Parasites and Hosts 159 (phylogenetically) and not associated with functional morphological special- izations. Hence identifying this behaviour in a fossil is more than challenging and therefore not further followed here. Neuroptera has been considered to have originated in the Permian (Grimaldi and Engel. The first instar larva is active and very mobile. Wiegmann et al. there are approximately 6000 described species (Beutel et al. Larvae of Mantispinae are obligate parasites of spiders’ egg sacs. 2007). 4.and morphologically based phyloge- netic analyses indicate that Coleopterida and Neuropterida are sister groups.. e NEUROPTEROIDA Comparably recent molecular. 2011). Calomantispinae. 2005). 2007). 2009).1. Wiegmann et al. Engel and Grimaldi. Thus. 2008) and its sister group Raphidioptera (Beutel et al. Mantispinae and Symphrasinae. Some larvae are ectoparasitic on spiders. when the spider will become adult and produce an egg sac. 2014). whereas the next two stages are immobile. the host spider induces and terminates a diapause of the mantispid larvae (Ohl. 4. to find and reach a spider’s egg sac.. 2014. 2011. The . 2005). 2011. Hence they feed on haemolymph until they finally can parasitize the egg sac and feed on the eggs (Ohl. the larva remains within the chambers of the book lungs of the spider until the next year. The only known parasitic in-group of Neuroptera is Mantispidae.. There are generally four in-groups recognized: Drepanicinae. before these produce an egg sac. If a mantispid larva attaches to a juvenile spider. INSECT PARASITISM S. Neuropterida consists of Neuroptera þ Megaloptera (Asp€ ock and Asp€ ock. 4.STR.. All larvae are all highly specialized obligate parasites of spiders or hymenopterans (Grimaldi and Engel. 2005). 2009). most larvae of Mantispinae are parasitic on spider eggs.1 General aspects Mantispidae (mantid lacewings) is a group within Neuroptera with 400 species known globally (Engel and Grimaldi. It is necessary that the larvae are agile..

Five of them were found in amber: Micromantispa cristata (Figure 3(d)) in Cretaceous amber of Myanmar (Shih et al. elongated body and bears strong thoracic legs. the Eocene (Wedmann and Makarkin.2 Phylogenetic inference of appearance and molecular estimations of early evolution Grimaldi and Engel (2005) suggested a radiation within Mantispinae during the Palaeogene (60 ma) hence a rather young age. anterior on the opisthosoma (Figure 3(e)). Feroseta prisca in Dominican amber (Poinar. 2011). Also adult forms provide evidence since the Early Cretaceous (Shih et al. Haug larva of the fossil Dicromantispa moronei has been proposed as a parasitoid of spiders. 2007. 2007. Hence also Mantispidae is at least that old. Ansorge and Schl€ uter. 2011). 4. moronei in Dominican amber (Engel and Grimaldi. 2007). Makarkin. Wedmann and Makarkin. 2015.. This morphology indicates that it is likely the first instar larva of a species of Mantispinae. Two additional fossils ascribed to Mantispidae are two species of Mantis- pidiptera. Poinar and Buckley. 2007. Dicromantispa electromexicana in Mexican amber (Engel and Grimaldi.. 2007). A fossil larva in amber found by Ohl (2011) (see below) is the first direct fossil record of a parasitic larva of Mantispinae and provides their minimum age (Eocene. Doratomantispa burmanica in Burmese amber (Poinar and Buckley. Cockerell. the Cretaceous (Makakrin. • Adult mantispidans. which would indirectly indicate the presence of parasitic larvae. 2015). Two fossil species ascribed to Drepanicinae demonstrate an appear- ance of these at least in the Late Cretaceous (100e66 ma. 1921) and the Oligocene (Nel. 1980). 1990). This represents the first and so far only discovery of a fossil mantispid larva (Ohl. The larva has a flattened. 2007). 2015). described by Grimaldi (2000) and Whalfera venatrix. 4. 1988). that imply active movement of the larva.1. 2006).3 Fossil representatives • Ohl (2011) found one spider-boarding larva ascribed to Mantispinae in Middle Eocene Baltic amber (44 ma) on a juvenile clubionid spider in a typical position. • The others were found in deposits dating from the Jurassic (Wedmann and Makarkin. are rare in the fossil record (Engel and Grimaldi. 2011). Shi et al. 1990.1. Haring and Asp€ ock (2004) predicted an origin in the Late Triassic (202 ma) or the Early Jurassic (200 ma) based on molecular data. described by . 2007). Only 14 species have been ascribed to Mantispidae.. 44 ma). 1996.160 Christina Nagler and Joachim T. Panfilov. D. yet without further explanation (Engel and Grimaldi.

.000 extant species and 600 fossil species of Coleoptera have been described (Grimaldi and Engel. the large coleopteran in-groups Myxophaga and Adephaga radiated. 2014). 2008).2. A dramatic increase in species richness occurred in the Late Creta- ceous. 2014).. This interpretation has been questioned by Kukalova-Peck and Beutel (2012). when we look on parasitism (Grimaldi and Engel. 2014). 4. also first representatives of Polyphaga appeared (Beutel et al. 2008. Bethoux (2009) interpreted the Carboniferous fossil Adiphlebia lacoana as a possible early coleopteran implying an older age of the coleopteran lineage. 2011.. Coleoptera) are a monophyletic in-group of Ten- ebrionoidea with almost 3000 species (Bologna et al. Cantharidin causes blisters on the skin of sensitive animals (some humans or horses). 2003). Wiegmann et al. 2005). Capinera. 2014. 2005). Due to the damaging effect on the digestive tract of animals. where the first so-called triungulin phase is the most important one. 2005).. possibly coupled to the radiation of the angiosperm plants (Beutel et al. The assignment of these two fossils to Mantispidae is doubtful at best (Wedmann and Makarkin. 2014). 4. It also acts as a sexual attractor and is linked to the sexual behav- iour in the in-group Meloinae (Bologna et al.2 Coleopterida (Coleoptera. Niehus et al..Insects as Parasites and Hosts 161 Engel (2004). 2014. This sister group relationship has been established rather recently based on molec- ular. Hypermetabolous development includes seven larval stages.. Yet. Another radiation of Coleoptera took place in the Jurassic. Meloidae have two exciting evolutionary modifications: the terpenoid cantharidin and hypermetabolous development (Grimaldi and Engel. 2012.and morphologically-based phylogenetic analysis (Beutel et al. 2009). 2003). Archostemata is thought to be the (extant?) sister group of all remaining coleopterans.. They have been considered to have originated in the Permian (Beutel et al. which led to their common name ‘blister beetles’ (Capinera. The triungulin larva .1 General aspects Blister beetles (Meloidae. Thus it protects meloids and their eggs from predators. the terpenoid cantharidin is effective against predators. Meloidae) Coleoptera and Strepsiptera are now considered to represent sister groups within the monophyletic group Coleopterida (Beutel et al. 2007). Approximately 355. The lineage of Coleoptera is extremely diverse and abundant on all continents (Beutel et al. In the Late Triassic... 2005). Grimaldi and Engel..

. Capinera. the host takes them in its nest and they parasitize the clutch (Engel. • The oldest and definitive direct observation of a hosteparasite relation- ship has been found in Middle Eocene Baltic amber (45 ma. 2008.162 Christina Nagler and Joachim T. 2003). the larva will be a pupa and is found in the soil. but appears unlikely when applying the concept of Occam’s razor. It has been suggested that phoresy appeared at least seven times independently within Meloidae (Bologna et al. Haug (Figure 3(f)) is often highly specialized for ectoparasitic behaviour in the form of phoresy (Chmielewski. They parasitize Hymenoptera (Apoidea) and sometimes grasshoppers (Acridoidea. If you consider that bees are quite uncommon in amber.2 Phylogenetic inference of appearance and molecular estimations of early evolution The triungulin larva evolved once in the stem-group Meloidae (Meloinae. thus this fossil indicates a loss of this hoste parasite relationship (Engel. 2005). 2005). • Poinar (1992) described a larva of Meloidae sp. One of their strategies is to wait on flowers and attach to the host with their grasping claws on the thoraco- pods. 2008). yet this interpretation has been questioned (Engel.. 2003). from Early Miocene Dominican amber. 2005). the larvae feed on eggs and moult briefly in the second stage from larval instars IIeV (Capaneira. Engel. Molecular clock studies indicate an even earlier appearance of Meloidae. Nemognathinae) around 112 million years old. They appear to have radiated fast with the acquisition of parasitism and hypermetabolism (Bologna et al. 1977 named phoresy ‘transportation para- sitism’) and is adapted to reach its host. 4.3 Fossil representatives There are three fossils of meloid triungulins. 2008).2. it was very lucky to find one with meloid triungulins on it. A similar relationship between Meloidae and stingless bees is not known nowadays. during the Early Cretaceous (125e135 ma). Proplebeia dominicana. Tetraonycinae. Bologna et al. 4. Once locating the host’s egg pod. • Larsson (1978) described an isolated meloid triungulin from Middle Eocene Baltic amber. Hymenoptera). Thus.2. . After two more stages. Engel (2005) described meloid triungulins on the setae of the bee Protolithurgus ditomeus (Megalichidae. 2005). on the pronotal dorsal surface of the extinct bee..

Given this pattern of character distribution. Proctotrupo- morpha. The only symphytan parasitoid group is Orussidae. Evanoidea. Trigonalyoidea.000 extant described species. Stephanoidea and Megalyroidea. which is the likely sis- ter group to Apocrita (Grimaldi et al.. 2013a). This type of biology is also retained the next group branching of the lineage towards the more derived apocri- tans. hence are parasitoids on parasitoid larvae (Perrichot.1 Hymenoptera 5.. Megalyroidea. Currently there are 125. 2002). Ephialtioidea. Representatives of Megalyroidea parasitize not only wood-boring bee- tles (as the groups before) but also spheciform wasps. parasitoidism appears to have evolved in or slightly before the stem species of Orussidae þ Apocrita (and was lost in apocritan in-groups). PARASITOIDS 5. 2013). Surprisingly the hosts of most extant species appear to be unknown (Engel and Perrichot.Insects as Parasites and Hosts 163 5. are ectoparasitoids of wood-boring beetles and symphytan wasps (Grimaldi and Engel.1 General aspects Hymenoptera is one of the most diverse groups among insects. are hyperparasitoids. Ephialtioidea (Figure 4(a)). Their close relatives. Stephanoideans have a very similar biology to species of Orussidae. 2014). 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. Ichneumonoidea (all of these Apocrita. Like species of Orussidae. trigonalyoideans. Stephanoidea. 2005). formerly also together called Parasitica) and some groups of Aculeata (Grimaldi and Engel. hyperparasitoidism and kleptoparasitism occur in numerous in-groups: Orussidae (a group of ‘plant wasps’). species of apocritan groups branching off early. This appears to have been an essential novelty for effective parasitoidism. traditionally divided in two groups: ‘Symphyta’ (‘plant wasps’) and Apocrita (‘waisted wasps’) (Delcl os et al. The wasp waist is restricted to Apocrita. 2005). This morphological character appears to provide them a better mobility of the abdomen and hence the ovipositor. 2007). Parasitoidism. but the . The supposedly ancestral appearing representatives of Aulacidae (Figure 4(b)) are parasitoids..1. Representatives of Evanoidea are diverse. The females use their elongated ovipositor to pierce through wood into the host that is later eaten by the parasitoid larvae (Engel et al.

Chrysidoidea) (modified after Gugliemino and Olmi (2011). Ceraphroni- dea. (2013b.164 Christina Nagler and Joachim T. 2014). Their inferred oldest rela- tives are species of the extinct group Praeaulacidae. Figure 2A)). (2013. more derived forms such as evaniids and gasterupiids are larval predators of cockroach oothecae (Grimaldi and Engel. Chrysidoidea) (modified with permission from Elsevier from Engel et al. Figure 4(b))). (a) Praeproapocritus flexus (Ephialtiti- dae. Haug Figure 4 Fossil representatives of Hymenoptera. (e) Deinodryinus areolatus (Dryinidae. Platygastroidea (Grimaldi and Engel. 2005). Ceraphronidea) Plo (modified with permission from Elsevier from McKellar and Engel (2011. Proctotrupomorpha is a group of usually very small and tiny parasitoids (except the giant Pelicinidae). Figure 2). Figure 3)). (b) Aulacus eocenicus (Aulacidae. Figure 1)). (d) Necrobythus pulcher (Scolebythidae. 2005). species of this group were abundant in the Jurassic and Early Cretaceous of Australia and Asia (Li et al. In-groups are Stigmaphronidae. Evanoidea) (modified after Nel and €eg (2004. These wasps are . Ephialtioidea) (modified with permission from John Wiley & Sons from Li et al. (c) Tagsmiphron spiculum (Stigmaphronidae..

beetles. Species of Pompilidae are also ectoparasitoids of spiders. only a few lineages retain a plesiomorphic parasitoid lifestyle. of web spinners (Embioptera). 2012). of beetle larvae (Coleoptera). Sapygidae in- cludes forms that are ectoparasitoids of larval wasps or kleptoparasites of bees..to endoparasitoidism (Grimaldi and Engel. 2011). Chrysidoidea appears to be the less-derived group and is rather species poor. The larvae of species of Dryinidae. Ecto- parasitoids in contrast suppress the immune system of the host with a poly- DNA-virus (Longdon and Jiggins. Tiphiidae comprises species that are ectoparasitoids of ground- dwelling larval beetles.. Among Ichneumonoidea (Braconidae and Ichneumonidae) the species of less-derived in-groups are ectoparasitoids of wood-boring beetles. stinging wasps). Rhopalosomatidae and Scoliidae. This is known in Chrysidoidea. 2014b). Within Ichneumonoidea different lineages switched multiple times from ecto. 2012). symphytans. lepidopterans or green lacewings and some are hyperparasitoids on other apocritan species (Shih et al. Within Vespoidea only few ‘primitive’ lineages are parasitoids. an in-group of Chrysidoidea. Representatives are ectoparasitoids of butterfly larvae (Lepidoptera). Species of Platygastridae and Scelionidae (in-groups of Platygastroidea) are both endoparasitoids of insect and spider eggs. dipteran pupae. 2007). 2013). cater- pillars and wood wasps. 2011). flies. In Aculeata (including ants. The known representa- tives of Ceraphronidea (Figure 4(c)) are either endoparasitoids of caterpillars. parasitize adult and nymphal cicadas (Auche- norrhyncha. 2002). Species of Mutillidae are ectoparasitoids of different holometablous . Hemiptera. of walking sticks eggs (Phasmatodea) and sometimes klepto- parasitic on bees and vespids (Azar.Insects as Parasites and Hosts 165 endoparasitoids of wood-boring or cone-boring beetles.. This has been seen as an indication that the morphology of these forms was preserved since the Cretaceous (Olmi et al. 2005). Guglielmino and Olmi. Mutillidae. Vespoidea and Apoidea. Sapygidae. namely Tiphiidae. The oldest fossil dryinids have been ascribed to a cosmopolitan extant genus. they paralyze their hosts.. All ichneumonid endoparasitoids possess a special poison that manipulates the host to construct a specific protection for the ichneumonid larva. other apocritans or Thysanoptera or hyperparasitoids on apocritans or aphidid hemipterans (McKellar and Engel. 2014a. such as species of Scarabeidae. Although ichneumonids are well reported since the Early Cretaceous. Scelionidan species do not complete their development until the host has reached adultness (Grimaldi et al. bees. such a virus could not be directly detected or visualized (Longdon and Jiggins. Olmi et al. Pompilidae.

. 2012. xylophagous and fungivorous. McKenna and Farrell. as Hyme- noptera is considered to be the sister group to the remaining holometabolans (Wang et al. moths. Vilhelmsen and Zimmermann.166 Christina Nagler and Joachim T. it remains unclear if these suggestions include the possibility that we might have holo- metabolous forms already in the Carboniferous.1. 5. After the host is dead. but with the origin of parasitoidism (estimated about 210 ma) hymenopterans diversified rapidly. Spe- cies of Rhopalosomatidae are ectoparasitoids of crickets. but also cockroaches. wasps. Sharkey et al. it is likely that the radiation of Orussidae took place in the Middle Cretaceous (100 ma. but no fossil forms of these have been found so far (Grimaldi and Engel. the larvae spin a cocoon and pupate within the host (Grimaldi and Engel.. Sphecidae and Crabronidae are parasitoids. Fossils ascribed to Proctotrupomor- pha from the Cretaceous support a possible Jurassic age of the group (Grimaldi and Engel.. 2012). Yet.2 Phylogenetic inference of appearance and molecular estimations of early evolution It has been put forward that the key feature in hymenopteran evolution was the development of parasitoidism. some ants are secondarily ectoparasitoids or klepto- parasitic. Within the proctotrupomorph Platygastroidea .g. 2011. Ampu- licidae. 2014). beetles. Lastly species of Scoliidae are ectoparasitoids of ground-burrowing beetles (Grimaldi and Engel. Their larvae feed on the living host for several larval stages. 2005). 2013). 2005). Heraty et al. 2013. Spheciform wasps are evolutionarily important as they are the sister group to bees (e. The fossil wood wasp Cratoenigma articulata from the Lower Cretaceous of Brazil seems to be an ‘intermediate’ form between the endophytic (non- parasitoid) forms of Xyledoidea and the parasitoid species of Orussidae (Krogmann and Nel. 2005).. These forms should have evolved at least in the Early Triassic. 2014). 2010). Based on phylogenetic and morphological studies. Engel et al. Johnson et al. different types of kleptoparasitism are known (Litmann et al. such as bees.. flies.. 2005). Klopfstein et al. Within eusocial bees. 2013a. Derivatives of early branchings in Hymenoptera are phytophagous. which triggered the largest radiation of parasitic arthropods in the wide sense (including parasitoidism). Also in the lineages that diverged from the ancestral type of parasitoidism and switched to other strategies. parasitoidism (or parasitism?) has (re-) evolved. 2014a. For example. entering the host’s body and live as endo- parasitoid. Haug groups.. Also species of spheciform wasps.

parasitoidism in this group originated near the TriassiceJurassic boundary (210 ma). 2014. 2005)... 2013b). Delcl os et al. Ward et al. a Cretaceous origin has been proposed. In short. Vilhelmsen.. but probably even earlier). 2009). Slightly younger finds are from the Upper Triassic of Argentina (Lara et al. Grimaldi and Engel. McKellar and Engel. 2013. Heraty and Darling. 2014) and from the Middle Jurassic of China (Wang et al. For Ceraphronidea. Hymenoptera evolved latest in the Middle Triassic (230 ma. 2013a. Stigmaphronidae. exclusively known from the . 2012). 2014b). • The few fossils ascribed to Ephialtioidea stem from the Early Jurassic to the Early Cretaceous (Li et al. 2013).1. Grimaldi and Engel. The occurrence of ants and bees was coupled to the radiation of angiosperms in the Middle Cretaceous (125e100 ma. 2014). • The fossil record of Orussidae is sparse with only two specimens from Cretaceous amber of Siberia and New Jersey. The group has been estimated to comprise not less than 500. • There are only a few fossils of Stephanoidea known so far. Chalcidoidean species are endoparasitoid or hyperparasitoid on a large range of hosts among insect par- asitoids.. They have been found in the Late Cretaceous of New Jersey. 2014. Aculeatan species existed from the Jurassic (155 ma) onward and radiated in the Early Cretaceous (140 ma). An in-group.Insects as Parasites and Hosts 167 the in-group Chalcidoidea underwent a spectacular radiation during the Eocene (55e35 ma. This lead to a rapid radiation of Apocrita in the Jurassic (195 ma).. Vilhelmsen et al... Additionally there is a single compression fossil from the EoceneeOligocene bound- ary of Florissant (Engel et al. Among the saw flies is the largest hymenopteran fossil with an estimated wing span of 92 mm (Gao et al. • Megalyroideans are known from Cretaceous Siberian amber. based on their biogeographic distribution (Perrichot et al. 2007). 2005.. and two specimens from the Late Jurassic of Kazakhstan and from the Oligocene of Colorado (Vilhelmsen and Zimmermann. the Middle Eocene Baltic amber and the Middle Cretaceous Burmese amber.. It comes from the Middle Triassic (220 ma) of Kyrgyzstan in Cen- tral Asia (Rasnitsyn. 5.. 2009). 1969).3 Fossil representatives • A specimen of Xyleoidea (saw flies) represents the oldest hymenopteran fossil.000 species (Heraty and Darling. 2003). 2007. Burmese amber and New Jersey amber and from Baltic amber (Delcl os et al.

Grimaldi and Engel. Grimaldi and Engel.. 2007. Grimaldi and Engel (2005) reported . Grimaldi and Engel.. Eocene Rovno. • The early record of modern in-groups of Ichneumonidea comes from the Lower Cretaceous. 2013. 2013. 2013. • Trigonalyoideans are rare in amber. • Proctotrupomorphans have been reported from the Early Jurassic of Asia. 2007. 2013. 2007). Jennings et al. • Evanoid fossils have been described from Cretaceous Lebanese amber. 2014. 2013b. Mexican. Engel. 2012. Poinar and Huber. 2005. 2007). 2009. 2004b). 2005. the group Dryinidae (Figure 4(e)) is the best recorded ectopar- asitic group in amber (Arillo.. 2002) (2) an ichneumonid female ovipositing into a caterpillar (Poinar and Miller. 2000). 1992) and (4) an ichneumonid larva that spins its cocoon over the eggs of a spider (Poinar. Grimaldi and Engel. 2011.. 2002) (3) an ichneumonid larva attached to a spider (Poinar. Late Eocene. Dominican. 2014.. Burmese.. as well as based on compression fossils from the Lower Cretaceous (Engel. Arillo. from the Cretaceous of China.168 Christina Nagler and Joachim T. from the Lower Cretaceous of Brazil and from the following amber deposits: New Jersey Baltic. Fossils are abundant as both. 2005). Grimaldi and Engel. Delcl os et al. Krogmann. of (Figure 4(d)) than there are extant species (Engel et al. 2011. 2013. Ortega-Blanco et al. Notable specimens are fossils come from Baltic and Dominican amber: (1) a braconid larva emerging from an ant (Poinar. Barling et al. Myanmar amber and New Jersey amber. Kolyada and Petrovsky. 2007): a fossil stigmaphronid hymenopteran from Mesozoic Spanish amber shows ovi- positing into a dipteran (Alonso et al.. 2004). Haug Cretaceous. Shih et al. dating from the Early Cretaceous to the Early Miocene. 2002). 2013a. 2013b. Delcl os et al. 2011... includes an additional fossil that provides direct evidence for their endoparasitoidism (Engel and Perrichot.... 2014. 2014. • Representatives of platygastrid Serphitoidea as well as of Scelionidae and Platygastridae are already known from the Cretaceous. • There are more fossil forms of Chrysidoidea.. but are not found in younger deposits (Engel and Perrichot. from the Cretaceous of Spain. but abundant as compression fossils (Early Cretaceous. Heraty and Darling. McKellar and Engel. Delcl os et al. 2005). 125 ma) (Engel and Perrichot. Canadian. Grimaldi et al. amber inclusions and as compression fossils until the Palaeogene (McKellar et al. 2005). 2007. Within Chrys- idoidea. Miocene amber from Peru (Perrichot et al. Nel et al. Delcl os et al.

Most females are wingless and sack-like. In some groups which retain some more ancestral features. In a comparable case. Grimaldi and Engel. special enzymes allow the larva to enter the host. To avoid the host’s immune defence. females bear short antennae. was interpreted as a spider wasp. the Lower Cretaceous fos- sil Cariridris bipetiolata (Brandao et al.2. This mechanism is unique among insect parasitoids and . Antropov and Pulawski. Hymenoptera. The first larva. • There are several spheciform wasps from the Caenozoic preserved as compression fossils and amber inclusions (Antropov. Hemiptera and Zygentoma (Rasnitsyn and Quicke. They are agile fliers. The larvae hatch immediately when the egg is laid (ovovivipary).Insects as Parasites and Hosts 169 a fossilized leafhopper with an attached thylacium. 2002)..1 General aspects Strepsipterans are obligate endoparasitoids. but was redescribed as a spheciform wasp (Dlussky and Rasnitsyn. These parasitize numerous different types of insects. Membracidae). 2000. but has been redescribed as a spheciform wasp (Rasnitsyn. 2005).. After finding a potential host. 2009. 2009). is called a triungulin (cf. mainly representatives of Auchenorrhyncha (like Cicadellidae. 600 extant species. 1975). The Caenozoic fossils resemble the modern spheci- form wasps (Grimaldi and Engel. 2009). • The Cretaceous Pompilopterous (Rasnitsyn. 2003). • Most vespoid in-groups occur since the Early Cretaceous. reduced (but still present) eyes and legs. Part of their success has been attributed to their pronounced sexual dimorphism and life cycle. a protective structure formed by retained parts of the exuviae of the first instar larva of the parasitoid. as the name suggest. 1998). Most of them search for larvae or nymphs. Strepsipteran males bare halteres and hind wings. The hosts’ life span can last until all strepsipteran larvae emerge from the host (Kathithiramby. They live their entire life within the host. Meloidae). the larvae mimic the host at a mo- lecular level. This larva actively searches for a host. 5. some go for eggs (Kathithiramby. 1996). 2002). but the oldest known specimen is a pompilid spider wasp (hence likely a parasitoid) from Middle Cretaceous amber of Myanmar (Grimaldi et al. the strepsipteran larva attaches to the host. lack functional eyes and antennae. but live only a few hours. Strepsiptera comprises ca. 2005). to find a female (Kathithiramy.2 Strepsiptera 5. 1990) has been originally described as ant.

Niehuis et al. especially CT analysis of Mengea tertiaria in Baltic amber (Beutel et al... A related case is known in endoparasitoid Aphelinidae (Kathithiramby. Finally the last larval stage emerges from host to pupate externally in all males. crickets and mantids.. derived from holometabolans. there are four further larval stages. Pohl and Kinzelbach (2001) suggested that the primary hosts of Myrmeco- lacidae were ants. 2013. Grimaldi and Engel (2005) proposed that it would not be surprising. the females also leave the host to pupate. 2005). In species in the less- derived group Mengenillidae. only the anterior region is visible from the outside (Kathithiramby. . The newly discovered Bahiaxenidae (Figure 5(a)) from Brazil has been considered to be the sister group of the remaining modern Strepsiptera. All other females remain endoparasitic in the host.2. The development of strepsipter- ans is classified as hypermetamorphosis (again cf. 2009). Eoxenos has been resolved as the sister group to all remaining forms (McMahon et al. 2012). The extinct forms Protoxenos. Probably during the Eocene (45 ma). Meloidae).170 Christina Nagler and Joachim T. such as stem- group neuropterids or mecopteroids. 2010). 2009)...and morphologically-based phylogenetic studies provide support that Strepsiptera is the sister group to Coleoptera (Boussau et al. Pohl et al. They have been interpreted as a relic group having changed only little since the Permian (Bravo et al..2 Phylogenetic inference of appearance and molecular estimations of early evolution The systematic and phylogenetic position of Strepsiptera has long been controversial.. Myrmecolacidae shows the so- called heterotrophic heteronomy (see Kathirithamby et al. 2010). Representatives of the extinct strepsipteran in-group Mengeidae were parasitoids of Zygentoma (silverfish. Haug explains their success (Kathitiramby. Bravo et al. if Strepsiptera is a highly modified lineage. 2009).. Pohl and Beutel. 2014. The hosts for males are ants. 5. those for females are grasshoppers. They have been thought to be the most problematic group of insects in terms of its systematic placement (Pohl et al. Grimaldi and Engel.. Cretostylops and Mengea are considered to be the derivatives of the evolutionary lineage towards modern Strepsiptera. excluding Bahiaxenidae. Within the remaining modern strepsipterans. 2009). the transition between less-derived and modern strepsipterans took place (Kathithitramby. After the triun- gulin larva. Recent molecular. 2010). 2009). 2014. 2009). 2011. This is based on morpho- logical data. One special case within Strepsiptera.

Kathirithamby and Grimaldi.. 2012. 1994. 1985. Strepsiptera) (modified from Grimaldi and Engel (2005. 2014. Figure 10. 2005. plant parasitic gall wasp (Figure 5(c)). Meng. 2008. 1866). Kinzelbach and Lutz. Poinar. Mengenillidae and Myrmecolacidae have been found. Ulrich.88) with kind permission of Cambridge University Press and David Grimaldi). Pohl et al. Hymenoptera) (modified from Grimaldi and Engel (2005. 2010. Figure 2)). (a) Bahiaxenos relictus (Bahiaxenidae. 1983. 5. Strepsiptera) (modified with permis- sion from John Wiley & Sons from Bravo et al. Kogan and Poinar. 1927. 1990. Kathirithamby and Hendricks. 2001.3 Fossil representatives • The majority of strepsipteran fossils have been found in various types of amber: Burmese (100 ma). 2002. 2001. Figure 11. Kinzelbach. Lutz. (b) Bohartilla kinzelbachi (Bohartillidae.Insects as Parasites and Hosts 171 Figure 5 Fossil parasitoid strepsipterans (Figure 5a and b). (c) Gall-forming cyn- ipidan (Cynipidae. Kulika. 1993. Cook.2. 2010. Canadian (75 ma). (2009. Mainly forms ascribed to Mengeidae. A great diversity of less-derived Strepsiptera has been found in Cretaceous Burmese . 1995. 1979. Eocene Baltic (42e45 ma) and Miocene Dominican (25 ma. Kinzelbach and Pohl.17) with kind permission of Cambridge University Press and David Grimaldi). Pohl and Kinzelbach. Kulika. 1979.

In such systems. phytophagous hymenopterans (sawflies). Donovan et al. this is a form of plant parasitism. (4) two parasitized planthoppers. Haug amber. here the line to phy- tophagy is not easy to draw.. Thysanoptera (thrips). Moth larvae are important leaf miners. Grimaldi and Engel. Galls are remarkable structures occurring on all organs of a plant. based on their unique characteristics. 2005). 2001).. 2013).. With galls an insect is forcing the plant to provide nutrition and/or a habitat. PLANT PARASITISM (VERSUS PHYTOPHAGY) 6. (2) an ant with an emerging parasite preserved in amber (Pohl and Kinzelbach. 1994). Tingidae (lace bugs). Psyllidae (jumping plant lice). mites. 2001). • 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.. 2014. Exceptionally preserved fossils from the US provided an uncompressed planteinsect system from the Palaeocene (Donovan et al. Some insects oviposit eggs into plants and induce the growth of galls. position on the plant. 2014. (5) a female specimen ascribed to Myrmecolacidae parasitizing an ant in Baltic amber (Pohl and Kinzelbach. (3) an empty male puparium associated with a hyme- nopteran preserved in amber. shape. Cecidomyii- dae (gall midges). viruses and nematodes (Knor et al. However. 2004b) and preserved in amber.g. the larvae feed on the plants until they emerge as pupa or adult. path of the mine and size. fungi. the egg is oviposited into the leaf and the larvae feed on the mesophyll until they pupate and fall on the ground (Labandeira et al. e. Anisoptera (dragonflies). Wappler et al. it is possible to identify the parasite that caused fossil mines and galls (Carvalho et al. In leaf miners. 2013. Galls can be also induced by bacteria.. host specificity. thus it is comparable to larval parasitoids feeding within insects. 1990). Aphididae (plant lice). 2009). 2014. Yet some insects also make use of plants in other ways. 6. more modern (Figure 5(b)) and less-derived strepsipterans occur together... Cicadellidae (leaf- hoppers) and some heterocerans (moths) (Knorr et al. thus this should represent a case of true parasitism. from one of these planthoppers emerge larvae (Poinar. Gall- inducing insects are representatives of Cynipidae (gall wasps).1 General aspects Numerous insects consume plants. Coleop- tera (beetles). In Baltic and Dominican amber.172 Christina Nagler and Joachim T. Grimaldi and Engel. 2005). .

2 Phylogenetic inference of appearance and molecular estimations of early evolution Inducing galls has evolved multiple times independently among the insects. Krassilov.. The main radiation of Ceci- domyiidae took place during the Palaeogene coupled to the evolution of flowers (Wappler et al. 2013. 2010). 2005). But this attribution has been considered doubtful. (2008) reported eggs which were found inside the interior of a fossil leaf from the Carnian of Austria (150 ma). 1994). A significant radiation of gall-inducing and also leaf-mining insects occurred in the Late Cretaceous.Insects as Parasites and Hosts 173 6.. 2002). • Pott et al. These dipterans have been considered to have originated in the Late Jurassic. 2002. The origin of gall making in Hymenoptera occurred first in the Middle Cretaceous when first forms of Fagacea (beeches and oaks) appeared in the fossil record (Grimaldi and Engel.. 2007).3 Fossil representatives There are numerous plant fossils with galls (Palaeogallidae) and mines (Palaeominidae) on plants as well as adult free-living plant parasitic insects. like modern relatives (Grimaldi and Engel. 2011). They suggested . 2005). at first parasitizing gymnosperms and switching later to angiosperms (Labandeira et al.. most likely coupled to the radiation of the angiosperms (Knorr et al. Rasnitsyn and Quicke. Several fossils indicate an origin of Cynipodea in the Jurassic. see Labandeira (2013) and Labandeira and Currano (2013). • There is one extraordinary fossil: galls on the seed of a redwood from the Miocene of Germany containing larval and pupal gall midges (M€ ohn. 6. Most fossil galls resemble their modern counterparts. 2013.. Labandeira et al. as also mites may produce comparable galls (Grimaldi and Engel. which emphasizes the long-term evolutionary coexistence and coevolution of host plant and parasitic gall- making insect (Knorr et al. The gall midges (Cecidomyiidae) are known since the Late Jurassice Early Cretaceous (Grimaldi and Engel. This ability is considered to have originated first about 300 ma in the Carboniferous in a not further known holometabolous larva (Labandeira. Hence we only list here some examples: • The oldest representative of Cynipidae (Figure 5(c)) is from Baltic amber and could induce galls on rosaceans. 2005. 2005). 1960). Rasnitsyn and Quicke. For a more comprehen- sive review. 1994).

174 Christina Nagler and Joachim T. Maas.g. 2001). Labandeira. Gordiids have a free-living aquatic phase and an obligate parasitic phase on terrestrial invertebrates. Poulin. 2002. . Poinar. 2005). Rota-Stabelli et al. Although there are about 20. 2011a. 2013 and references therein). Within the hairworms.1.1. 2013). moths on mahogany (for 40 million years) and beetles on Heliconia (for 70 million years) (Grimaldi and Engel. INSECTS AS HOSTS 7. small aquatic insects.500 species that are endoparasites of arthro- pods and vertebrates (Poinar and Thomas.2 Phylogenetic inference of appearance and molecular estimations of early evolution Nematoidea has been considered to have originated in the Precambrian (Poinar. 350 extant species are known which fall into two groups: Gordiida with freshwater and terrestrial forms and Nectoma with marine forms (Schmidt-Rhaesa. 2006).1 General aspects The monophyletic group Nematoidea consists of the two sister groups Nematomorpha (hairworms) and Nematoda (roundworms) (Bleidorn et al. several million species have been estimated (Schierenberg and Sommer. moths on poplars (for 20 million years). 2001). Cambrian fossils of cycloneuralians are diverse and hence indicate an older divergence of the subgroups (e. Fossil nematode parasites are treated in detail elsewhere in this volume (Poinar. the final host (insect) has to eat the intermediate host (freshwater snail.. Yet also other insect groups possess long ovipositors. Schmidt-Rhaesa and Ehrmann. cockroaches and praying mantids (Schmidt- Rhaesa and Ehrmann. 2013a. that is needed to pierce through the robust leaves of bennet- titalean plants.000 described extant nematode species. 2015b. 2002. 2014. 7. 2013). due to the elongated ovipositor.. 2015). grasshoppers. 2011a. 2013). 2012a). Poinar. 7. Extant species parasitize carabid beetles. • There are some leaf-mining fossils that appear extremely similar to their modern counterparts: moths on oaks (for 20 million years). Haug the possible parent could have been a dragonfly. The parasite goes through two hosts. Schmidt-Rhaesa.1 Nematoida 7. Nematoda includes about 10. 2011.

without a host (Poinar and Buckley.2. Mites use insects.Insects as Parasites and Hosts 175 7. due to coevolutionary processes.3 Fossil representatives It has been considered that less-derived forms parasitize less-derived insect groups (Blattaria and Mantoptera) and more derived nematomorph groups parasitize more derived insects. ants and other arthropods for transport in a phoretic way also (Dunlop and Penney. 2012). 2007). • Other nematomorph fossils include two females in association with their cockroach host from Dominican amber (15e45 ma) (Poinar. we could assume a similar age to these insect groups.. .1. 2001). • Cretachordodes burmitis comes from the Early Cretaceous Burmese amber (100e110 ma).2 Mites 7. They are also important vectors of several viruses and bacteria. like coleopterans (Schmidt-Rhaesa and Ehrmann. yet it is an isolated specimen. Australia.1 General aspects Acari comprises about 55. The oldest nematomorph fossils were found in Cretaceous deposits (Poinar and Buckley. There are some fossils that need to be discussed in reference to Gordiida recorded so far. for example Borrelia burgdorferi that causes Lyme disease and might have already been so in the past (Poinar 2014a. 2012). known as mites. 2006). which is attractive to roaches and carabids and that small forest streams seem to be their aquatic habitat (Schmidt-Rhaesa. 7. Yet. Hence although the direct fossils are rare.. that their habitat was moist to wet. They can be free-living herbivorous and scavenging. 1994). A fungus and its ecology indicate.000 described extant species. 2010). • Other fossil worms of Palaeoscolecida may resemble Nematomorpha (Xianguang and Bergstr€ om. partic- ularly termites.b. resembles a nematomorph larva in many aspects (Maas et al. similar to kino- rhynch cycloneuralians. this form may have lived in the meiofauna. 1999). 2013). but have been interpreted to be early offshoots of the lineage towards Priapulida (Harvey et al. 2015). 2006). • Shergoldana australiensis from the Middle Cambrian of Queensland. Pereira et al. as well as predatory.. 2012. or parasites of insects and vertebrates (Dunlop and Penney.

7. 270 ma. . Azar. 2002).. 2007). 2007).2. 1997). Azar. 2014. a wide range of dipterans. Koteja and Poinar. 2007. Chironomidae. • There are also mites parasitizing hemipterans from several different amber deposits (Poinar et al.. They occur together with their host. Dunlop et al. • In Baltic amber. Dabert et al. Arillo. 2009. • Phoretic behaviour has been reported from Cretaceous amber sites and Eocene Baltic amber (Dunlop et al. has been proposed based on molecular data (Garwood and Dunlop. 2007. For the parasitic in-group Astigmata an origin in the Middle Permian. have been reported to parasitize several forms of Diptera (Arillo. 2007).. 2012). • Some parasitic mites in amber are associated with their host. Klompen and Grimaldi. 2005). • A representative from the supposedly more ancestral Anactinotrichida is known from Rhynie chert of Scotland (395 ma) and other Devonian sites (Norton et al. 2010). They parasitize rep- resentatives of Chironomidae (nonbiting midges) or Trichoptera (caddis flies.. 2007). but also compression fossils) of mites (Figure 6(d)) preserve them still attached to their insect hosts (Judson and Maakol. Parasitic mites (Figure 6(c)) of the species-rich group Leptus have been preserved in Baltic amber. 2007. Mites parasitizing representatives of Drosophilidae. Dunlop. 2001. both from the Lower Cretaceous.2. Poinar et al. • Mites from Spanish amber and Lebanese amber. 2014. like fungus gnat (Limoniidae). but also with different types of hymenopterans (Dunlop et al.. 2012. 2007. Haug 7. Phoretic behaviour in mites has been proposed to have evolved at least in the Eocene (44e49 ma. Labandeira.. 1988). 2012. Arillo. Arillo.176 Christina Nagler and Joachim T. water mites have been found too. 2012).2 Phylogenetic inference of appearance and molecular estimations of early evolution The origin of mites was estimated to be in the Late Silurian (Mans et al. • Cretaceous fossils (in amber. 2011)..3 Fossil representatives Acari are comparably abundant in the fossil record with 309 fossil records (Dunlop and Penney. Sciaridae and moths have been reported from Domin- ican amber (Arillo. window gnats (Empididae) and Dolichopodidae..

3. (e) Cheliferidae indet (Cheliferoidea. Also pseudoscorpions possess a characteristic cheliceral spinning apparatus .Insects as Parasites and Hosts 177 Figure 6 Vectors and hosts. Acari) attached to Ctenobethylus goepperti (Dolichoderinae. Diptera) (modified after Poinar (2008b. (Mesostigmata. Formicidae) parasitized by nematodes (modified after Poinar (2012a. Acari) on a chironomid midge (Chironomidae. (c) Myrmozercon sp. Formicidae) (modified from Dunlop et al. yet their posterior segments are not differentiated as a tail. (a) Pheidole dentata (Myrmicinae. Pseudoscorpionida) (modified from Judson (2009. Figure 5(b)) with kind permission of Geodiversitas and Mark Judson).1 General aspects There are currently 3533 described extant species and 41 fossil species of pseudoscorpions (Harvey. Figure 6(c))). (d) Erythraeid mite (Erythraeidae. (b) Lutzomyia adiketis (Phlebotominae. 7. Figure 2 with kind permission from Springer Science and Business Media). Pseudoscorpions distantly resemble scorpions. 2013). Figure 1)).3 Pseudoscorpions 7. (2014. Figure 1(b)) with kind permission of the Royal Society). Diptera) (modified from Poinar and Krantz 1997.

It has been proposed that phoresy originated at least five times within pseudoscorpions (Judson. 2014. 2010).178 Christina Nagler and Joachim T. Diptera (Aguiar and B€ uhrnheim. and allows dispersal via phoresy (Poinar.. Species of Tridenchthoniidae.. yet this would mean that the long time stable group Lipoctena would represent an artefact. Representatives of a few pseudoscorpion groups show highly complex behaviour and are subsocial in the form of brood care (Del-Claro and Tizo-Pedroso. Lechytiidae. Cheliferoidea (which has representatives showing phoretic behaviour) has been considered to be the most derived group of pseudoscorpions due to their morphology and behaviour. Szymkowiak et al. Lepidoptera. 1998) and other arthropods (Grimaldi and Engel. 2004). Dunlop. Geogarypidae.2 Phylogenetic inference of appearance and molecular estimations of early evolution The origin of arachnids has been considered to be in the Silurian. Boucot and Poinar. Judson. The minute pseudoscorpions live in cryptic environments and are predators of other nonvertebrates (Del-Claro and Tizo-Pedrosos. Due to some complex morphological characters. The phoretic relationship between pseudo- scorpions and invertebrates provides evidence for a long-standing and stable coevolution (Boucot and Poinar.. 2007). Some pseudoscorpions are host-specific and some are also site- specific on the host (Poinar.3. 2009). 2013b. 2007). All pseudoscorpions have chelate pedipalps (a major reason why they distantly resemble scor- pions) and many groups have a venom gland inside the pedipalp. 2010). The fossil record of pseudoscorpions reaches back to the Devonian (Dunlop. 2010). Host species are known from Coleoptera. because representatives were diverse and wide- spread in the Cretaceous already (Judson. 2009. 2005). Grimaldi and Engel. Boucot and Poinar. Recent morphological and molecular studies resolved a sister group relationship between pseudoscorpions and scorpions (Garwood and Dunlop. This is done in a way that does not affect the locomotion capacities of the host. 2010). 2010). 2010. 2009). Chernetidae and Cheliferidae are known to be phoretic (Szymkowiak et al. traditionally pseudoscor- pions are interpreted as the sister group to camel spiders (Solifugae. Sternophoridae. Haug (Dunlop. 2010. With their chelate pedipalps some pseudoscorpions temporarily attach themselves to larger nonvertebrates. Homoptera. 2009. 2004). Pepato et al. Larcidae. . Cheiridiidae. 2013b. The origin has been suggested to be older than the Cretaceous. Syarinidae. 2005). Judson. 7.

1996) and Lower Cretaceous Albian amber (Delcl os et al. It remains unclear whether this spe- cies was phoretic. Grimaldi. 1998) and also from Baltic amber (Hendrickx et al. 1920). Chelifer eucarpus. 2014b). 1991). all preserved in various types of amber. • The next younger fossil is known from approximately 250 million years later in Cretaceous amber. 2014). 1996). About the same age are three pseudoscorpions (two specimens of Heur- taultia rossiorum and one undescribed specimen) (Figure 6(e)) from the Lower Cretaceous Albian amber from France (Judson..3 Fossil representatives • The only non-amber and oldest pseudoscorpion fossil is Dracochela depre- hendor from the Middle Devonian (374e92 ma). 1992. 2010). (2) two pseudoscorpions from Madagascan copal and (3) two specimens from Colombian copal (Judson. 2006).. 2000. The most important arthropods that serve as vectors are haematophagous insects and arachnids (ticks). • Five subfossil specimens of unclear exact age have been reported from: (1) Zanzibar copal. INSECTS AS VECTORS 8. • There are several fossils with direct very evidence for phoresy: pseudo- scorpions on beetles (Poinar.Insects as Parasites and Hosts 179 7. 2007). but it is difficult to give fossil evidence for it (Poinar. 1991). . Undescribed pseudoscorpions have been reported in Upper Cretaceous New Jersey amber (Grimaldi et al. Lower Cretaceous Lebanese amber (Grimaldi.1 General aspects Extant insects are important vectors for numerous viruses..3. 2009). 8. on a braconid wasp (Weitschart and Wichard 1998). Another species has been described from Miocene Chiapas amber (Riquelme et al. on a nem- atoceran fly (Kosmowska-Ceranowicz. 1998). 2002). 2004. on a snipe fly (Ross. bacteria and protist. Cockerell. 1998). several specimens from Dominican amber (Judson. on flies (Judson. It is a nymphal specimen attributed to Che- liferoidea from Upper Cretaceous Canadian amber (Schawaller.. 2001). on a moth (Boucot and Poinar. Also there are two specimens from Burmese amber (Judson... Poinar et al. 2013b. based on isolated cuticle fragments (Schawaller et al. 2010).

They can be mutualistic. 2011). coprophagic beetles and synanthropic flies. cucumber beetles. 2014). an in-group of Trypa- nosomatida is spread through bites by sand flies. 2015. parasitic and commensalic (Longdon and Jiggins. Fleas via their mouthparts can transmit one of the most devastating diseases in human history: the plague that is caused by the bacteria Yersinia pestis. Examples are trench fever. The most ‘famous’ disease transmitted by culi- comorphans is malaria that is also caused by a protozoan parasite. 2001). bacteria and rhabdovirus (Azar and Nel. with phytopathogen fungi (Kluth et al. anaplasmosis.. blackflies and tsetse flies (Poinar.. spittlebugs. Also some viruses. mosquitoes. and then transmitted to vertebrates (Poinar. dermatomycosis. Light et al. breakbone fever. flea beetles. Ceratopogonids and mosquitoes are vectors for more than 300 viruses that cause. Czosnek et al.. malaria parasites. river blindness or elephantiasis (Grimaldi and Engel. Also they are vectors for several worm parasites and protists (Grimaldi and Engel 2006). 2007). relapsing fever. due to their phytophagy.. Lebombo virus or heartworms (Mitchell. psyllids and fruit flies serve as vectors for several bacterial phyto- pathogens that damage plants (Nadarasah and Stavrinides. with trypanosomatids as the most widely distributed pathogen. Aphids. Phlebotomines transmit several animal trypanosomes. Endosym- biotic bacteria. Almost 10% of all described extant sand flies transmit bac- teria. but also wildlife diseases. like swine pox. Additionally cockroaches. leafhoppers. Haug Extant lice transmit significant human diseases. 2005). called geminiviruses (Graczyk et al. 2010). Aphids and some beetle species mechanically transport fungus spores and infect plants. 2003).180 Christina Nagler and Joachim T. typhus. 2005. whiteflies.. 2014b). leafhoppers and treehoppers are important vectors of protozoan parasites and viral elements. It has been proposed that free-living trypanosomatids associated with food sources for dipteran larvae were eaten by these. viruses and protozoans can influence the biology of their insect vectors. 2012). An important endosymbiotic bacterium is Wolbachia that has been reported to be transmitted by almost all terrestrial arthropods as well as nem- atodes (Koutsovoulos et al. 2010). and then were still present in the adult stage of a dipteran. for example. 2008b. 2002). One of the most important groups in transmitting pathogens is Diptera. cytoplasmic polyhedrosis . especially in-groups such as sand flies. All forms of Trypanosomatida are parasitic (Lopes et al. viruses and protozoans.. The intracellular protozoan Leishmania.

which are viruses transmitted by insects. The long relationship of parasites and insects indicates a coevolutionary mechanism (Czosnek et al. 2003).. where the insect served as vector and host. These may have coevolved with certain species of Diptera (Psychodidae and Culico- morpha) since the Early Cretaceous. . Due to their haematophagy parasitic diseases are likely as old as the sand flies themselves (Azar and Nel. 2008a). to the final form with the insect as host. Poinar. 2014). 8. Different insect-borne viruses. in the Middle Caenozoic. at least 20 ma (Duron et al. a c-proteobacterium. 2011. together with species of Ceratopogonidae as their ancient vectors (Pérez- de la Fuente et al. Thus the protozoan parasites should have originated at least in the Early Cretaceous. Poinar. Similar parasites that were vectored by sand flies have been proposed to have contributed to the extinc- tion of the dinosaurs (Azar and Nel.. 2003). These viruses are always fatal to the population of the infected insects.Insects as Parasites and Hosts 181 virus (CPV) and nuclear polyhedrosis virus (NPV). Thus phytopathogenic bacteria evolved to become insectopathogenic bacteria (Nadarasah and Stavrinides. The recent discovery of Arsenophonus.. 2004a. infect only insects and are distributed among their populations. 2011).. have been considered to exist for at least 100 million years. 2005). The similarity of fossil and extant and fossil trypanosomes has been seen as a strong indication for haematoph- agy in the past (Poinar. 2015. thus providing an evolutionary path for vertebrate infections (Poinar and Poinar. 2011). The interaction between wolbachians and insects is stable at least since 100 million years according to some molecular studies (Cerveau et al.2 Phylogenetic inference of appearance and molecular estimations of early evolution Throughout their evolution sand flies and parasitic organisms likely have coevolved. probably played an important role in the evolution of bat flies and louse flies for the development of their true ectoparasitism. 2005c). 2013).. Greenwalt et al. Current research on phytopathogens transmitted via insects sheds new light on their evolution. whereas some attack mammals and birds also. 140 ma. supposedly with bats as primary hosts (Otalora-Luna et al. 2001). The association of hemipterans and trypanosomas originated at a similar time. The traditional role of insects might have evolved over a transitional stage..

In both cases. • different plasmodia on dipteran specimens from Cretaceous amber (Poinar. in early hymenopterans by injecting the egg into a host. the provided images cannot easily be used to judge this ascription. for example. a few overriding patterns can be mentioned. Poinar and Poinar. 2005). which likely triggered a . in fleas or lice. Haug 8. 2005). Also here the images provided in the description hardly allow a confident judgement or interpretation. 2005).182 Christina Nagler and Joachim T. However. CONCLUSION Given the shear vastness of examples of parasitism in and by insects. there were in- dependent switches to feeding on flower products. Poinar and Telford. where developing successful dispersal mechanisms are likely one of the important factors in the early diversification of these two lineages. the parasitic act is directly linked to the provision of nutrition to offspring.3 Fossil representatives Despite the small size of many of the organisms. Compared to other lineages the parasitic act is therefore less of an ‘everyday business’. and in dipterans by haematophagy of the female to have enough nutrients to be stored in the eggs. 2005c) • two trypanosome parasites (Paleoleishmania proterus and Paleoleishmania neotropicum) from the gut and proboscis of a specimen of Phlebotominae (Figure 6(b)) from Dominican amber and Burmese amber (Poinar. • three fungal pathogens from insects in Dominican amber (Poinar and Poinar. 2005) 9. there have indeed been some fossil finds in amber that were interpreted as including: • numerous flagellates (similar to Trypanosoma) on a faecal pellet of a hae- matophagic hemipteran from Dominican amber (Poinar. • a supposed NPV in a sand fly from Burmese amber (Poinar and Poinar. Another similarity is that in both Hymenoptera and Diptera. So we can indeed ask what made these two lineages so successful. namely Hymenoptera and Diptera. Two of the four hyperdiverse lineages appear to have their early radia- tions coupled to parasitism sensu lato. which mainly means that in both lineages the mobility of the adult is retained. it is hard to draw any major conclusions. 2011b. 2004b) • a supposed CPV and Trypanosoma infection in a midge from Burmese amber (Poinar and Poinar. This is quite different. 2008a.

Regrettably most fossil examples for palaeoparasitism only provide indirect evidence for parasitism (pathological changes of the host. Nevertheless. for which there is a much better record than in many other metazoan groups. including fossil data. An overview of the origin of the discussed species is given in Figure 7. second diversification. we . 10. phylo- genetic inference) and these are more difficult to compare to their extant counterparts.Insects as Parasites and Hosts 183 Figure 7 Timescale of the discussed groups. This must remain a task for future approaches. OUTLOOK With the given examples. But even with all these fossil examples. Solid lines are based on actual findings of the respective groups. Dashed lines indicate the ghost range of the respective groups. yet it would be an interesting candidate pair for a closer comparison. This parallel type of pattern in Hymenoptera and Diptera might be superficial. Also we find lineages within Hymenoptera and Diptera that switched back again to parasitic lifestyles. these fossils have the potential to reveal impor- tant aspects of the origins and diversification of parasitic lifestyles in various evolutionary lineages. functional morphology of the isolated parasite. we provide direct and indirect evidence for palaeoparasitology concerning insects.

They also provide their minimum age. we have to combine several methods. B€uhrnheim. but it is important to find these fossils. Yet. Both authors thank J. J. Unfortunately ectoparasites may well be removed during the preparation process. N. their environmental impact. we can hope to identify more interme- diate forms between fossils and extant species or between different lifestyles.F. their evolution with their minimum age. we are able to answer questions of the functional morphology. radiations and extinctions and the changing of their lifestyle from free living to parasites to vectors. Much of the direct evidence for parasitism is found in amber. the smallest mite can be visible on an insect. ACKNOWLEDGEMENTS Foremost we thank the editors for the invitation to contribute to this volume. their ecol- ogy. Often parasitic insects would not be recognized due to their size or lifestyle. biogeographics.184 Christina Nagler and Joachim T. Image Analyzer. 1998. Fossils provide a snapshot of the historical biogeography. To understand the evolution. Haug only get a phenomenological insight. evolutionary history and morphological diversification. While molecular data are generally thought to help to develop an evolutionary scenario only fossils allow a true look into former times. because this resin preserves specimens with microscopic details. Phoretic pseudoscorpions associated with flying in- sects in Brazilian Amazonia. Thus. REFERENCES Aguiar. ecology and morphology of these fossil parasitic insects. Arachnol. CombineZM. P. But also fine-grained sedimentary rocks preserve fossil specimens very well. With the aid of additional fossils. molecular studies. M. this is not a one-way road. phylogenetics. JTH is kindly funded by the German Research Foundation (DFG) under Ha 6300/3-1. Starck. Munich. for his support. . such as OpenOffice. To tell their ‘true’ story (or at least to come closer to it) more and more fossils are needed. taphonomy.g. biology. Only holistic approaches with a mature concept of reciprocal illumination between fossil and extant knowledge will provide a more detailed understanding of the evolutionary processes leading to the modern forms. especially in groups that are considered to have a sparse fossil record.. CombineZP. often because they were not recognized as parasites. We thank all people involved in providing free and low- cost software. fossil record and extant species. 26.O. geochem- ical studies. CN is funded by the Studienstiftung des deutschen Volkes with a PhD fellowship. also knowledge on extant forms is necessary to better understand fossil specimens. 451e459. e..

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modifying growth rates. until recently. University of Missouri.doi. 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.edu Contents 1. CHAPTER FIVE Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time John Warren Huntley*. USA x Fachgruppe Pal€aoUmwelt. 201 .apar. have largely been overlooked by students of the fossil record. but. but induce the growth of characteristic malformations in the shells of their bivalve hosts. Concluding Remarks 225 Acknowledgements 226 References 226 Abstract Parasitism is one of the most pervasive phenomena amongst modern eukaryotic life and yet.1 Taxonomic. MO. Friedrich-Alexander-Universit€at Erlangen-N€urnberg. Kenneth De Baetsx *Department of Geological Sciences. Germany 1 Corresponding author: E-mail: huntleyj@missouri.05. in some Advances in Parasitology. causing immobilization and. temporal and ecological occurrences 211 3.1016/bs. relative to other biotic interactions. In this review. j ISSN 0065-308X http://dx. almost nothing is known about its history in deep time. These malformations are readily pre- served in the fossil record. Trematodes are known to negatively affect their bivalve hosts in a number of ways including castration.004 All rights reserved. we present the various malformations induced by trematodes in bivalves.org/10. Detrimental Effects of Trematodes on Living Bivalves and Their Potential 222 Evolutionary Implications 5. Columbia. which have practically no body fossil record. Trematode-Induced Shell Malformations in Living Bivalve Molluscs 206 3. 1. Occurrences of Trematode-Induced Pits in Fossil and Subfossil Bivalves 211 3. Erlangen.3 Trematode-induced malformations as palaeoenvironmental indicators 220 4. Volume 90 © 2015 Elsevier Ltd.2015. GeoZentrum Nordbayern. Digenean trematodes (Platyhelminthes) are complex life cycle parasites. Introduction 202 2.2 Taphonomy and the origin of the trematodeebivalve parasiteehost 217 interaction 3.

.. consider the potential biases introduced by the process of fossilization and try to disentangle these biases from the biotic record so that . Kowalewski et al. 1969. is one of the most pervasive phenomena amongst modern eukaryotic life (Poulin and Morand. 2003). 2014. 1989. To that end. 2010). Klompmaker et al. 2000) and..202 John Warren Huntley and Kenneth De Baets cases. 1. 1967. There is an increasing appreciation for the roles of parasites in shaping communities (Hudson et al. 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. 1978. sys- tematically analyze the occurrence and intensity of parasiteehost interactions through geologic time. which has highlighted the likely role of antagonistic interactions in shaping macro- evolutionary trends (Vermeij. 2003... almost nothing is known about it in deep time (Littlewood and Donovan. Parasites and the traces they leave behind have been preserved as fossils (Moodie. Digeneans are expected to be significant agents of natural selection. 1984. 2014.. 1981. 1998. one must first explore its origin in a phylogenetically informed context. 1998.. however. 1923. Savazzi. we discuss how bivalves may have adapted to their parasites via heterochrony and suggest a practical methodology for testing such hypotheses in deep time. Littlewood and Donovan. De Baets et al. 2002. Boucot and Poinar.. 2007). Huntley and Kowalewski. Based upon their relative positions within trophic webs. 2006) and promoting evolvability (Zaman et al. but may not be an important agent of natural selection in benthic marine environments (Stanley. parasites are likely to be more abun- dant and diverse than predators in modern ecosystems. 2015a). Wilson et al. 1995. Cameron. 1998. 1977. Boucot. Huntley et al. 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. 2002. 2011). 2006. Signor and Brett. The primary focus of this pursuit has been the examination of predatoreprey interactions. Conway Morris. 2003. Gahn and Baumiller. 2008. 1990. 2008). Ruiz and Lindberg. 2011. Kelley and Hansen. Parasitism.. but the docu- mentation of the intensity of specific parasiteehost interactions through deep time is rare indeed (for some notable exceptions see Brett. 2003. Fry and Moore. 2014). Feldman and Brett. Tyler and Leighton. Madin et al. Feldmann. altering host behaviour making the host more susceptible to their own predators. Baumiller and Gahn. Competitive interactions have received some attention in the literature (Hermoyian et al. relative to predation.

of course there are exceptions: Fry and Moore. Zottoli and Carriker.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.g. we know that the trace or mal- formation was the result of a liveelive interaction. 2007. A variety of taxa can produce or induce the formation of a trace or shell malformation when interacting with the bivalve. Baumiller and Gahn. thereby. 1974. fungi. 2005). prokaryotes (e. 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.g. Poinar. Chlamydia and Rickettsia). whereas live spionids were not identified in borings found in dead brachiopods from the same location.. . 2003. and. Huntley. 2007). strictly parasitic in origin.and deposit-feeding (Dix et al. 2015). bryozoans and arthropods). 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. platyhelminths. Unfortu- nately. in some cases. 2002. and (2) interactions that induce a growth reaction by the bivalve. Rodrigues. amongst others). Rodrigues. 2007. annelids. The work of Rodrigues et al. we must seek evidence for parasitism in the form of traces and malformations on the mineralized hosts. Bivalve molluscs serve as hosts to a diverse group of parasites and disease- causing agents including viruses. 1973. Gahn and Baumiller. 2007.g. therefore. Indeed. and. we should not expect an extensive record of body fossils (although. From this perspec- tive. we cannot distinguish between a liveedead and a liveelive interaction. parazoans (e. Spio- nids are generally capable of suspension. For instance. molluscs. boring sponges like Cliona) and metazoans (e. not all interactions result in the production of a trace or shell malformation. Thayer. 1974. see Lauckner (1983) for an excellent account of the myriad parasites and diseases of bivalves. protistans. thereby. relative to the bivalve. (2008) revealed that spionid borings in live brachiopods of coastal Brazil were nearly always occupied by live spionids. 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. 1969. 2003. one of the primary challenges when interpreting these traces is determining if the interaction was ante-mortem or postmortem. Given that many parasites are typically small-bodied and often lack biomineralized skeletons. Many taxa produce this first type of trace in bivalves and they may not be. Huntley and Scarponi.

Boucot and Poinar. 2010).g. arthropods. therefore. 2003. 2015). 2001. In order to maximize the likelihood of studying liveelive interactions in the fossil record. we are left hypothesizing the taxonomic nature of the putative parasite. Though the taxonomic iden- tities of the culprits are uncertain. which may or may not be parasitic. Littlewood. result- ing in a raised blister within the valve. respectively. In both examples. which is filled with mud and worm faeces (Blake and Evans. There are many other taxa that bore into bivalves and other carbonate substrates. bivalves and predatory gas- tropods (Boucot.204 John Warren Huntley and Kenneth De Baets Despite evidence for liveelive interactions in modern settings. occasionally and subsequently a vertebrate intermediate and/or a final stage within a vertebrate definitive host (Cribb et al. including cavities. 1990. annelids). Cliona). 1973. and is. Savazzi (1995) reported shell malformation of diverse morphologies. including sponges (e.. Huntley. 2006). Such traces are also made by the aforementioned. Digenean trematodes (Platyhelminthes) are endoparasitic flatworms with complex life cycles that can include free- swimming stages. 2007. Ozanne and Harries (2002) document the occurrence of ‘bubbly nacre’ and ‘Hohlkehle’ (a rib-like malformation on the valve interior) in Cretaceous inoceramids of the Western Interior Seaway. Huntley and Scarponi. Given that these traces can be made following the death of the putative host they will not be considered further here. Boucot and Poinar. bryozoans. pits. 2010). ridges and crests. it is imperative to investigate interactions where the actions of the parasite induced a growth reaction by the host. near the ligament in Pliocene Isognomon (Hippochaeta) maxillatus from Northwestern Italy. amenable to study in deep time via the fossil record of bivalve hosts. which results in the induction of characteristic host shell malformations. foraminifera. potentially kleptoparasitic and shell weak- ening. one or more intermediate stages within an invertebrate host (bivalves. Savazzi (1995) hypothesized that these traces were the result of bivalve growth (rather than bioerosion) responding to what was likely a polychaete endoparasite. Mudblisters form when the spionid begins boring at the growing margin of the bivalve. 1990. Ozanne and Harries (2002) suggested that the traces were the result of pathogens or parasites between the mantle and shell wall and parasitic polychaetes. Trematodes can cause all . Similar blister and tube-like traces of unknown origin have been docu- mented in the fossil record (Boucot. gastropods. spionid polychaetes in the form of mudblisters. barnacles. we cannot always say with certainty that such traces were produced on live bivalves in the past. There is a parasiteehost interaction that has been comparatively well- studied in modern ecosystems.

immobilization and induced risky behaviour (Swennen.. the fossil record of trematode-induced malformations has garnered more attention due to the increasing recognition of its potential for revealing the ecological and evolutionary implications of parasiteehost interactions in deep time and amongst modern death assemblages (Ituarte et al. 2011. stunted growth. 2014). more continuous fossilization potential. For nearly two decades this initial study stood alone in its attempt to document trematodeebivalve interactions in deep time. high temporal reso- lution records of Holocene trematode malformations provide unique in- sights into the influence of climate change on parasitic interactions through geologic time and enable us to make predictions for how such in- teractions will potentially respond to anthropogenic climate change in the future (Huntley et al. 2012. The purpose of this paper is to review our current state of knowledge of the fossil record of trematodeebivalve interactions and to outline prospects for future inquiry. This includes discussions of the morphologies of gymno- phallid trematode-induced malformations in bivalves. Ruiz and colleagues (Ruiz and Lindberg. 1969... De Baets et al. when it is serving as a second intermediate host. 2015b). gigantism. expanded to the North American Atlantic coast by the Miocene. gymnophallid trematodes are known to induce the growth of an array of shell malformations on the interior of the bivalve. 2009). 2015. of course. 2005. highly preliminary and warrant further study to determine the timing of the origin and dispersal of this interaction. 2003. Ruiz and Lindberg (1989) hypothesized that the gymnophallid-bivalve parasiteehost interaction originated in Europe during the Eocene.. the . Lim and Green. 1991) docu- mented a 5-million-year history of parasitism amongst bivalves of North America and identified the oldest known occurrences of gymnophallid trematode-induced pits in three genera from the Eocene (Lutetian) strata of the Paris Basin (a record that was recently extended to an even earlier Age of the Eocene (Ypresian) by Todd and Harper (2011) from the London Clay of southern England). De Baets et al.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 205 manner of trouble in their bivalve hosts including castration. Huntley and Scarponi. 2001. Ruiz. These results are. 1989. The soft-bodied trematodes themselves have very low body fossilization potential (Poinar. which have a greater. Todd and Harper. Ballabeni. Hechinger et al. however. 2007. within the pallial line (the best known being oval pits with raised rims). 1995. Huntley. 1991. Recently. 2015b). examples of living par- asites in close proximity to malformations in the shells of their hosts. 1998.. and again to the North American Pacific coast by the Plio- cene. 2003. Taskinen. Littlewood and Donovan. Indeed.

Pits are the traces most frequently cited as fossil indicators of trematode parasitism (Ruiz and Lindberg.206 John Warren Huntley and Kenneth De Baets temporal distribution of reliable trematode traces within the phylogenetic context of their bivalve intermediate hosts. Semelidae. 2008). irregular calcareous deposits (ICD) and valve discolouration (Table 1). Ituarte et al. many more questions about the origin and history of this interaction present themselves. problems of taphonomy and how they influence our understanding of the origin and history of trema- todeebivalve interactions. Though gymnophallids are typically considered to be the digeneans respon- sible for inducing pit growth in their hosts. Ruiz and Lindberg (1989) suggested that these pits are not features of shell erosion. .. Ituarte et al. TREMATODE-INDUCED SHELL MALFORMATIONS IN LIVING BIVALVE MOLLUSCS Live digenean (mostly gymnophallid) trematodes have been found living in close spatial proximity to shell malformations on the interior of their bivalve hosts. These malformations have taken a variety of forms. the utility of trematode traces as palaeoenviron- mental indicators and the negative effects of trematodes on bivalves and their likely evolutionary implications. Johannessen. Most trema- tode taxa found living in association with pits are members of the Gymno- phallidae and were parasitizing taxa from the bivalve families Veneridae. The best known characteristic shell malformations induced by trematode parasites are oval-shaped pits with raised rims (Figure 1(a) and (b)). Ranging from the most to the least reliable. Gaimardia trapesina from southern Argentina (Table 1. an unknown species from the digenean family Lepocreadiidae has been found living in association with a pit on the interior of a cyamiid bivalve. Campbell. igloos. rather. 1989. 1989. and these forms span a range of utility for being characteristic traces of trem- atodes (Figure 1). Ruiz and Lindberg. 2001). Indeed. blister pearls. This interpretation is evidenced by growth lines wrapping around the pit structure when viewed in thin section rather than the pit cutting across growth lines (as would be expected with shell erosion). Despite all that we have learnt about this interaction in deep time. 2. the life and feeding modes of infested bivalve taxa through geologic time. free pearls. the pits are the result of shell growth intended to encapsulate the parasite. 1985.. Cardiidae and Psammobiidae (Table 1. indicators of trematode parasitism are pits. there is room for addi- tional palaeontologists and neontologists to address these important (palaeo-) ecological questions. 1973. 2001.

(c) Flatbed scanner image of blister pearls in Eocene (Lutetian) Sunetta semisulcata from the Paris Basin (Grignon. China (Core PRD-10. France (Gg2003/517. (e) Photomicrograph of discolouration that may be related to trematode infestation in Holocene Cyrenodonax formosana from the Pearl River Delta.. Ituarte and colleagues (Ituarte et al. (2005). Huntley. De Baets et al. In this case. sample 120).Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 207 Figure 1 Images of trematode-induced shell malformations. (2001) interpret the igloo structures to represent a response of the host meant to isolate the parasite. Ruiz. 2015. 2012. China (Core PRD-10. 2001.. Faluni ere). sample 157) and (b) Holocene Chamalea gallina from the Po Plain. thus . 2011. Huntley et al. 2015b). (f) Photomicrograph of irregular calcar- eous deposits that may be related to trematode infestation in Holocene C. Italy (Core 240S8. 2014. 13. (d) Scanning electron micrograph of igloo-shaped malformation in Recent Neolepton bennetti from the Falkland Islands (Adapted from Ituarte et al. 2014) have described unusual igloo-shaped morphologies of trematode-induced traces from high-latitude shallow marine deposits in Argentina (Figure 1(d)). Todd and Harper. formosana from the Pearl River Delta. 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.. Museum National d’Histoire Naturelle).). however. Photomicrographs of trematode-induced pits in (a) Holocene Potamocorbula amurensis from the Pearl River Delta. 1991.. and there is no other biotic interaction (known so far) that induces the growth of an oval-shaped pit with a raised rim. sample 124). Huntley and Scarponi. 2007. Ituarte et al.10 m). 2005. Presta et al. China (Core PRD-10.

discolouration. luteum Tellinidae Tellina fabula Deposit Tellina tenuis Tellina solidula Distomum margaritarum Pearls Mytilidae M. (2005) ICD. (2014) Unknown species Cyamiidae Gaimardia trapesina Epifaunal Suspension Ituarte et al. (2001) Gymnophallidae Parvatrema borealis Pits Veneridae Gemma gemma e e Ruiz and Lindberg Transennella confusa Infaunal Suspension (1989) Transennella tantilla ICD ¼ irregular calcareous deposits. discolouration Psammobiidae Tagelus plebius Ituarte et al. trapesina Epifaunal Suspension Ituarte et al. (2001) Lepocreadiidae Unknown species Pits Cyamiidae G. (2008) ICD. discolouration Lomovasky et al. (2006) Bartolius sp. . Pits.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. margaritarum Mytilus galloprovincialis ‘Unknown trematode’ Margaritiferidae Margaritifera margaritifera Proctoeces milfordensis Mytilidae M. pearls Vazquez et al. Blank cells indicate the same content as the above cell and the dashed lines indicate that the value is unknown. edulis Epifaunal Suspension D. pearls. rebecqui Cardiidae Cerastoderma glaucum Suspension Gymnophallus somateriae Pearls Mytilidae Mytilus sp. Igloo Neoleptonidae Neolepton cobbi e e Presta et al. edulis John Warren Huntley and Kenneth De Baets Gymnophallidae Bartolius pierrei ICD Mactridae Darina solenoides Infaunal Suspension Cremonte and Ituarte (2003) Unknown species Pits. discolouration Veneridae Venerupis pullastra Infaunal Suspension Johannessen (1973) Parvatrema rebecqui Pits Semelidae Abra tenuis Deposit Campbell (1985) P. Epifaunal Jameson (1903) e ‘Unknown distome’ Pearls Mytilidae Mytilus edulis Epifaunal Suspension Stunkard and Uzmann Brachycoelium luteum ICD Donacidae Donax trunculus Infaunal (1958) B.

2008). 1985. Free pearls are similar to blister pearls in that they are the result of a bivalve’s defensive overgrowth of foreign bodies. Although various parasitic flatworms have been associated with pearl formation (both blister and free). 2015). 2014). Fossils give a minimum constraint to the origin of modern shore birds or charadriiform-like forms to the Eocene (Mayr. round to elongate. 2014). although these are not consistent with known extant host-relationships between shore birds and gymnophallid trematodes (compare De Baets et al. 2006. 1958. 1903. Gymnophallid trematodes have been found in association with pearl-bearing bivalve individuals from the Mytilidae. Margaritiferidae and the Psammobiidae families in Europe. Liljedahl.. Ituarte et al. 1979. Presta et al. blister pearls are commonly of comparable size to the oval-shaped pits.. Bartolius sp. Free pearls date as far back as the Triassic (Kutassy. Littlewood and Donovan. convex features on the interior surface of bivalves which are sometimes associated with trem- atode parasites (Figure 1(c)). In no instance was the parasite completely isolated by the shell malformation. (2005) extended identified igloo-shaped traces into the subfossil record in Holocene cyamiid. Liljedahl (1985. Conway Morris. Campbell (1985) described shell malformations in the bivalve Abra tenuis reacting against the trematode Gymnophallus rebecqui (termed ‘blisters’ by the author) that are intermediate in morphology between oval pits and blis- ter pearls. Interestingly. although various molecular clocks place the origin of Chara- driiformes into the Cretaceous. 1937. however. although no unequivocal fossils have been found from this interval (Smith. they are not attached to the shell wall. The earliest known blister pearls date from the late Silurian to early Devonian (Kríz. it is important to note that other pathogens and inorganic particles can also . 2003). and nuculanid Holocene bivalves from Falkland Islands and Tierra del Fuego.. and two other gymnophallid species whose genus. When co-occurring with pits.and species-level taxonomy were not resolved have been identified living in igloo-shaped traces on the interior of cyamiid and neoleptonid bivalves (Ituarte et al. 1983). 1981. Stunkard and Uzmann. Vazquez et al. but this morphology serves as further support for the inducing of pearl growth by trematodes. neoleptonid. Ituarte et al. 1994. 2001. Blister pearls are small.. 2015b).. 1994) noted similar traces on the interior of praenuculid bivalves from Silurian strata in Sweden. discrete.. De Baets et al. 2011) and are often thought to repre- sent overgrowths of dead parasites as in recent bivalves (Lauckner.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 209 producing an igloo-morphology. North America and South America (Jameson.

Caceres-Martínez and Vasquez-Yeomans (1999) documented the presence of pearls in Mytilus galloprovincialis and Mytilus californianus with copepods and platyhelminths that also lacked trematodes (though other individuals in the samples possessed various combinations of the three types of parasites and pearls). ICDs or shell discolouration as a direct evidence for trematode infestation in the instance that the interaction is well documented amongst living repre- sentatives or. 1974. Lauckner. Lomovasky et al. 2006. ICDs are similar in morphology to spionid mudblisters except that there is no void space in the valve underlying them. of course. valve discolouration has been identified in association with digenean trematodes in venerid and psammobiid bivalves in Norway and South America (Johannessen. Elston. Vazquez et al. Table 1). 1979. at worst.. Lauckner. Therefore one should use caution when attempting to positively identify trematode parasitism via pearls. Features similar to ICDs and shell discolouration have been identified in Cyrenodonax formosana from core-sampled Holocene de- posits of the Pearl River Delta. 1958). by comparison.. ICD. with closely related taxa. are of a more simple morphology and could potentially be induced by a diverse group of irritants (G€ otting. 1983). 1979. ICDs have been identified in association with Brachycoelium luteum in donacid and tellinid bivalves from France (Stunkard and Uzmann. 1973. 2006. 1908. China (Huntley et al.210 John Warren Huntley and Kenneth De Baets result in pearl formation (Newton. Shell discolouration and ICDs can be linked to a number of parasites including chromalvelolates (Haplosporidium nelsoni) and fungi (Ostracoblabe implexa.. in that they are morphologically complex and no other known organisms induce the growth of such structures today. Cremonte and Ituarte. . 2005. Pits and igloos are the most reliable proxies for gymnophallid trematode infestation in the fossil and subfossil record. as these are subfossil deposits. 2003. No association with trematodes could be confirmed. One should only use blisters. 2014).. 1974. Table 1). 2005. 1983). Additionally. Pits and igloos are highly diagnostic. 1990). G€ otting. and shell discolouration are the poorest diagnostic traces of trematode parasites. and digenean trematodes (Bartolius pierrei and two unidentified species) in mactrid and psammobiid bivalves from Argentina (Cremonte and Ituarte. Lomovasky et al. Blisters. ICD are low-relief malformations occurring in the interior of the shell. 2003. Blister pearls and ICDs. The probability of preserving discolouration likely decreases dramatically with geologic age.. Vazquez et al.

The occurrence of trematode-induced traces was plotted on the evolutionary time tree of the Bivalvia modified from Bieler et al. Workum and Wierum) consisting of 7423 valves from 16 taxa. un- published data). Archihe- terodonta and Imparidentia. unpublished data). temporal and ecological occurrences It is instructive to explore the distribution of gymnophallid trematode infestation across the phylogeny of their bivalve intermediate hosts in deep time. Such a distribution can aid in the development of hypotheses regarding the origin of this interaction and the potential nonbiological (taphonomic) biases upon this record. Table 2). Bulk samples of death assemblages from the swash zone were collected by the senior author at 10 locations in the Netherlands (Callantsoog. The largest temporal gap in evidence for trematode infestation currently exists in the Protobranchia lineage of bivalves. This record is most complete in Eocene and younger sediments and is characterized by significant temporal gaps. Liljedahl (1985) reported an igloo-like trace in the praenuculid Nuculodonta gotlandica from the Silurian of Sweden (compare Liljedahl. (2014) (Figure 2. In the interest of taking the most conservative approach. Egmond Aan Zee. 2014): Protobranchia. igloos and igloo-like structures from fossil and subfossil (Holocene samples from sub-surface deposits and surficial death assemblages) records will be considered in this analysis. This trace is remarkably similar to . museum survey of Eocene (Lutetian) bivalves in the collections of the Museum National d’Histoire Naturelle (MNdHN. Trematode-induced traces have been identified in four of the six major bivalve lineages (Bieler et al. Paris. and from the peer-reviewed literature. only pits.1 Taxonomic. Pteriomorphia. OCCURRENCES OF TREMATODE-INDUCED PITS IN FOSSIL AND SUBFOSSIL BIVALVES 3. Table 2). Huntley. Data are compiled from occurrence data from the North Sea coast of the Netherlands (Huntley. Harlingen. including 46 genera from 19 families (Figure 2.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 211 3. Katwijk Aan Zee. Hoek van Holland. Faluniere. IJmuiden. The two lineages in which trem- atode traces have not yet been identified are Palaeoheterodonta and Anom- alodesmata. The senior author conducted a cursory survey of the extensive Eocene (Lutetian) bi- valves from the Paris Basin in the collections of the MNdHN on lots with multiple specimens (1505 valves from 147 species occurrences) from Grignon.. Makkum. but this might represent a sampling artefact given the dearth of attention this interaction has historically received from palaeontologists. Zandvoort. 1994).

It cannot therefore be ruled out. Note that geologic time is not to scale. Pliocene). the Cenozoic is exaggerated to show more details. trematode-induced igloos (I) and igloo-like (IL) traces on bivalves found in fossil and subfossil death assemblages map- ped onto the evolutionary time tree of Bivalvia (Adapted from Bieler et al.). Temporal units from the oldest to the youngest are Cambrian. Paleogene (Paleocene.. Ordovician. 2015b). Silurian. Significant temporal gaps in the trematode record also . that they are related with other organisms with similar behaviour (De Baets et al. 2015b). the igloo structures described by Ituarte et al. Cretaceous. Quaternary (Pleistocene. the oldest fossil evidence for trematodes and parasitic flatworms in the fossil record (De Baets et al. Triassic. but all members of this family are included within Pteriomorphia. then these would be. 2005). *The family Arcidae is not monophyletic in the analysis of Bieler et al. Oligocene). Jurassic. by far..212 John Warren Huntley and Kenneth De Baets Figure 2 Distribution of trematode-induced pits (P). The Holocene time bin includes both sub-surface Holocene deposits and modern/Ho- locene death assemblages. If Liljedahl’s igloo-like structures are indeed the result of trematode infesta- tion. Devonian. Holocene). more comparative work is required to determine the relatedness of the Silu- rian igloo-like traces and trematode parasites. Carboniferous. (2005) in the nuculanid Yoldia woodwardi from modern death assemblages in Argentina (Ituarte et al. (2014). (2014).. Eocene. Permian. Currently. Neogene (Miocene.

Myidae Mya sp. Mactra stultorum Myidae Mya arenaria Brackish Pharidae Ensis sp. (2005) Neolepton concentricum Nuculanidae Yoldia woodwardi Pits Corbulidae Potamocorbula amurensis Semi-infaunal Suspension Brackish China Holocene Huntley et al. 213 (Continued) . (1989) Tresus sp. (2014) Donacidae D. Marine Tellinidae Macoma balthica Deposit/suspension Marine M. balthica Brackish Angulus tenuis Suspension Marine Cardiidae C. semistriatus Infaunal Suspension Marine Italy Huntley and Scarponi (2012) Donax sp. USA Ruiz and Lindberg Mactridae Mulinia sp. glaucum Italy Huntley and Scarponi Donacidae Donax semistriatus (2015) Lucinidae Loripes lucinalis Chemosymbiotic Mactridae Spisula subtruncata Suspension Mytilidae Mytilus galloprovincialis Epifaunal Veneridae Chamalea gallina Infaunal Igloo Neoleptonidae Neolepton bennetti e e Marine Argentina Modern Ituarte et al.Table 2 Occurrences of trematode-induced traces on fossil and subfossil bivalve death assemblages Bivalve host Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time Trace type Family Species Life mode Feeding mode Environment Country Age Reference Pits Cardiidae Cerastoderma edule Infaunal Suspension Marine Netherlands Modern Huntley NL survey Brackish Cerastoderma glaucum Marine Brackish Donacidae Donax vittatus Marine Mactridae Spisula sp.

e e Marine Argentina Holocene Ituarte et al. Donacidae Donax sp. USA Psephidia sp. Venerupis sp. USA (1989) Rangia sp. Transennella sp. Deposit USA Veneridae Anomalocardia sp. Sweden Igloo Cyamiidae Cyamiomactra sp. Brackish Psammobiidae Sanguinolaria sp. Deposit/suspension England Tellinidae Macoma sp. Canada Sweden Veneridae Ch. Parastarte sp. Transennella sp. Venus sp. Tivela sp. Infaunal Suspension Marine Sweden Pleistocene Ruiz and Lindberg John Warren Huntley and Kenneth De Baets Mulinia sp. Deposit USA Veneridae Cyclinella sp. e Marine Yemen Tellinidae Tellina sp. Sweden Pliocene Tellinidae Tellina sp. Protothaca sp.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. gallina Suspension Italy Huntley and Scarponi (2012) Gemma sp. USA Ruiz and Lindberg (1989) Canada Gouldia sp. (2005) Pits Mactridae Mactra sp. Suspension . Suspension Gemma sp.

Tellinidae Arcopagia sp. 215 . (Venericardia) planicosta Infaunal Suspension Marine France Eocene Huntley MNdHN survey Tellinidae Tellina sinuata Deposit Veneridae Cytheraea (Callista) laevigata Suspension Meretrix (Callista) laevigata Igloo-like Praenuculidae Nuculodonta gotlandica Infaunal Deposit Marine Sweden Silurian Liljedahl (1994) Blank cells indicate the same content as the above cell and the dashed lines indicate that the value is unknown. USA Veneridae Chione sp. Ruiz and Lindberg (1989) Veneridae Sunetta semisulcata Suspension Huntley MNdHN survey Venus sp. Parastarte sp. Ruiz and Lindberg (1989) Blisters Carditidae C. Deposit/suspension France Miocene Macoma sp. Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time Transennella sp. Suspension Gemma sp. Gemma sp. Arcidae Arca (Barbatia) filigrana Epifaunal France Eocene Huntley MNdHN Carditidae Cardita (Venericardia) planicosta Infaunal survey Venericor clarendonensis England Todd and Harper (2011) Glycymeridae Pectunculus (Glycymeris) pulvinatus France Huntley MNdHN survey Lucinidae Corbis lamellosa Chemosymbiotic Lucina caillati Phacoides (Pseudomiltha) caillati Phacoides (Pseudomiltha) giganteus Phacoides concentricus Mactridae Mactra semisulcata Suspension Tellinidae Tellina patellaris Deposit Tellina sp. Venericardia sp.

These results. appreciably more data are available from death and fossil assemblages than from living assemblages. Despite the large number of fam- ilies displaying trematode-induced traces in the Imparidentia. Pits have been identified amongst 12 of these families and igloos have been documented in the Cyamiidae and Neoleptonidae families.216 John Warren Huntley and Kenneth De Baets occur in the oldest of bivalve lineages. Trematode-induced pits have been identified amongst three pteriomorphan families Arcidae (Eocene). should be interpreted with the understanding that much investigation remains to be done. The ecological distribution (i. and Mytilidae (Holocene). tellinid and venerid bivalves from the Eocene-aged deposits (Lutetian) of the Paris Basin (Table 2). the majority of parasite occurrences are from the Pleistocene and Holocene. Semi-infaunal and epifaunal taxa are less well-represented as trematode trace-bearing hosts. life mode and feeding mode of hosts) of trematode-induced malformations in bivalve intermediate hosts is roughly comparable amongst living assemblages and death/fossil assemblages. As sug- gested by Tables 1 and 2. along with much of the other data reported here. This is the only known instance of trematode infes- tation amongst the archiheterodontids. mactrid. .e. Glycymeridae (Eocene). Suspension feeding is the dominant feeding mode of trace-bearing bivalve hosts (both live and dead/fossil) followed by deposit-feeding and chemosymbiotic taxa (the latter only occurring in the dead/fossil assemblages). The majority of the instances of trematode traces have been identified amongst 13 families in the Imparidentia. The oldest noncontroversial evidence for trematode infestation of bi- valves is found in the Archiheterodonta lineage. Amongst these families.. Trematode traces are most commonly found amongst infaunal bivalve hosts. and the seeming lack of trematode traces from the Cambrian to Paleogene Periods might therefore also be partially the result of insufficient sampling to date. 2015b). Todd and Harper (2011) presented clear evidence of trematode-induced pits in the carditid Venericor clarendonensis from the Eocene (Ypresian) London Clay in the UK (compare De Baets et al. Pteriomorphia. the Tellinidae and Veneridae display the most temporally complete fossil record of trematode traces. though this pattern is more strongly expressed in death/fossil assemblages than in living ones (Figure 3). only a few research groups have published one or more papers primarily on trematode malformations in modern and fossil bivalves and a few more groups mention the interaction in passing as a secondary topic. To date. The earliest occurrences of trematode traces in the Imparidentia are pits in lucinid. Fifty million years separate these occurrences.

2 Taphonomy and the origin of the trematodeebivalve parasiteehost interaction Patzkowsky and Holland (2012) argued that the primary problem in palae- ontology is determining to what extent the fossil record can be literally inter- preted as the history of life.. Alroy et al. amongst many . 3. 2000. Peters. 2008. from the death of an organ- ism until it is collected by a palaeontologist. Indeed. 2005. Miller. numerous taphonomic filters introduce bias as organisms pass from the biosphere into the geosphere. strongly influencing the record of biodiversity through deep time (Sepkoski et al..Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 217 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). 1981. Taphonomy is the study of all the processes influencing the production of the fossil record.

or complete in- ternal moulds formed by lithified infilling sediment. Bivalve skeletons are a composite material comprised of calcium carbon- ate crystals (calcite and/or aragonite) and an organic matrix (Rhoads and Lutz. thereby reducing the likelihood of pre- servation of parasite-induced malformations. aragonitic or mixed . and their body fossil record extends to the Cambrian. 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. Anatomical detail is typically lost during recrystallization as the primary aragonitic microstructure recrystallizes into much larger crystals of blocky calcite. and this is no less true for the fossil record of trematodes. Trema- todes are small-bodied metazoans (typically submillimetre in length) that produce neither biominerals nor recalcitrant organic material for skeletons. Trematode pits have been found preserved in positive relief on a Holocene steinkern (Huntley et al. The only means we have to study their occurrence in deep time are their trace fossils (e. Moreover. the biomineralized skeletons of bivalves are much more robust to the taphonomic vagaries of the fossil record than trematodes. Trematodes are amongst the least likely organisms to be preserved as fossils. 2006). 2003.. 2004). and internal moulds are not as likely to display pits as the original shell material. Boucot and Poinar. the characteristic pits and igloos whose growth they induce in their bivalve hosts. 2003.218 John Warren Huntley and Kenneth De Baets others). indeed.. Therefore. De Baets et al.. 1980 and the chapters therein). 2010. Trematode traces are likely to be obliter- ated by the coarse process of recrystallization. 1970). Littlewood and Donovan. Despite the robust nature of the fossil record of bivalves (compared with other taxa). in many cases steinkerns are comprised of sediment whose grain size is similar to or larger than the millimetre-scale trematode pits. The calcite polymorph is more stable under temperature and pressure conditions at Earth’s surface than aragonite. 2014) and blister pearls can potentially also be traced further back in time (cf. Fortunately. however. Littlewood. 2011). it is still subject to significant taphonomic biases. Specimens whose aragonite dissolves can sometimes be preserved as steinkerns.g. they have little to no body fossil record (Ruiz and Lindberg. Indeed. Littlewood and Donovan. 2015b). 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. and this factor could likely play a role in diminishing the fossil record of trematode traces. 1989. De Baets et al. aragonite often recrystallizes to calcite or preferentially dissolves dur- ing the processes of sediment lithification and diagenesis.

The earliest reliable indicator of trematode infestation of bivalves is in the Ypresian stage of the Eocene (V. 2009). one could only collect data from specimens with exposed interiors that are free from encrusting epibionts and lithified sediments. The roots in deep time for both host and parasite coupled with the diverse array of host taxa already parasitized in the Eocene seem to suggest an earlier origin for the interaction. 1980) and putative parasitic flatworm re- mains are known from the late Paleozoic (Zangerl and Case. 2001. De Baets et al. 2015b). Bivalve molluscs first appear in the early Cambrian (Jell. gas- tropods and polychaetes as either first or second intermediate hosts is a derived state that has evolved multiple times. The temporally disparate distribution of both aragonite preservation and lithified sediment are likely to be contributing explanations for our current understanding of the temporal distribution of trematode traces. Indeed. In rocks older than the Cretaceous. De Baets et al. dissolution of carbonate rock with acid to extract silicified bivalves). Furthermore. clarendonensis... Since trematode-induced malformations are restricted to the interior of the valve. The nature of the sediment in which bivalve taxa are preserved can poten- tially bias our ability to properly interpret the fossil record as well (Hendy. 2015b).g.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 219 aragonite/calcite taxa likely have a lower preservation potential in deep time. and marine shore birds are the . Perhaps the search for the origination of trematodeebivalve parasiteehost interaction should proceed from the perspective of the definitive host rather than the intermediate host. 2011. 1976. 2015b). Dentzien-Dias et al. Todd and Harper. phylogenetic analyses suggest that the adoption of bivalves.. Unless one uses time- intensive physical and. Upeniece. Geologically younger sedimentary layers are often unlithified which allows for the easy extraction of whole bivalve valves. De Baets et al. 2003). then ob- servations are restricted to specimens exposed on the surface of rock slabs. it is rare to find unlithified sediments. in some cases chemical (e.. 1999.. thereby reducing the preservation potential of the parasitic traces they harboured in life. extraction techniques. 2006. 2013. molecular clocks place the origin of bivalves as early as the Pre- cambrian and current parasiteehost extrapolations place the origin of parasitic flatworms (Neodermata) in the CambrianeOrdovician (Littlewood. but it is not unreasonable to hypothesize that the interaction between these two groups originated much earlier in time. the traces were induced by the Gymnophallidae (Table 1). In nearly all documented cases of trem- atodes found in association with traces in living bivalves. 2011. The ancestral digenean life cycle has fewer stages and is strongly linked with marine teleost fishes as vertebrate definitive hosts (Cribb et al.

a regression analysis allowed for the calculation of depth values for the samples. and calibrating this gradient using the modern depth preferences of 24 of the most common extant genera in the samples. . 2006). 2015). Since the ordination scores for taxa were strongly correlated with preferred depth. Trematode-infested species occurrences were restricted to between 7 and 9 m depth. been addressed amongst living molluscan communities. DCA was particularly use- ful in this case because it provides ordination scores for taxa and samples. Water depth for the examined samples ranged from 0 to 14 m depth.3 Trematode-induced malformations as palaeoenvironmental indicators Ruiz and Lindberg (1989) suggested that traces of trematodeebivalve inter- action should serve as precise palaeoenvironmental indicators of intertidal en- vironments. identifying a primary environmental gradient related to depth. the infested bivalve second intermediate hosts should occur in depths shallow enough for the birds to prey upon the bi- valves. Scarponi and Kowalewski (2004) provided the environ- mental context for these 89 samples from three cores comprised of 98 genera and over 23. Huntley and Scarponi (2012) were able to approach the question of trematode depth distribution quantita- tively using PleistoceneeHolocene molluscan assemblages from the Po Plain of Northern Italy. This. Smith. 1995.220 John Warren Huntley and Kenneth De Baets definitive hosts for gymnophallid trematodes (Ching. but has received more attention in the fossil record. The depth distribution of trematode malformations has not. in turn.000 molluscan specimens by conducting a detrended correspon- dence analysis (DCA).. though this does not preclude the possibility that trematodes infested closely related and/or ecologically similar predecessors of modern shore birds (compare De Baets et al. 1989. 3. allowed for a refined and independent interpretation of the sea- level curve from these samples to complement the one derived from sedimen- tary and stratigraphic analysis. Galaktionov. 2014. 2015b for a review). Mayr. to our knowledge. Given that marine shore birds are the typical definitive host of gymnophallid trematodes. This association would suggest that the origin of the modern trematodeebivalve interactions might be linked to the origin and radiation of marine shore birds somewhere between the Cretaceous and the middle Eocene (Ruiz and Lindberg. contrary to the prediction of Ruiz and Lindberg (1989) that pits would be a reliable in- dicator of intertidal environments. Huntley and Scarponi (2012) examined the same samples for trematode-induced malformations and were able to quantify the distribution of parasitism along the depth gradient (Figure 4).

In a follow-up study. beyond its . Grey columns are noninfested species occurrences and black columns are trematode-infested species occurrences. 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). 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. nearly absent in the vicinity of the delta and returned to higher values much further south of the delta. North of the Po River Delta. but.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 221 Figure 4 Frequency of Holocene bivalve species occurrences along a water depth gradient from the Po Plain of Italy. of course. 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. Adapted from Huntley and Scarponi (2012). As predicted. it is very difficult to disentangle the numerous abiotic and biotic variables that change with sea-level cycles. This influence wanes with distance to the south and is virtually absent to the north of the delta. conditions are very much like that during Holocene transgression with bar- rier island/lagoon/estuary complexes. trematode prevalence values amongst modern death assemblages were high at north of the delta. Conversely. 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.

They were able to rule out changing salinity and host availabil- ity as driving factors of trematode prevalence. altered behaviour making the host more susceptible to . (2014) documented extensive evidence for trematode parasitism of the estuarine bivalve Potamocorbula amurensis in the Pearl River estuarine/deltaic deposits in China over the last 9600 years.222 John Warren Huntley and Kenneth De Baets influence (Huntley and Scarponi. interpretable patterns can emerge. Trematode-induced malformations may not always indicate intertidal environments. in some cases. Specifically. but were not yet able to address other environmental factors like temperature and nutrient availabil- ity (see Cheng and Combes. Responses of these environmental vari- ables may be linear or nonlinear and their influence on the biota (e. it is important that we are able to un- derstand the mechanics driving the increase in prevalence. modified growth rates. For this reason. This especially seems to be the case when dealing with ecological time scales. one finds hints of a previously unobserved modern macroecological pattern that was predicted from palaeontological data. ranging across environment (estuary vs marine). 1990 for a review on environmental factors influencing the invasion of molluscs by parasites). In these three case studies. however. Additionally. As sea level rises and falls on the time scales of millennia. time (Pleistocene. in documenting a predictable biotic response to sea-level change and in understanding the underlying driving factors. Huntley et al. 2014). but their prevalence values do seem to be systematically elevated during times of sea-level rise. Holo- cene and Recent) and geography (northern Italy and southern China). 2012). Huntley et al.g. (2014) demon- strated that trematode prevalence was significantly higher during the first 300 years of sea-level rise than during any other phase of sea-level rise and delta progradation (relative sea-level fall) during the Holocene in the Pearl River Delta. of course.. many biotic and abiotic factors change as well (Patzkowsky and Holland. immobilization and. There is a difference. which are miniscule in comparison to geologic time. 2015). as illustrated in these case studies. a pattern which may have dire consequences for future gener- ations in the context of anthropogenic climate change and sea-level rise (Huntley et al. DETRIMENTAL EFFECTS OF TREMATODES ON LIVING BIVALVES AND THEIR POTENTIAL EVOLUTIONARY IMPLICATIONS Trematodes are known to negatively affect their (mollusc) hosts in a number of ways including castration. the first intermediate hosts and the definitive hosts) can seem to be unpredictable. 4.

1984. Thieltges (2006) attrib- uted these differences to tissue disruptions. but gigantism is likely either (1) a nonadaptive response to parasitism wherein energy is diverted into growth that would otherwise be spent on reproduction. The exact mechanism causing these changes in growth rate is not always clear. 1983. 1987) demonstrated how parasitic castration of first intermediate gastropod hosts was nearly always fatal (not so in second intermediate hosts). Taskinen (1998) reported a density-dependent negative correlation between parasite prevalence and bivalve growth rates. It is clear that trematodes influence the growth rates of their hosts in modern settings. Ballabeni. Trematodes affect the growth rates of their molluscan intermediate hosts in various ways (Sousa. 1991. Bivalves typically serve as the second intermedi- ate host for trematodes (the stage during which trematodes induce pits) and occasionally as the first intermediate host (the castrating stage). so perhaps we should not expect the same effects on bivalves as experienced by gastropods. but do these physiological responses scale up to evolu- tionary changes in life history within lineages or are they merely expressed at the scale of the individual? One would predict from life history theory that . 1987).. 1998). 1998) and stunted growth (Lafferty. the stage during which trematodes are parasitic castrators. These negative impacts on individ- uals scale up to influence population dynamics. Hechinger et al. In a field-based experiment with freshwater Anodonta piscinalis bivalves from Finland. hampered ability of the bivalve to ingest food particles and the growth of metacercarial cysts within the host. 1998. Trematode infestation also contributed to host mortality by making individuals more susceptible to environmental stressors (Lauckner. particularly short-living freshwater species. Most studies have addressed the effects of trematodes on the growth rates of gastropods as first intermediate hosts. targeted larger post-spawning individuals and resulted in a seasonal reduction in mean body size giving the appearance of negative growth. Thieltges (2006) demonstrated stunted growth rates in parasitized North Sea Mytilus edulis relative to their nonparasitized counterparts.b) have both been documented in numerous gastropod taxa. and are. Lauckner’s work with larval digeneans on North Sea tidal flats (1984. 1993a. Taskinen. 2001 and references therein). expected to be significant agents of natural selection. Sorensen and Minchella. 2009). Similarly. 1969. Gigantism (Sorensen and Minchella. Lim and Green.Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 223 predation (Swennen. Much less attention has been given to the influence of trematode parasites on bivalve host life history. 1995. (2) an adaptation of the host to outlive the parasite or (3) an adaptation of the parasite to increase the fitness of the host thereby increasing its own fitness (Taskinen. therefore.

However. 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. 1986. it is possible to estimate the actual temperature of the sea water (Grossman and Ku. 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. 1989. 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. these data suggest reduced growth in year two and an overall trend of increasing tem- perature during the three years. In addi- tion to providing an internal chronology for this individual clam. Moreover. The cycles are inter- preted as three annual cycles and the sharp troughs likely represent growth cessation in the winter. 1989). This specimen was live-collected and sacrificed in February 2010.. Following this methodology. 1998. amongst others). reported in per mil. this interpretation was based upon sizeeage rela- tionships that need to be confirmed as consistent through geologic time. 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. Goodwin et al.224 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. a significant decrease in growth rate often indicates the onset of sexual maturity of marine inver- tebrates (Romanek and Grossman. therefore. 1986). As an example. it is possible to determine the calendar years that correspond to these annual cycles. if we can estimate the d18O value of the sea water in which this clam grew. 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. Kirby et al. 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. Moreover.. Romanek and Grossman. 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 . often an inverse proxy for temperature) values of bivalve carbonate along the axis of maximum growth. 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. 2001..

Igloo-like structures have been found in Silurian Protobranchia. trematode parasitism on the life history of hosts through geologic time and should be a fruitful avenue for future research. CONCLUDING REMARKS There is an increasing interest in elucidating parasiteebivalve interac- tions through deep time. in terms of geologic time that is. induce the growth of a number of characteristic malformations on the interior shell walls of their bivalve hosts. 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.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). Large gaps in the fossil record of such structures might potentially . which can be traced back in the fossil record. 2015b). though lacking a continuous body fossil record. in seven families from three lineages). Trematodes. 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. 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. Gymnophallid trematodes living in close association with malformations on the interior of living bivalves have been well-docu- mented. 5.

Ecol. Shannon Haynes. Franz T. 1995. Funding for this proj- ect was generously provided by the Alexander von Humboldt Stiftung (Renewed Research Stay Grant. many questions remain unanswered and some have not even yet been asked. JWH) and the University of Missouri Research Council (SRF-14-019. 2010. P. Though the efforts of many palaeobiologists and neontologists have greatly expanded our understanding of parasiteehost interactions amongst trema- todes and bivalves. rather a combination of taphonomic biases and too few people looking for these traces likely mask a much older origin. ACKNOWLEDGEMENTS John Huntley is grateful to Kenneth De Baets and Tim Littlewood for the invitation to contribute to this volume. JWH). 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. A pattern of significantly increased prevalence values in transgressive settings (sea-level rise) seems to be emerging from marine and estuarine settings spaced widely in space and time. Trematodes are known to influence the growth rates of their intermediate hosts in various ways. a relationship which suggests that trematode prevalence will in- crease in estuarine settings in the coming decades and centuries in the context of anthropogenic climate change and sea-level rise. Fieldwork was made possible by a generous Ford Ka grant from the Corey and Heather Long Foundation (JWH). Boucot and Poinar.. but the long-term evolutionary implications of this negative effect can only be tested in the fossil record through the establishment of ‘in- ternal chronologies’ within individuals from lineages through deep time. Royal Netherlands Institute for Sea Research) for their thoughtful and constructive suggestions that improved this manuscript. J.226 John Warren Huntley and Kenneth De Baets indicate that a different culprit (e. Funding to conduct these analyses was generously provided by the Keller Opportunities for Excellence Fund of the Department of Geological Sciences. 2008. The sudden appearance of trematode traces in the Eocene probably does not reflect the origin of the interaction. Jesse Broce. 97e100.. Phanerozoic trends in the global diversity of ma- rine invertebrates. F€ ursich kindly encouraged and enabled the exploratory fieldwork of the senior author that led to this line of inquiry. University of Missouri. Parasite-induced gigantism in a snail: a host adaptation? Funct. 887e893. Daniele Scarponi (Universita di Bologna) and Paola De Muro kindly prepared the Primi Piatti bivalve sample. Page Quinton and Tara Selly). . p. Stable isotope samples were collected and analyzed by Ken MacLeod’s Methods in Paleoclimatology class at the University of Missouri (Claire Beaudoin. et al. We thank reviewers Michelle Casey (University of Kansas) and David Thieltges (NIOZ. Science 321.. Ballabeni. (and 33 co-authors).g. parasite) is involved in older occurrences (cf. 9. REFERENCES Alroy. 28).

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com Contents 1.2 Copepods in echinoderms 252 3. Crustaceans as Hosts of Parasites 236 2. Volume 90 © 2015 Elsevier Ltd.1 Fossil evidence 236 2.3.3.1016/bs.2 Equivocal fossil evidence 246 2.4 Gall crabs (Cryptochiridae) in corals 259 3.3. CHAPTER SIX Fossil Crustaceans as Parasites and Hosts Adiël A.001 All rights reserved.1 Ascothoracidan barnacles in invertebrates 249 3. Geoff A. USA x Department of Life Sciences.3 Copepods in fish 253 3.3 Modern evidence only 269 3.1.2.5 Pentastomida 261 3.2 Rhizocephalan barnacles in decapod crustaceans 244 2.2.1.5 Facetotecta 271 3.3.org/10.3 Modern evidence only 246 2. Introduction 234 2. London.7 Malacostraca 272 Advances in Parasitology.1 Non-crustacean parasites 246 2. Natural History Museum.3 Platyhelminthes in crustaceans 246 2.1.1.2 Tantulocarida 270 3.doi.3.2 Crustacean parasites 247 3. 233 .3 Branchiura 270 3.3.1.1.2.1 Isopod parasites in decapod crustaceans 236 2. UK 1 Corresponding author: E-mail: adielklompmaker@gmail. FL. Klompmaker*.3.apar.2.1 Fossil evidence 249 3.2. Crustaceans as Parasites of Non-crustacean Hosts 249 3.1 Copepods 269 3.2015.3 Isopods (Cymothooidea) in fishes and squids 267 3. 1.3.1. j ISSN 0065-308X http://dx.3. Gainesville. University of Florida.1 Ciliates on ostracods 246 2. Boxshallx *Florida Museum of Natural History.4 Ostracoda 271 3.1.2 Barnacles (Pyrgomatidae) in corals 266 3.2 Equivocal fossil evidence 265 3.06.4 Crabs (Trapeziidae) and corals 269 3.1 Barnacle borings attributed to Acrothoracica in marine invertebrates 265 3.6 Thoracica 272 3.

but have not yet been recognized in the fossil record. Parasitism can be further confirmed when the parasites themselves are preserved. 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. parasitic crustaceans use representatives from many metazoan phyla as hosts. one dating back to the Cambrian. Rohde. 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. but insight can be generated by integrating data on fossils with molecular studies on modern parasites. Crustaceans also serve as hosts to a rich diversity of parasites. as well as to pro- blems with ascribing traces to parasitism with certainty. Indeed. Conway Morris. Tapanila. such as reduced growth. with only 11 examples. This may be due to the limited preservation potential and small size of parasites. In modern marine ecosystems. Little attention has yet been paid to the origin of parasitism in deep time. 1990. inquilinism and parasitism. Darrell and Taylor (1993) concluded that the terms parasitism. commensalism.234 Adiël A. including other crustaceans. 1980. It is espe- cially difficult when dealing with fossils. Overview Fossil Evidence and Future Research 273 Acknowledgements 276 References 277 Abstract Numerous crustacean lineages have independently moved into parasitism as a mode of life. Here. In this chapter. Discerning the precise nature of a close symbiotic association between two species can be problematic. In addition. Klompmaker and Geoff A. Although the confirmed stratigraphic ranges are limited for nearly every example. and to a lack of targeted research. Surface scars caused by the attachment of sessile . 2011). for similar definitions). phoresis. 2005. 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. there are other traces left by parasites that could fossilize. see also Kinne. we show that the fossil record of such parasitic inter- actions is sparse. even when studying living organisms. INTRODUCTION Crustaceans can enter into a wide variety of interspecific associations including mutualism. by analogy with related living taxa or (2) by the presence of cysts or swellings that were inhabited by parasites. 1. mutualism and especially commensalism should be used with caution or avoided altogether (compare Zapalski. when considering fossil symbiotic associations. Boxshall 4. 2008a.

Christoffersen and De Assis.g. for example. 2010.. fossils of whale barnacles such as Coronula are known (e. but again.Fossil Crustaceans as Parasites and Hosts 235 barnacles to the plastron and skull of turtles are known from the fossil record (Hayashi et al. 2014). in parasites of humans such as Guinea worm (Dracunculus) and fish tapeworm (Diphyllobothrium latum). 1988).. Okawachi et al. Xenocarida and Hexapoda.. therefore. Williams and Boyko. 2012) and dige- nean trematodes (e.g. 1976). We follow a recent sys- tematic review of the arthropods (Regier et al. Lester. fishes. including tunicates. Crustaceans also serve as intermediate or definitive hosts to an enormous range of parasites. 2005. the Branchiura (e. including protists (e. 2013). monogeneans (e. Glenner and Hebsgaard. 2005. The Oligostraca contains two main parasitic linea- ges.. B€ ockeler. acanthocephalans (e. the crustacean serves as an intermediate host as. 2013). but modern turtle barnacles are not treated as parasites. 2006. 2005a) and Pentastomida (e. but evidence of crustaceans serving as hosts for parasites.. cestodes (e. Pérez-Losada et al. nematodes (e. Oligostraca. 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. McClelland. Rhizocephala. Thoracica) (e. reptiles and mammals. Boxshall. within a monophyletic Pancrustacea.g. 2005) or Isopoda (e. The Vericrustacea contains a far greater diversity of parasitic forms within the sublineage Multicrustacea including the wholly parasitic Tantulocarida (e. 2010) that recognized four main lineages.g. Taraschewski. or . 2002).. 2005c) and Malacostraca. Rees et al. these are non-parasitic epibionts and are not the focus of this chapter.g. Giribet and Edgecombe.g. 2013). The hosts used by parasitic crustaceans include representatives of many aquatic metazoan phyla. 2005b) as well as numerous parasitic lineages within the subclasses Thecostraca (e. Hayashi et al. 2004. Within the Malacostraca. Copepoda (Boxshall. from sponges and cnidarians to chordates.g. but it is not nutritionally dependent on the host as it still uses its modi- fied thoracic limbs for suspension feeding.g. 2012). The classification of the Crustacea is in a state of flux. Crustaceans have an extensive fossil record stretching throughout the Phanerozoic. 2005).g. Similarly. Boxshall.g. Cribb.g. In the great majority of platyhelminthecrustacean associations. 2000). 2013). Such an association is a phoresis in which the barnacle is transported by the host. although it is now widely accepted that the Hexapoda emerged from within the Crustacea and. that the traditional Crustacea is a paraphyletic taxon (see Edgecombe.g. both of which use freshwater copepods as intermediate hosts. and even other crustaceans. Asco- thoracida.g. Dollfus. Vericrustacea. Levine. the majority of parasitic forms are pe- racarids belonging to the Amphipoda (L€ utzen.

1 Isopod parasites in decapod crustaceans 2. Roccatagliata and Lovrich. Table 1). USA (UF). Oertijdmuseum De Groene Poort. 2004. 2009).1. Adult females release epicaridium larvae that locate . Denmark (MGUH).2 Life cycle and parasitism Decapod crustaceans are not the only hosts for bopyroids as life cycles typi- cally involve two hosts.1 Fossil evidence 2. Geological Museum.1. Natural History Museum of Denmark. 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. CRUSTACEANS AS HOSTS OF PARASITES 2. University of Florida. McDermott. Dumbauld et al. Table 3) found that a total of 3. 2015. but Boyko and Williams (2009) raised this value to 4. Markham (1986. respectively) compared to Brachyura (only 1. Cericola and Williams.1 Modern evidence Many modern decapod species exhibit a swelling in the branchial region caused by a parasitic bopyroid isopod.1.7% and 12. 2008. 1991.. Preva- lence rates for bopyroids on decapod hosts are typically <30% (e. 2.. 2. The Netherlands (MAB k). Body fossils of the para- sites themselves are particularly rare.9%. Boxtel. We also explore what molecular clock studies reveal concerning the stratigraphic range over which such parasitic interac- tions involving crustaceans may have occurred. Gonzalez and Acu~ na. 2011). 1999. The Caridea and Anomura both have relatively high infestation rates (12.200 instead of 7863 species). Rayner.0%. Klompmaker and Geoff A. provide a brief overview of exclusively modern examples and discuss the potential of finding their traces in the fossil record. but rates may increase to 94% of specimens of a population in the case of invasive bopyroids on naïve hosts (Smith et al. 2011. Boxshall exhibiting a parasitic mode of life is relatively rare. Denmark (OESM).g.1. 1985.3%) (Boyko and Williams. based on more com- plete data (w12. Faxe.6% of species in various decapod clades were infested. Institutional abbreviations: Geomuseum Faxe. Gainesville.1.236 Adiël A. Florida. Dumbauld et al. Florida Museum of Natural History. Vienna. Austria (NHMW). Uni- versity of Copenhagen. 1935.. O’Brien and Van Wyk. we aim to discuss the fossil evidence of crustaceans as parasites and hosts. In this chapter. Naturhistorisches Museum Wien.

After an extended period on the copepod host. modification of secondary sex characters and distortion of the epipodites (e. Boyko and Williams. The effects of larval parasitism on the copepod hosts are not well known.. by far. the lack of body fossil evidence and the fact that other isopods may also cause swellings in the branchial region.3 Fossil record The fossil record of bopyroids is non-existent: no body fossils are known. 2. Klompmaker et al. They listed 88 host species. Haemo- lymph is also the source of nutrition for larvae on the copepod host (Boyko and Williams. the best known example of parasitism in or by crustaceans from the fossil record. dating back to the Jurassic (e. and moult into a microniscus larva.g. given the ancient age of such swellings. Beck. Wienberg Rasmussen et al. Gonzalez and Acu~ na.. (2008) referred to them as bopyriform swellings. 2004. Boyko and Williams (2009) even specu- lated that members of the Ioninae may have caused swellings in fossil crabs. however. 2012). 1982. to which three . develops into an adult female. 1991. Given the close morphological similarity to swellings induced by bopyrids in modern decapods. expressed some doubt that these are all caused by bopyrids. Williams and Boyko. In addition to nutrients. 1969.. 2012) using their mandibles to pierce the inner cuticle (Bursey. but may include reduced growth rate and a decrease in swimming efficiency. 2009). Hernaez et al.1. 2014). Bopyroid females feed on haemolymph or ovarian fluids of the host (Williams and Boyko. These traces are. O’Brien and Van Wyk. However. the microniscus larva trans- forms into a cryptoniscus larva that seeks out the definitive decapod host (Dale and Anderson. Figure 3). Van Wyk. 1951. McDermott. 2009. 1985. These authors referred to them as isopod-induced swel- lings and formalized the name of this embedment structure by erecting the ichnotaxon Kanthyloma crusta. Petric et al.. these soft-bodied parasites also benefit from the shelter that the decapod cuticle provides. 2010. lower fecundity leading to parasitic castration in extreme cases. (2014).1. 2010. This larva attaches to the gills in the branchial chamber or to the abdomen of the decapod. Negative impacts on the decapod host include a reduced growth rate. typically a planktonic calanoid copepod (Baer. Wienberg Rasmussen et al. Hessler. pronounced swellings of the branchial chamber of fossil decapods are well known and widely accepted to represent swellings induced by para- sitic isopods. 1930. and subsequently mates with the smaller adult male. 2008.Fossil Crustaceans as Parasites and Hosts 237 the intermediate host.g. 1980. 1982). Klompmaker et al. 1978). in the case of infestation in the branchial chamber. Tucker.

2012. Fraaije et al. 2013. 2012.. g) Frontal and dorsal views of Cycloprosopon sp. Schweitzer and Feldmann. 2004. Recently. Kanthyloma crusta was previously unknown from G.238 Adiël A. 2013). MGUH 31265. Schneider et al. Austria (e. 2012. UF 252037. MAB k2603.g. Housa and Vasícek.. (c. 1997. from the Upper Jurassic (Tithonian)eLower Cretaceous (Berriassian) part of the Stramberk Formation of the Kotouc quarry. Jakobsen and Collins.g. 1994) and the crab Cristafrons praescientis from the Late Cretaceous (SantonianeMaastrichtian) of Antarctica (Feldmann et al. (a) Galathea strigifera from the lower Palaeocene (Danian) Faxe For- mation of the Faxe quarry.0 mm. crusta in the crab Speo- carcinus berglundi from the late Miocene (Tortonian) of California (Tucker et al. Lauridsen et al. but this record is difficult to confirm in the absence of a figure. Fraaije et al.. New fossil specimens exhibiting K. Klompmaker et al. 2013b. 2013). NHMW 2014/0194/0965. Boxshall further species are added here (see Figure 1) plus K. 2013b.. 2008. Spain (e.. . primaeva and Goniodromites ?dentatus. (2015) mentioned a swelling in the branchial region of the Eocene (Ypresian) squat lobster Acanthogalathea squamosa from Italy. 2013a). 2014). Klompmaker. strigifera. Denmark (e. M. OESM-10059-21721. Robins et al. Beschin et al.g.. d. (f) Juvenile Eodromites grandis from the Late Jurassic (Tithonian) Ernstbrunn Limestone of the Ernstbrunn quarries. NHMW 1990/0041/4646. Czech Republic (e. (d) Munida primaeva from the lower Palaeocene (Danian) Faxe Formation of the Faxe quarry. Denmark. (b) Goniodromites ?dentatus from the Upper Jurassic (Tithonian) Ernstbrunn Limestone of the Ernstbrunn quarries. 2012. Austria. Specimen about same size as (e).. (e) Eomunidopsis navarrensis from the mid-Cretaceous (upper Albian) Eguino Formation of the Koskobilo quarry. 1993) based on evidence from figures. crusta have been reported recently Figure 1 New examples of swellings (ichnotaxon Kanthyloma crusta) attributed to iso- pods in the branchial region of fossil decapod crustaceans including squat lobsters (a. e) and crabs (rest). Klompmaker and Geoff A. Lauridsen and Bjerager.. Scale bars 5. 2011.g.

This can be explained by the lower fossilization potential of shrimps due to their relatively soft exoskeleton. 1990. 1930. but this would be difficult to detect in fossils unless specimens are exquisitely preserved. Beck. 2014). crusta and the percentage of species infested show a peak during the Late Jurassic... Klompmaker et al. but this swelling was probably not caused by a parasitic isopod (Klompmaker et al.Fossil Crustaceans as Parasites and Hosts 239 in taxa from which such swellings were already known (Fraaije.. for Galathea weinfurteri. 2009). although a few data exist on prevalence rates by locality and/or by host taxon (Bachmayer. 1956). Modification of secondary sex characters by epicaridean isopods.1. 2014). 2014). for Gastrosacus wetzleri. 2009). the Late Cretaceous infesta- tion of all species is <5%. These swellings have been found mostly in fossil true crabs (Brachyura) and squat lobsters (Galatheoidea). has been recorded in modern decapods. after which values dropped to stabilize in the Late Cretaceous and Cenozoic. such as feminization of the male chelae in shrimps (e.1.1. Radwa nski. This may suggest that infestation rates comparable to today were already reached in the Late Cretaceous. Housa. highlighting the relatively common occur- rence of such swellings. Both the number of species exhibiting evidence of K. for Cretocoranina testacea). which is comparable to today’s value (see Boyko and Williams. 2. 1972. 2008. Kornecki. The latter authors collected data for all species at a locality by systematically collecting all specimens they encountered..4 Quantitative data per fauna Quantitative data on infestation by isopods are sparse. 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. 1980) and widening of the abdomen in male crabs (Reinhard. Tucker. (2008). 2014. 1963.. evidence of infes- tation of lobsters and shrimps is relatively scarce (Wienberg Rasmussen et al. Boucot..5 Infestation patterns through time Inspired by the initial data set gathered by Wienberg Rasmussen et al. 1955. Interestingly. . Hyzný et al. Klompmaker et al.g. 2008. potentially suggesting host specificity. 2014. They showed that more common species tend to have a higher prevalence rate. 2015). Klompmaker et al. 2.1. 2014. (2014) expanded this data set and figured infes- tation patterns through geologic time (Figure 2). Wienberg Rasmussen et al. despite the common occurrence of isopods in modern shrimps (Boyko and Williams. Only one swelling is known from a shrimp (Franţescu.

. (2014) suggested that the pattern through time is likely to show one or more biological signals rather than being dominated by collecting and reporting biases. Inset shows the percentage of marine decapod.. could the infestation peak in the Late Jurassic be solely explained by reef abundance? This seems unlikely because coral-associated deposits from the Late Cretaceous (Maastrichtian) of the Netherlands did not yield a single specimen exhibiting K.. brachyuran. The peak infestation remains visible. crusta. Larger graph: number of infested marine decapod. galatheoid anomuran and lobster species infested per Jurassic and Cretaceous epoch to circumvent the potential effect that the high species diversity in the Late Jurassic (see Klompmaker et al. isopod-induced swellings in fossil decapod crustaceans (ichnotaxon Kanthyloma crusta) throughout geologic time. Figure 3) showed that most deca- pods were found in reef-associated environments at that time. Figures 5 and 6)) Klompmaker et al. (Modified from Klompmaker et al. Klompmaker and Geoff A. galatheoid anomuran and lobster species standardized per 20 Myr per epoch. Adaptations increasing resistance to infes- tation.240 Adiël A. galatheoids). 2014. 2013a) may have on the pattern. pers. copepod-related changes and/or changes in decapod size through time may have contributed to the observed pattern.g. (2014. AAK). (2013a. which is not surpri- sing given that Klompmaker et al. falls in diversity of infestation-prone groups (e. Boxshall Figure 2 The prevalence of parasitic. brachyuran. Most infested species from the Late Jurassic originate from reef-associated settings. and swellings in decapods in a reef from the Palaeocene (Danian) of Denmark are rare (Klompmaker et al. obs. Given a subsequent decline in the contribution of reef-associated decapods to overall diversity.

Dreyer and W€agele.. 2010.1.. Using three species. based on a phylogeny using morphological and mole- cular evidence (Selden et al. 2014). Thus far. 2013). Early Jurassic and older occurrences are theoretically possible as the two host groups would have been available.g. Jones et al. crusta. Middle Jurassic deposits have not yielded an example of K. crusta originates from Indonesia (although it is disputed).Fossil Crustaceans as Parasites and Hosts 241 2. 2010). (2012) showed that the last common ancestor of the Bopyridae. Some insight may come from related isopods such as the Cymothooidea (e. and this discontinuity adds to the uncertainty surrounding the Early Jurassic record. North America.. Klompmaker et al. Table 3). Figure 12) speculated that cirolanid-like cymothoids feeding on fish evolved to become parasitic on/in fish (Cymothoidae). The only study is based on limited evidence.. Boyko et al.7 Biogeography It is noteworthy that the oldest report of K. 2014). Whether this European peak in the Late Jurassic and Early .1. Thus. New Zealand and Antarctica. The non-parasitic Cirolanidae have an undisputed fossil record into the Middle Jurassic. The Cymothoidae have.1. 2001. whereas all Late Jurassic and Early Cretaceous occurrences are from Europe (Klompmaker et al. Dajidae and Sphaeromatidae (non-parasitic) would root in the Permian.6 Age This type of parasitism in decapods dates back to the Jurassic. 2. 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.. 2014). 2014. A global distribution of this type of parasitism does not occur until the Late Creta- ceous with occurrences in Europe. 2008. and the presence of decapods since the Devonian (e.g. resulting in the radiation of bopyrids. Feldmann and Schweitzer. then no isopod-induced swellings in decapod crustaceans are to be expected from the Palaeozoic. Given the estimated occurrence of calanoid copepods as far back as the Silurian. no fossil record (Smit et al. This radiation may be best expressed in the Late Jurassic (Figure 2). whereas the Cymothoida are known from the Early Triassic (Etter. Gueriau et al. Unfortunately. which may indicate a low preservation potential. although this is only inferred from a drawing (Wienberg Rasmussen et al. possibly the Early Jurassic (Toarcian) based on a lobster.. and also gave rise to the Bopyridae infesting crustacean hosts.. 2014).. Lins et al. Dreyer and W€agele (2001. 2014. no rigorous phylogenetic analyses of epicarideans including estimated divergence times are known to us. however.1.

Boxshall Cretaceous represents a sampling bias remains to be investigated. (2006. The swellings in decapods were classified ichnotaxonomically because as Bertling et al. we advocate nomenclatu- rally (not taxonomically) treating them as if they were ichnotaxa’. p. Table 1) who suggested that pathologies are in a ‘grey zone’ and are ‘non-traces’. Tapanila (2008b). crusta by Klompmaker et al. as such. In his opinion. Bromley et al. the ichnotaxon should not have been erected. p.. p. 2014a).. these represent pathological struc- tures. 2. Bioclaustrations were called trace fossils by Palmer and Wilson (1988) and. (2012) and C onsole-Gonella and Marquillas (2014). 1214) referred preserved embedment pits without evidence of boring to an ichnotaxon (Oichnus). 1978). Donovan (2015) cast doubt on the establishment of the ichno- taxon K.8 On the erection of an ichnotaxon In a note. Knaust (2012). 1999. (2006) were of the opinion that bioclaustrations do not repre- sent trace fossils. by Tapanila and Ekdale (2007). Boring and growth are both of note in this case because the mandibles of isopods bore into the inner cuticle for food extraction from the host resulting in the growth of the parasite today (Bursey.. Hybrid structures caused by parasites have been described ichnotaxonomically (Vinn et al. and.1. crusta as an embedment structure or bioclaustration following Bertling et al. (2014b. (2008). p. ‘for convenience and in order to maintain stability of names with a high ecological meaning. It was not addressed why these swelling do not represent embedment structures. Furthermore. However. Wilson et al. Wilson et al. but many others disagree. We welcome this opportunity to discuss this issue further here. following Bertling et al. (2014) for the branchial swellings exemplified in Figure 1. (2006. (2014) treated K. this peak may not be surprising.1. Santos et al. 267): ‘embedment . McKinney (2009).242 Adiël A. An ichno- taxon name is convenient here and such swellings convey ecological insights into the origin of parasitism in deep time.. Klompmaker et al. Klompmaker et al. Radwa nska and Radwa nski (2005) and Boucot and Poinar (2010) called copepod-induced swellings trace fossils. Figure 10) and the radiation of Brachyura and certain Anomura (Klompmaker et al. Similarly. 268) noted with regard to hybrid structures resulting from borings and growth. (2006. 2014. more recently. 2013a). 12) did not specifically call these swellings (classified as bioclaustrations) trace fossils in view of the ongoing discussion as to whether such embedment structures should be treated as trace fossils. Klompmaker and Geoff A. (2014. Bertling et al. given the abundant reefs in Europe during the Late Jurassic (Kiessling et al.

they represent . p. and he gave examples including the results of a mosquito bite and a gall-maker puncture. In conclusion. Rather. the swellings in the branchial region cannot be considered pathological structures sensu Bertling et al. which represents the cavity of the isopod body. all the types represent internal moulds without cuticle. The direct morphological result of infestation is a slower growth rate (as recorded for modern isopod-infested decapods). which is the direct result of the disease or irritation. (2006). (2014. (2006). Unlike for the swellings described in Bertling et al. not to the cuticle surrounding it. the isopod parasite creates space in the bran- chial chamber in order to grow. Furthermore. citing Bertling et al. crusta. the same: the body is encased by or embedded within the host. Klompmaker et al. The result is. a boring. however. The swel- lings described by Bertling et al. This is very different in K. crusta refers to the (infilled) cavity that was created by the inhabitation of the isopod. but in reverse so that the bulge is formed from the inside of the branchial wall. 13) referred to the cuticle as the substrate (not the embedment structure). Such a swelling represents a gradually formed indentation of the isopod embedding in the substrate (¼ the cuticle of its decapod host). (2006) and referred to in Donovan (2015). a pupal chamber.Fossil Crustaceans as Parasites and Hosts 243 structures in calcareous skeletons that are produced by an actively growing organism around disturbing or irritating objects or living organisms’ because the cuticle of the host continues to grow around the isopod.g. (2006) and cannot be considered a ‘trace of a trace’: they constitute a recognizable trace of the body of the isopod. Indeed. K. This is not a direct expression or result of the disease. or an exit hole etc. 114) made a similar distinction between pathological and parasitic deformities in echinoid tests. they may be named as such’ in referring to an ichnotaxon. but not the swelling it- self. Therefore. but also ‘if they do contain a recogni- zable trace fossil.. or the domicile of the isopod. these swellings represent pathologies. e. 268) ‘swollen tissue and plant reaction tissues may at best be considered ‘traces of traces’ having an original tracemaker. in his opinion. the swellings in decapods do not fit pathological structures as defined in Bertling et al. but is the endpoint of a coevolutionary history of the embedment of one organism within another. faecal pellets. p. (2006) consist (nearly) entirely of animal or plant tissue or carbonate created by the affected organism. whose trace (the puncture) is obli- terated by the induced plant growth’. The latter authors noted that (2006. p. a potentially thickened cuticle and/or feminization of the claws (see above). and they also referred to swellings in the branchial region. Donovan (2015) argued against erecting an ichnotaxon for a swelling because. Radwa nska and Radwa nski (2005.

cumaceans and thoracican barnacles (e. the abdomen appears wider than in males (but narrower than in females). resembling that of a female (O’Brien and Van Wyk. 1985. Høeg et al. O’Brien and Van Wyk. Moreover. This is partly due to the incomplete preser- vation of the majority of decapod specimens (i. Høeg. to a lack of large samples of particular species and perhaps to a lack of study of collections in which feminization might be observed. 1983) confirmed that the ornamentation on the sternum is the same as in males. for additional details). Feldmann (1998) considered that the latter would qualify more likely as a parasitized specimen. Boxshall bioclaustrations or embedment structures. K. 1985) and the major claw of a male may not grow as large. 2005). best expressed in the form of the claws and abdomen (Feldmann. This type of parasitism is well known in modern decapods. 2.1. 1983. Klompmaker and Geoff A. and the granular orna- mentation on the sternum is the same as in males. 1994.e. isopods. 1998.g. Feldmann (1998) described the . the abdomen is of intermediate width and the gonopores are most reminiscent of females (see Bishop. an intersex specimen of the crab Dakoticancer overanus from the Late Cretaceous (Maastrichtian) of South Dakota (USA). and concluded that parasitism was the most likely explanation for the occurrence of the intersex specimens. The discovery of a second conspecific specimen from the same locality (Bishop. feminization of males and a reduced host growth rate. 1995. stomatopods. complete ventral sides are rare). however. Feldmann. but much less is known from the fossil record. This specimen bears female gonopores. 1998). 1998). Some evidence exists. and.244 Adiël A. Infestation by rhizocephalans can cause castration of the decapod host. resembling a female claw (Feldmann. many other researchers also consider bioclaustrations to be trace fossils. Bishop (1974) was the first to recognize a sexually aberrant fossil decapod.2 Rhizocephalan barnacles in decapod crustaceans Most modern rhizocephalan barnacles are parasitic on brachyurans and anomurans. The abdomen of a rhizocephalan- parasitized male decapod may become broader. Takahashi and Matsuura. to the extent that moulting ceases and maximum size is reduced (e.g. Table 1).. Infested females do not adopt male features. but males display female se- condary sexual characters after infestation. Jones (2013) studied the Bishop collection from the same area and found 11 intersex specimens of the same fossil crab. 1998). crusta is consi- dered a valid ichnotaxon. disarticulation. as such. but some infest caridean and axiidean shrimps. The parasite extracts nutrients from the host via an embedded rootlet system that penetrates the host’s internal tissues (see Feldmann.

and a possible rhizocephalan barnacle infested conspe- cific specimen showing feminization of the abdomen and claws. (a) Abdomen of a mature female. Miyashita. from specimens of the crab Tumidocarcinus giganteus from the Miocene of New Zealand (Figure 3). Careful examination of the carapace may show slight deformations in entoniscid-infested crabs (e. (From Feldmann (1998). 1973). but its expression may not Figure 3 Normal female and male specimens of the Miocene crab (Tumidocarcinus giganteus) from New Zealand.Fossil Crustaceans as Parasites and Hosts 245 best preserved examples of this type of parasitism. Figure 3) . be noted that parasitism by epicarideans (including non- bopyroids such as entoniscids) can also result in the feminization of males. 1985). (d) Ventral side of a feminized male. A feminized male showed a broader than usual abdomen and its major claw was more like those of females in terms of size. 91). Scale bars 10 mm. (b) Ventral side of a mature male. 1956. It should. He specifically attributed this to parasitism by rhizocephalan barnacles. p. 1941. including a widening of the abdomen and reduction in claws (Reinhard. so that these infestations can ‘duplicate closely the effects by Rhizocephala’ (Reinhard. (c) Ventral side of a juvenile female. Rasmussen. however. 1956. unlike previous accounts.g. Shields and Kuris.

Given the definition of parasitism used here. but the fact that only a single specimen out of thousands of mysidaceans was reported to contain hooks (Upeniece. Another hook was found close to a Conchostraca (clam shrimp) specimen.3 Modern evidence only 2.3. 2001) may indicate accidental parasitism of these crustaceans at best. For comparison. 2011..1. (2007) and Siveter et al. including microsporidians. 1998. 1994. 2015). 2. Boxshall be obvious (e. Klompmaker and Geoff A.1 Non-crustacean parasites Crustaceans serve as intermediate or definitive hosts to an enormous range of unicellular and metazoan parasites and such infestations can be of economic significance in large-scale commercial aquaculture. Therefore. gaujicus were found. ascribing feminization in fossil crabs to infestation by rhizocephalans is not without uncertainty.3 Platyhelminthes in crustaceans Platyhelminth worms have been reported to infest Late Devonian (Frasnian) fishes from Latvia based on the presence of hooks in 16 specimens of the pla- coderm Asterolepis ornata and in 27 specimens of the acanthodian Lodeacan- thus gaujicus (Upeniece. Two hooks were also found in a crustacean specimen ascribed to the Mysidacea. Boyko and Williams.g. Modern crustaceans can act as hosts of platyhelminthes (e. we do not consider these ciliates parasitic on the ostracods because they were inter- preted to be filter feeding and not nutritionally dependent on their host (see Weitschat and Guhl. Figures 9 and 10). 2005. 2.2. Brockerhoff.g.2 Equivocal fossil evidence 2. Wilkinson et al. 2011) considered the hooks too large relative to the size of this crustacean for it to have been a host. 2. The produc- tion of farmed marine penaeid crustaceans. De Baets et al.1 Ciliates on ostracods Weitschat and Guhl (1994) reported on stalked peritrichid ciliates (Cilio- phora) attached on the inner part of the shell and on the epipodal appendages of ostracods found within an Early Triassic ammonite from Spitsbergen. for example. 2011). . of which 16 and 27 specimens yielded hooks. (2015) referred this association to ectoparasitism.246 Adiël A. but Upeniece (2001. Fredensborg and Poulin. can be adversely impacted by infections with various protists. Shields and Ward. ornata and more than 50 specimens of L. 1999. 2004). 2001. but the inference that it constitutes evidence of parasitism is not convincing. over 300 A.

uses freshwater copepods as an interme- diate host. mysidaceans. amphipods are the commonest intermediate host taxon. Littlewood. Digenetic trematodes are also typically endoparasitic and have similarly complex life cycles involving free-living stages as well as a succes- sion of hosts (Cribb. 2002). 2002. for example. 1993). Similarly. stomatopods and decapods (Dollfus. branchiopods. D. 2. in the brood . but Udonella is hyperparasitic on caligid copepods (Okawachi et al. Crustacean groups known to serve as either first or second intermediate hosts include copepods.. larval Anisakis are found in pelagic crustaceans such as copepods and euphausiaceans that are fed on by larger nekton (fish and squid) that form the diet of the final host. Most of these protist and platyhelminth parasites are microscopic and inhabit the internal organs of their crustacean hosts. 2013). is ingested by benthic cope- pods. 2006). In contrast. The fish tapeworm of humans. barnacles. In marine species. but others such as brachyuran crabs and mysida- ceans are also used (Taraschewski. 2012)... The newly hatched larva of the sealworm Pseudoterranova decipiens. Wey-Fabrizius et al.2 Crustacean parasites Crustaceans are used as hosts by parasitic crustaceans including all members of the Tantulocarida as well as some copepods. Near. The Acanthocephala were once treated as a distinct phylum. most monogeneans are ectoparasites of aquatic vertebrates and have direct life cycles. isopods and cirripedes. the second can often be a crustacean that either consumes the infective cercarial larva or is penetrated by it.g.Fossil Crustaceans as Parasites and Hosts 247 haplosporidians and gregarines (Lightner. 1976). 2005). 2003. the Syndermata (Herlyn et al. While the first intermediate host is usually a mollusk. 2003. Acanthocephalans typically use vertebrates as final hosts.. latum.3. but many use crustaceans as intermediate hosts (e. Cestodes typically use vertebrates as the final host. Weber et al. but they have complex life cycles often involving a succession of two or more intermediate hosts. amphipods or mysidaceans that in turn may be eaten by larger crusta- ceans or small fish before being consumed by the mammalian final host. Various crustaceans serve as hosts to copepods of the family Nicothoidae and it has been suggested that these tiny parasites are egg mimics since they are commonly found in the marsupium of peracarids. but are now considered close relatives of the rotifers within a single phylum. their impact on the host is un- likely to leave a readily recognizable trace should the host be fossilized (see Littlewood and Donovan. Nematodes are highly diverse and numerous parasitic nematodes have heteroxenic life cycles that include crustaceans as hosts (McClelland. 2000). 2013). amphipods.

These free-swimming adults are the mating stages. copepods. although a few other nicothoids that inhabit the bran- chial chambers of their hosts are known to cause swellings or cysts (Boxshall and Lincoln. Infection of modern decapods by members of the Entoniscidae has been reported to cause asymmetrical carapaces (Miyashita. but are non-feeding (Huys et al. 1941. the tantulus attaches to its crustacean host. the tantulus larva that is typically about 100 mm in length. 1987). no examples of fossil crustaceans infested by nicothoids have yet been reported.or endoparasitic. or on the egg mass of decapods (Boxshall and Halsey. 2014). established in 1983 (Boxshall and Lincoln. euphausiaceans. Marine crustaceans including copepods. Examples of this could also be expected from the fossil record (Klompmaker et al. parasites have little discernable impact on the host and no examples of fossil taxa from these groups have been reported as harbouring isopod parasites. This mimicry is presumed to reduce the risk of removal by the host’s grooming behaviour. .. Ostracods. barnacles. Some evidence in the fossil record may be expected for barnacles because Hosie (2008. These egg mimics have little detectable impact on the host. 1983b). mysids and other isopods are all known to serve as hosts to parasitic isopods of the su- perfamily Cryptoniscoidea (e. sheds its post- cephalic trunk and develops into a sac-like asexual female within which develops the next generation of tantulus larvae (Boxshall and Lincoln. however. In the asexual cycle. 2004).. Shields and Kuris. and use an oral stylet to make a single puncture in the host’s cuticle. for ostracods). are minute ectoparasites. Figure 12(a)) showed a cryptoniscoid-induced swelling in the stalk of the modern barna- cle Smilium zancleanum. amphipods. The Tantulocarida. but may be difficult to differen- tiate from swellings caused by bopyroids. These tiny parasites attach externally to their crustacean hosts using an oral disc only a few microns in diameter. Boxshall pouch of myodocopan ostracods. 1993). In the sexual cycle. Vannier and Abe. They are unlikely to be fossilized and cause only a minimal lesion that would be on such a minute scale as to be unrecognizable as of tantu- locaridan origin.g.248 Adiël A. In many cases. Klompmaker and Geoff A. the post-cephalic trunk of the tantulus swells to form a sac within which a single adult male or female develops. while adults may be ecto. 1983a. ostracods and peracarid mala- costracans are hosts to tantulocaridans. 1993. Figure 1(a)). 1985). The life cycle includes an asexual and a sexual cycle that share a free living. The larval stages of cryptoniscoids are often ectoparasitic. infective stage. Such cysts have the potential to be visible on fossils of the hosts. after attaching to the host.

rather. but structures attributed to ascothoracidans have been reported from the fossil record (Figure 4. but ectopa- rasitic on anthozoans. Several ascothoracidans (Ascothorax. He considered it did not represent a true endoparasite deriving its food from the host. but see Grygier and Høeg. Body fossils of these barnacles are unknown. he sug- gested that commensalism or ‘syn€ okie’ (inhabitation of host and taking part in meals of the host sensu K€ orner. 2005). Moyse (1983). scleractinians and antipatha- rians) (e. showed morphologi- cally similar galls on modern octocorals. Many are endoparasitic in the main body cavity of asteroids and echinoids. 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. for example. 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. 1979) was more appropriate. Grygier. Grygier and Høeg. Moyse. zoanthids. Subsequently. 1996. 2011.Fossil Crustaceans as Parasites and Hosts 249 3. presumably by an ascothoracidan. 1983. 2005). crinoids and ophiuroids (references in Krawczy nski and Wilson. However. 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). 2005). 2005).g. Fossils attributed to ascothoracidans have also been found in an echinoid and possibly in a brachiopod.1 Ascothoracidan barnacles in invertebrates These small barnacles (up to 8 mm in size) parasitize a variety of modern marine hosts. CRUSTACEANS AS PARASITES OF NON-CRUSTACEAN HOSTS 3.1. Voigt (1967) found further Late Cretaceous evidence for infestation of octocorals. Madsen and Wolff (1965) described the . Grygier and Høeg (2005) noted that little is known about their feeding behaviour. research on modern ascothoracidans suggests that they are parasitic (see Grygier and Høeg. Table 1). similar to rhizocephalans. but basal forms have piercing and sucking mouthparts while the more transformed genera such as Ulophysema and Dendrogaster employ absorptive feeding. although their photograph (Figure 7(c-1)) does not allow identifi- cation of the parasitic structure.1 Fossil evidence 3. Ulophysema and Dendrogaster) cause castration of their echinoderm hosts (Grygier and Høeg. particularly echinoderms (but not regular echinoids and sea cu- cumbers) and cnidarians (gorgonians.

25.7e25. (e) Possible ascothoracidan infestation (marked) in the brachiopod Moorellina negevensis from the Middle Jurassic (late Callovian) of Israel.2 mm. Krawczy nski and Wilson (2011) described a gall. possibly of ascothoracidan origin. Scale bar (e) 0. ((b) ¼ holo- type of E.250 Adiël A. in a .9 and 26. b. (aed) Galls or cysts (ichnotaxon Endosacculus moltkiae) in the octocoral Moltkia minuta from the Late Cretaceous (Maastrichtian) of the Netherlands (a. ((aed) from Voigt (1959). pl. d) and the Late Cretaceous (Campanian) of Sweden (c). scale bar for others not available.2. Restudy of the specimen is called for. There may be further evidence from echi- noids: Bromley (2004) suspected that the two round holes in an Early Creta- ceous echinoid attributed to boring gastropods by Kier (1981) may be the work of ascothoracidans. Boxshall Figure 4 Growth anomalies in octocorals and a brachiopod attributed to infestation by ascothoracidan barnacles. moltkiae). (e) from Krawczyn ski and Wilson (2011). Figure 2(a)) presence of holes in a Late CretaceousePalaeocene echinoid and attributed them to two specimens of Ulophysema based on similar holes in echinoids produced by modern Ulophysema. Klompmaker and Geoff A.

moltkiae Late Cretaceous If€ o (Schonen). ‘Tr€ ummerkreide’. Sten Jakobsen to AAK. 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. minuta E. Israel * pers. Fossil Crustaceans as Parasites and Hosts Table 1 Structures attributed to ascothoracidan barnacles from the fossil record Host taxon Name cyst/parasite Age Locality and country Stratigraphic unit References Moltkia minuta Endosacculus Late Cretaceous The Netherlands ‘Maastrichter Voigt (1959) (Octocorallia) moltkiae (late Tuffkreide’ Maastrichtian) M. 251 . Voigt (1959) (Octocorallia) (Campanian) Sweden rocks with Actinocamax mamillatus Isis sp. comm. Krawczy nski and (Brachiopoda) (late Callovian) Hamakhtesh lamberti Zone Wilson (2011) Hagadol. Endosacculus (?) Late Cretaceous South Emba. Denmark (1965) (?Maastrichtian eDanian)* Moorellina negevensis e Middle Jurassic Matmor Hills in Matmor Fm.

Calverocherids induce the host to create galls in spines on the adoral surface. Pionodesmotids are rarely reported: more than a century passed between the establishment of the type species and the discovery of a second. Pionodesmotes domhainfharrai- geanus lives within endocysts located in the ambulacral region on the adoral side of the host echinoid’s test (Anton et al. . myzostomid annelids and ascothoracid barnacles (e. Exocysts caused by the asterocherid copepod Cystomyzon dimerum containing multiple openings are formed on modern hydrocorals (Zibrowius.. The hosts of both families are deep-sea echinothuriid echinoids that are atypical sea urchins in having a soft and flexible body. and some representatives of several other families also use echinoderms as hosts. While most of these copepods are ectoparasites.252 Adiël A. Neumann and Hostettler. 2013). Klompmaker and Geoff A. Other. 1968). referred to as the ichnotaxon Castexia douvillei. Richter.2 Copepods in echinoderms Thirteen families of copepods parasitize exclusively echinoderms. 1991. 1981). The gall has one pore located at its distal end. 2013). Halloween pumpkin-mask cysts are also known from fossil crinoids (Radwa nska and Radwa nski. These cysts have a single opening and are not visible externally. members of the Chordeumiidae live within cysts of host origin or within the genital bursae of their ophiuroid hosts and can cause swellings that are visible externally. Mehl et al. Fossil endocysts have not been found yet. The fossil record of these traces has not yet been investigated exhaus- tively given the limited stratigraphic range (Table 1).g. Stock (1968) described the swelling as consisting of loose calcareous material around an ampulla inside which a single copepod is found. have both been suggested to be treatable as trace fossils by Radwa nska and Radwa nski (2005).1. Boxshall brachiopod from the Middle Jurassic of Israel. 1981) (Figure 5). older interpretations of the trace maker of the latter cysts exist including trematodes. 3. Anton et al. 2005). No ascothoracidan-infested brachiopods are known today. and the so-called ‘Halloween pumpkin- mask’ cysts resembling the exocysts in modern hydrocorals (Zibrowius. 1898. Grygier. Two families living on echinoid hosts are known to induce their hosts to form galls. Grygier and Høeg (2005) suggested that galls formed by members of the Petrarcidae (e.. these galls are typically asymmetrical and located near the middle of the spine. 2004). The three species of Calverocheridae form galls in their host’s spines (Stock.g. 1990) could be recognized in fossil scleractinian corals. while the two species of Pionodesmotidae form galls within the test of the host (Bonnier. Also. 1991.. but exocysts on the surface of echinoid tests.

3 Copepods in fish A single species of parasitic copepod from a fish host is known from body fossils: Kabatarina patersoni was recovered from two skulls of an . Figure 11. d) Copepod cyst in the gonopore of an echinoid test of Acrosalenia spinosa from the Middle Jurassic (Bathonian) of Bicqueley. Scale bars unavailable in source articles.8 and 2. (c.Fossil Crustaceans as Parasites and Hosts 253 Figure 5 Examples of Halloween pumpkin-mask cysts (aee) and cysts ascribed to the ichnotaxon Castexia douvillei (fei). 3. (fei) Two cysts in an echinoid test of Collyrites dorsalis from the Middle Jurassic (Callovian) of Mortagne-au-Perche. showing cysts induced by the copepod Cystomyzon dimerum. (fei) from Radwanska and Radwan ski (2005). Orne. whereas the larger one (i) is positioned in an interambulacral column. pl. Lorraine. (e) Three cysts in a crinoid stem of Isocrinus tuberculatus from the Early Jurassic (Sinemurian) of Germany. France. Figure 4. chiefly from Europe.1) A list of echinoderms inferred to be infested by copepods resulting in cysts or swellings is presented in Table 2. b) from Zibrowius (1981). Thus far. are known. b) The modern hydrocoral Stylaster papuensis from Tagula Island. southwest Pacific.4. (c. (a. France. all inferred to be caused by copepod parasites.1. ((a. 1. Smallest cyst (h) located in an ambulacral co- lumn. d) from Radwan ska and Poirot (2010). (e) from sole figure in Weinfurtner (1989). only Jurassic occurrences. Louisiade Archipelago.

Table 2 Echinoderms inferred to be infested by copepods resulting in cysts or swellings Locality and Stratigraphic 254 Host taxon Name cyst Age country unit (if known) References Acrosalenia spinosa Halloween Middle Jurassic Bicqueley. (1991) Adiël A. Caillasse a Anabacia. Hildner (2014) (Echinoidea) pumpkin-mask (Kimmeridgian) Germany e test Paracidaris Halloween Late Jurassic Aargau. Basse. Mehl et al. Caillasses de Basse. spinosa Halloween Middle Jurassic Luc-sur-Mer. Ecarde Poirot (2010) e test France Acrosalenia Halloween Middle Jurassic Calvados. coronata Halloween Late Jurassic Teuchatz Quarry. Klompmaker and Geoff A. (Echinoidea) Germany e test P. Switzerland Birmenstorfer Mehl et al. Mehl et al. coronata Halloween Late Jurassic Obermain-Alb. e test Kimmeridgian) Germany P. 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. Radwa nska and (Echinoidea) pumpkin-mask (early France convergens Poirot (2010) e test Bathonian) Subzone A. (1991) (Echinoidea) pumpkin-mask (middle Oberfranken. Radwa nska and (Echinoidea) pumpkin-mask (late Bathonian) Normandie. (1991) laeviuscula pumpkin-mask (middle Schichten (Echinoidea) Oxfordian) (Argovium) e test . Lorraine. Boxshall coronata pumpkin-mask Kimmeridgian) Oberfranken.

?P. laeviuscula Halloween Late Jurassic Aargau, Switzerland transversarium Zone Zbinden (1991)

Fossil Crustaceans as Parasites and Hosts
(Echinoidea) pumpkin-mask (middle
e test Oxfordian)
Hemicidaris Halloween Late Jurassic Bernese Jura, bimammatum Zone Zbinden (1991)
intermedia pumpkin-mask? (middle Switzerland
(Echinoidea) Oxfordian)
e test
Stomechinus Halloween Late Jurassic Reuchenette, Neumann and
perlatus pumpkin-mask? (Oxfordian) Switzerland Hostettler (2004)
(Echinoidea)
e test
Plegiocidaris Halloween Late Jurassic (late Bielawy Quarry, Radwa
nska and
monilifera pumpkin-mask Oxfordian) Couiavia region, Radwa nski
(Echinoidea) Poland (2005)
e test
Plegiocidaris Halloween Late Jurassic Poitou, France Nicolleau and
crucifera pumpkin-mask (Oxfordian) Vadet (1995)
(Echinoidea)
e test
H. intermedia Halloween Late Jurassic Chasseral-Kette, Mehl et al. (1991)
(Echinoidea) pumpkin-mask (middle Switzerland
e test Oxfordian)
?H. intermedia Halloween Late Jurassic (early Ma1ogoszcz, Holy Upper Oolite Radwa
nska and
(Echinoidea) pumpkin-mask Kimmeridgian) Cross Mountains, Member Radwa nski
e ?test Poland (2005)
P. crucifera e Late Jurassic Near Cze˛ stochowa, Radwa
nska and
(Echinoidea) (middle Poland Radwa nski
e spine Oxfordian) (2005)

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)

Adiël A. Klompmaker and Geoff A. Boxshall
(Echinoidea) (late Callovian) France
e test
C. dorsalis C. douvillei Middle Jurassic Mortagne-au- Radwanska and
(Echinoidea) (late Callovian) Perche, Orne, Radwa nski
e test France (2005)
Collyrites acuta C. douvillei Middle Jurassic Caucasus, Solovyev (1961) and
(Echinoidea) (¼Canceripustula (Callovian) Daghestan and Solovyev and
e test nocens) Turkmenistan Markov (2013)
Collyrites ellipticus C. douvillei Middle Jurassic Wrwsowa Knobby layer Radwanska and
(Echinoidea) (Callovian) (Cze˛ stochowa), Radwa nski
e test Polish Jura, (2005)
Poland

Fossil Crustaceans as Parasites and Hosts
C. ellipticus C. douvillei Middle Jurassic Picrzchno near Knobby layer Radwa nska and
(Echinoidea) (Callovian) Klobuck, Polish Radwa nski
e test Jura, Poland (2005)
C. ellipticus C. douvillei Middle Jurassic Zawiercie, Polish Knobby layer Radwa nska and
(Echinoidea) (Callovian) Jura, Poland Radwa nski
e test (2005)
Cladocyclus None e body fossil Early to Late Serra do Araripe, Santana Formation Cressey and
gardneri (fish) copepod Cretaceous Ceara, Brazil (nodules mostly Patterson (1973)
e gill Kabatarina (Aptian from Romualdo and Cressey and
chambers pattersoni eCenomanian)x Member) Boxshall (1989)
Ventalepis e Late Devonian Pavari site on Ketleri Formation Luksevics et al.
ketleriensis (Famennian) Ciecere River, (2009)
(fish) e scale Latvia
Holoptychius sp. e Late Devonian Pavari site on Ketleri Formation Luksevics et al.
(fish) e scale (Famennian) Ciecere River, (2009)
Latvia
Psammolepis e Middle Devonian J~
oksi (Kalmetum€agi) Gauja Formation Luksevics et al.
venyukovi (fish) (Givetian) locality on Piusa (2009)
e scale River, Estonia
* Infested crinoid species and its age determined using Simms (1989).
x
Stages derived using Martill (2007).

257

258 Adiël A. Klompmaker and Geoff A. Boxshall

actinopterygian fish, Cladocyclus gardneri, which were preserved in calcareous
nodules (Table 2; Figure 6). These originate primarily from the Romualdo
Member of the Santana Formation (Cretaceous: AptianeCenomanian) (see
Martill, 2007) of the Serra do Araripe, Ceara in northern Brazil (Cressey and
Paterson, 1973; Cressey and Boxshall, 1989). It is likely that their environ-
ment was marine. Kabatarina is classified in the family Dichelesthiidae, a fa-
mily that also contains two extant genera of fish parasites, both monotypic
(Boxshall and Halsey, 2004). Kabatarina is the sole fossil representative of
the order Siphonostomatoida.
Fish are by far the most commonly reported hosts for modern parasitic
copepods, with over 2000 species known, and they can have a marked
impact on the host. The feeding activity and attachment mechanisms of
ectoparasitic copepods can cause erosion of the host’s epidermis and stimu-
late tissue proliferation and fibrotic responses in affected host tissues
(Boxshall, 1977, 2005c). Lesions apparent on Devonian fish have been
tentatively attributed to infestation by various parasites, including copepods
(Table 2). Luksevics et al. (2009, p. 342), based on the similar size and di-
mensions of the round fossulae in scales and skeletal elements of Devonian
sarcopterygian and placoderm fishes, suggested an ‘interpretation of these
structures as being produced by parasites similar to copepod crustaceans’.
In particular, Luksevics et al. (2009) inferred that perforations of scales

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).

3.1.4 Gall crabs (Cryptochiridae) in corals
Members of the Cryptochiridae inhabit corals, living in either pits or in true
galls created by modifying the coral (e.g. Abelson et al., 1991; Carricart-
Ganivet et al., 2004; Figure 7). Verrill (1867) was the first to call a crypto-
chirid species parasitic after studying specimens of Hapalocarcinus marsupialis
modifying its coral host to form galls. In contrast, Hiro (1937) referred to
Hapalocarcinus and Cryptochirus as commensal to their coral hosts. Subse-
quently, Kropp (1986) convincingly demonstrated that three cryptochirid
species (H. marsupialis, Utinomiella dimorpha and Cryptochirus coralliodytes
(¼ Favicola rugosa)) feed on coral mucus, debris and/or coral pieces instead
of filter feeding on particles from the water. Kropp (1986) had reservations
about calling them parasites, as he considered that mucus feeding by crypto-
chirids would not represent a metabolic drain on the corals. Johnsson et al.
(2006) concurred and suggested they should not be called parasites. The key
question is to what extent mucus feeding constitutes a sufficient negative

Figure 7 Modern crescentic cryptochirid crab dwelling of Troglocarcinus corallicola in
the coral host Colpophyllia natans from Curaçao (Modified from Van der Meij (2014),
Figure 1(b)). Fossil evidence of similar-shaped dwellings has been found recently.

260 Adiël A. Klompmaker and Geoff A. Boxshall

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

Fossil Crustaceans as Parasites and Hosts
Aengapentastomum Late CambrianeEarly Stora Backor quarry, Ceratopyge Waloszek et al. (2006)
andresi Ordovician V€asterg€
otland, Sweden Limestone
(late Tremadocian) (reworked)
Boeckelericambria Late Cambrian Roadcut between Zone 5C Walossek and
pelturae (late Furongian) Haggården and M€uller (1994)
Marieberg, Kinnekulle,
V€asterg€
otland, Sweden
Haffnericambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
trolmeniensis (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late Cambrian Kinnekulle area, Zone 5 Castellani et al. (2011)
ahlgreni (late Furongian) V€asterg€
otland, Sweden
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
gossmannae (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5 Walossek and
kinnekullensis (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late CambrianeEarly Stora Backor quarry, Ceratopyge Walossek and
repetskii Ordovician (late V€asterg€
otland, Sweden Limestone M€uller (1994)
Tremadocian) (?reworked)
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
scandica (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria CambrianeOrdovician Green Point, Martin Point Member, Walossek et al. (1994)
taylori boundary Newfoundland, Canada Green Point
Formation
Invavita piratica* mid-Silurian (Wenlock, Herefordshire, England Volcanoclastic deposit, Siveter et al. (2015)
late Sheinwoodian to Wenlock Series
early Homerian)

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).

because of their small size: the largest described CambrianeOrdovician
specimen has a length of 780 mm (the Canadian species), making them diffi-
cult to recognize with the naked eye, although the suggested Silurian spe-
cimens range from 1 to almost 4 mm in length, mainly due to a long trunk
(Siveter et al., 2015). Moreover, their generally soft bodies except for the
cuticle do not fossilize easily.
Surprisingly, all known fossil species are found in marine deposits,
whereas modern species are mostly known from terrestrial animals. Given
their very similar morphology to today’s representatives (evolutionary stasis),
Walossek and M€ uller (1994) suggested that modern representatives must
have derived from marine ancestors instead of from terrestrial arthropods.
early Palaeozoic specimens were most likely parasitic and Walossek and
M€ uller (1994) and Walossek et al. (1994) inferred that the Cambriane
Ordovician ones may have lived internally in cavities such as their host’s
gill chambers, as deduced from the limb morphology. If correct, the larvae
were already highly adapted to their hosts in the earliest Palaeozoic

Fossil Crustaceans as Parasites and Hosts 265

(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.

3.2 Equivocal fossil evidence
3.2.1 Barnacle borings attributed to Acrothoracica in marine
invertebrates
In their overview of the fossil record of parasitism in marine invertebrates,
Baumiller and Gahn (2002, Table 1) listed several instances of acrothoracican
barnacle borings in Jurassic and Cretaceous belemnites (Seilacher, 1968),
Devonian platyceratid gastropods (Baird et al., 1990) and Devonian brachio-
pods (Rodriguez and Gutschick, 1977). Boucot and Poinar (2010)
mentioned many more examples of acrothoracican borings in Palaeo-
zoiceCenozoic marine invertebrates. Taylor and Wilson (2003) even
mentioned the presence of such borings in gastropods from the Ordovician,
but did not refer to them as parasites. Baumiller and Gahn’s (2002) claim of
parasitism appears ambiguous. For example, Tomlinson (1969, p. 11) stated
that ‘the (acrothoracican) cirriped can, at most, be considered a modest shell-
weakening pest, and in general does little if any harm to the host. All species
of the order collect food without taking from or giving anything of value to
the host’. Furthermore, Baird et al. (1990, p. 233) inferred ‘that the relation-
ship between the barnacles and the host gastropods was one of obligate

266 Adiël A. Klompmaker and Geoff A. Boxshall

commensalism, perhaps bordering on parasitism’. Seilacher (1969) and
Ba1uk and Radwa nski (1991) further discussed the commensal nature of
acrothoracican barnacle borings in various fossil invertebrates. Although
difficulties exist to identify commensalism in the fossil record (see Zapalski,
2011), commensalism appears the best descriptor of this symbiotic relation-
ship, in accord with Patton (1967). Therefore, it is not considered further
here.

3.2.2 Barnacles (Pyrgomatidae) in corals
Santos et al. (2012) recently described evidence for parasitism in the middle
Miocene coral Tarbellastrea reussiana by the barnacle Ceratoconcha aff. C. cos-
tata (Figure 9). The coral provided a habitat and protection from predators,
and a filter feeding location. Negative effects on the host included inhibition
of skeletal growth, modification of coral wall geometry and the secretion of
additional material in response to stress. Santos et al. (2012) indicated that
these barnacles do not feed on coral tissue, but instead use their thoracic cirri
for filter feeding purposes. Probably for this reason, Malay and Michonneau
(2014, Table 1) classified extant species of Ceratoconcha as planktotrophic
rather than parasitic. The barnacle does undoubtedly hijack part of the
food of the coral, especially for the polyps surrounding the barnacles, but
it is not nutritionally dependent on the corals themselves. Therefore, we

Figure 9 Several cross-sections of specimens of the pyrgomatid barnacle Ceratoconcha
aff. C. costata next to an example of the trace fossil Imbutichnus costatum (arrow) resul-
ting from the overgrowth of the coral Tarbellastrea reussiana of this barnacle from the
middle Miocene (LanghianeSerravalian) of Portugal. Scale bar 5 mm. (Modified from
Santos et al. (2012), Figure 3(d))

Fossil Crustaceans as Parasites and Hosts 267

consider that this relationship is better described as commensalism. Members
of this genus are known from the Oligocene to the present (Ross and
Newman, 2002), although the Oligocene occurrence was based on a per-
sonal communication only. Santos et al. (2012) indicated that pyrgomatids
were associated with corals at least since the Miocene, while they may
have appeared in the early Cenozoic, based on molecular analyses (Tsang
et al., 2014). Savignium, Pyrgoma, Cantellius and Nobia may represent an in-
termediate step from filter feeding to full parasitism. After analysing carbon
isotopic composition of these barnacles and their coral hosts, Achituv et al.
(1997) suggested that these taxa may depend on the host as a source of food
to a great extent, which was supported by the presence of coral tissue in the
stomach contents of one species. However, their cirral nets are probably still
used for filter feeding and they may have fed on expelled zooxanthellae as
well (Achituv et al., 1997). Although Ceratoconcha and the other taxa are
not widely accepted to be parasitic, there is a group within the Pyrgomatidae
that is accepted as such. Ross and Newmann (1995) erected the Hoekiini
tribe for species feeding exclusively on tissue of the coral Hydnophora with
their biting trophi (mouthparts), while the aberrant cirri do not serve to cap-
ture food. Ross and Newman (1969) suggested that the retention of vestigial
appendages in Hoekia monticulariae could mean that its coral-eating habit has
evolved recently, or that the juveniles still use them. They speculated that
the parasitic relationship developed within the last 10 Ma. A late Cenozoic
origin is corroborated by Malay and Michonneau (2014), who suggested
that hoekiines evolved quite recently given that this tribe represented a rela-
tively short branch in their phylogeny. Their fossil record is non-existent
thus far. Their relatively thin and fragile wall will not be easily preserved,
but the calcareous portion of the basis with an amoeboid outline has a better
preservation potential (Ross and Newman, 2002). Moreover, it may be
more readily recognized given the shape.

3.2.3 Isopods (Cymothooidea) in fishes and squids
Boucot and Poinar (2010) cited Bowman (1971) describing a case of possible
parasitism. Bowman (1971, p. 540) documented the isopod Palaega lamnae
from the Upper Cretaceous (Coniacian) Lower Austin Chalk of Texas
(USA) and tentatively noted that ‘the isopod could have been associated
with the Lamna [shark] either as a parasite or as a scavenger on the corpse,
but there is no evidence to support either role except for their occurrence
together’. Wieder and Feldmann (1992) questionably included this isopod
in Palaega until more complete material is discovered and concurred with

In summary. The same applies to at least 20 cymothooids attached to a water bug from the Late Jurassic (Tithonian) of Solnhofen. The fossil record of Cirolanidae is relatively well known (e. Klompmaker and Geoff A. who suggested that the Late Jurassic (late Kimmeridgian) Palaega nusplingensis may have been parasitic on account of its attachment to the ventral side of teuthoid squid (Figure 10). Claims of para- sitic cirolanid species from the fossil record lack evidence (Palaega williamso- nensis: Rathbun. lamnae. Another inte- resting observation is the occurrence of Palaega pisana in association with a Pliocene ‘whale fall community’. where scavenging was deemed more likely (Polz.2). For example. If placement within the Cirolanidae proves correct. pl. then it could be inferred that P. Figure 10 Holotype of Palaega nusplingensis from the Late Jurassic (late Kimmeridgian) of Germany. 3. Boxshall the note of Bowman (1971). Wieder and Feldmann. 1992) with the possible exception of Polz et al.. there is no convincing evidence of parasitism by fossil Cirolanidae including Bowman’s P. Germany. and P. This specimen is mentioned to be attached to the ventral side of a teu- thoid squid. However. 2012a). 2014). 2011). 1935. A similar claim was made by Pasini and Garassino (2012b) for Palaega sp.. 2004). Cirolana enigma: Wieder and Feldmann. they could not exclude the possibility that the specimen was feeding on the squid carcass. 1992. which would have provided ample feeding opportunities for predators and scavengers such as Palaega (Pasini and Garassino. fossil cirolanids were found within the carcass of an actinopterygian fish from the mid-Cretaceous (Albian) of Australia (Wilson et al. Hyzný et al. suggesting a scavenging life mode. steatopigia from the Pliocene. lamnae is a scavenger since modern cirolanids are free-living scavengers and predators (Smit et al.268 Adiël A. Scale bar 1 mm (Modified from Polz et al. 2013) and provides some evidence of scavenging. .. (2006). (2006).g.

the impact on the host is more . but their fossil record is non-existent (Smit et al. given their lack of a calcified cuticle. such as swellings.2.3. members of the modern Cymothoidae do not leave distinct traces that would help to identify them as parasites in the fossil record. p.g. Beschin et al.0e2. Sipunculida. To our knowledge. cysts or galls on certain hosts. Trapeziid crabs are known to extend back to the Eocene (Schweitzer. Phoro- nida. Annelida.. Parasitic copepods are known to cause visible lesions. Cnidaria. 2014). their presence in the fossil record does not suggest parasitism. Although in many cases the precise nature of the association between the copepod and its host has not been elucidated. Echiura.. Boxshall and Halsey (2004) noted records of associated copepods from Porifera. Corallanidae and Cymothoidae. 3. but such macrolesions are relatively rare. 2005.0 mm) and. The first three families are mentioned to be commensal to and/or micropredators of modern fish (Smit et al. but most are small (body length 1. Unless members of these families and the Cirolanidae changed their lifestyle throughout evolutionary history from parasitic to non-parasitic. Tridentellidae. Therefore. Glynn.4 Crabs (Trapeziidae) and corals Boucot and Poinar (2010. 2013). In the majority of species. Nemertea. Arthropoda. Etter (2014. 1990. 36) listed these crabs as being potentially para- sitic to corals. their relationship is better described as mutualism (e. Echinodermata. feeding on coral mucus. 1983a.Fossil Crustaceans as Parasites and Hosts 269 Other modern members of the superfamily Cymothooidea are parasitic such as Cymothoidae. They were classified as obligate ecto- parasites by Knudsen (1967). 2014) because corals derive benefit as these crabs remove material from and defend the corals from starfish predators (e. 3. Brachiopoda. Bryozoa. 2014).3 Modern evidence only 3. De Angeli and Ceccon. 939) considered that there is no definite fossil record of predatory or parasitic Aegidae. have limited fossilization potential. 2005.g. However. this relation- ship is not addressed further here. copepods are known to be parasitic on hosts representing virtually every phylum of aquatic metazoans. Mollusca. Platyhelminthes. The largest copepods (body length of up to 80 mm) are parasites of cetaceans and large fishes.1 Copepods Nearly half of all known marine copepod species live in close symbiotic as- sociation with other organisms.b). p. Stimson. Schweitzer. 2007. Hemichordata and Chordata (including urochordates as well as vertebrates).. McKeon and Moore.

Three genera. such as the Mollusca. Buhl-Mortensen and Mortensen. 2010).4 mm. Cysts and galls attributed to infestation by parasitic copepods are known for some modern hard- bodied host taxa such as scleractinian corals (Zibrowius. 1981. Boxshall subtle and highly unlikely to be detected in a fossil.2 Tantulocarida About 35 species of tantulocaridans are currently known. 1988. .. Whereas asexual adult females can attain a maximum size of about 1.270 Adiël A. Argulus. Kim and Yamashiro.3 Branchiura Branchiuran fish lice are all external parasites of fishes (for example Figure 11). 1968. Huys et al. but not from others.2) and crustaceans (Boxshall and Lincoln. either from para- sitic stages attached to marine crustaceans.1. 1981. are exclusively freshwater in distribution. Chonopeltis. 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. 2007). while the largest genus. such as polychaete worms or tunicates because of the host’s low preservation potential. sexual adults of both sexes are less than 1 mm in length (Boxshall and Lincoln.3. No trace fossil attributed to a parasitic copepod has yet been reported from soft-bodied hosts. Larvae are typically about 100 mm in length. 1983a). occurs on both marine and freshwater fishes. Klompmaker and Geoff A. with the exception of Dolops ranarum that uses freshwater amphibians as hosts. Their small size and lack of a calcified cuticle indicate a poor fossilization potential. 2004. Dojiri. echinoids (Stock. 3. 1993).3. Dolops and Dipteropeltis.. With the exception of Dolops that attaches by means of Figure 11 Two adult females of Argulus japonicus parasitic on a goldfish showing a typical lesion with a surface swelling and haemorrhaging. 1987. 3. see also Section 3.

the so-called Y-larvae. 2008). 2010. Oakley et al. 2010. but Cohen (1983) considered that no myodocopids were truly parasitic and she suggested that these ostracods were scavengers on injured or unhealthy fish. 1966). Once erroneously treated as a subgroup of the Copepoda. A few ostracods live in close symbiotic associations. The feeding activity of branchiurans on the epidermis of their hosts can cause le- sions including epidermal erosion. even if fossilized. inhabit the burrows of freshwater decapods. The hosts of the presumed parasitic adults are unknown. 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. 1993). Bennett et al. . Facetotectan larvae. but it is not calcified and no fossils are known as a result. and will not be treated further. 2013) suggests a Cambrian origin (see Section 3.1. 3. but they were unable to confirm that the ostra- cods had ingested shark tissue. Harding. but the free-swimming larval stages are widely distributed in coastal marine waters. but the existence of parasitic forms is equivocal. orri was parasitic. In Argulus.. the eggs hatch directly into an infective larva equipped with cephalic swimming appendages that atrophy in subsequent parasitic stages. Bennett et al.. 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. have their body enclosed within a bivalved carapace (Glenner et al.3. (1997) examined S. branchiurans typically attach to their host using paired suckers derived from the maxillules (Gresty et al. but the estimated suggested sister-group relationship of Bran- chiura with the Pentastomida (Sanders and Lee.3.4 Ostracoda Ostracods are a diverse modern group with a rich and extensive fossil record. No fos- sils are known.5 Facetotecta The adults of the Facetotecta are as yet unknown. Regier et al. are very general and would be hard to attribute to a specific parasite taxon. but such soft tissue features would have a low fossi- lization potential. but adult females detach in order to lay eggs on submerged hard substrates. Members of the podocopan family Endocytheridae. 3. localized swelling and haemorrhaging (Figure 11). for example.. the Branchiura is now recognized as a distinct subclass of Oligostraca. but are probably commensals according to Hobbs and Peters (1977).g.. but such traces. The ostracods were typically found in small pockets between adjacent gill filaments.Fossil Crustaceans as Parasites and Hosts 271 paired clawed limbs.5). (1997) concluded that S. They feed while on the host.

Leung. Martin and Davis. 2013). which allows for their gorging feeding behaviour.7 Malacostraca The whale lice (Cyamidae) are dorsoventrally flattened amphipods found on various cetacean hosts. Boxshall 3. 2001). They are typically attached beneath the pedal disc of the anemone and feed by cropping its tentacles (Yusa and Yamato. 1999). 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. Heteralepadomorph barnacles typically live in as- sociation with hosts. it is therefore presumed that infestation spreads only during intraspecific bodily contact between host individuals. A recent molecular clock study (Rees et al. Whale lice cannot swim and lack any planktonic dispersal phase in their life cycle. feed on the blood of elasmobranch and actinopterygian fishes. Rhizo- lepas species are parasitic on marine polychaete hosts (Day.3. rather as a terrestrial tick.. but their thin non- calcified cuticle. but Koleolepas species participate in a tripartite symbiosis. 2003. 3. 2014. Gnathiid isopods have free-living. Cyamids were traditionally treated as a wholly para- sitic infraorder of the amphipod suborder Caprellidea (cf. 2014) places the split of Anelasma from Capitulum at 126. living on gastropod shells inhabited by hermit crabs and carrying sea anemones. many inhabiting the gills of decapods. They have a very distinctive appearance. non-feeding adults that inhabit ca- vities in muddy sediments. Most heteralepadomorph bar- nacles are likely commensal. 2014). The shell plates are reduced or even absent in these thoracicans and their fossilization potential is presumably lower than typical sessile or stalked barnacles. at least in part.5 Ma. Klompmaker and Geoff A. and they typi- cally have reduced or absent valves. on nutrients absorbed from their host via an embedded rootlet system. but the juveniles. praniza larvae. is likely to limit their fossilization potential. . Lowry and Myers. in dead barnacles or in sponges. Engorged praniza larvae drop off their hosts between blood meals. 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. so their fossilization potential is presumably lower than for typical barnacles.. 1939). Both Rhizolepas and Anelasma have an atrophied suspension-feeding apparatus and depend.3.6 Thoracica A scattered assortment of pedunculate thoracican barnacles has switched from their ancestral suspension feeding to a parasitic mode of life.272 Adiël A.

the copepod Kabatarina. 2001). 1994. but equally useful... however (see above). OVERVIEW FOSSIL EVIDENCE AND FUTURE RESEARCH Fossil evidence of parasitism in crustaceans is confined primarily to decapod crustaceans (Figure 12). examples of K.Fossil Crustaceans as Parasites and Hosts 273 4. Nearly every other example of parasitism is represented by only few specimens and/or is known from a limited confirmed stratigraphic range (black in Figure 12). Wienberg Rasmussen et al.. should be investigated further by focusing on a locality where specimens exhibiting K. This applies especially for examples of parasitism based on body fossils. The lack of targeted research may also be a factor. Ninety-three infested species and hundreds of infested specimens have been found (e. Klompmaker et al. 2008.0 mm. herein).g. Swellings in decapod crustaceans caused by infestation by isopods are by far the best represented evidence of para- sitism in or by crustaceans. additional evidence can be gained from the reporting of new examples of parasitism discussed here given the spotty distribution . Moreover. (2014) for the Koskobilo (Spain) locality. highlighting the need for additional research by systematically collecting all available specimens. Less quantitative. Upe- niece. This small size explains the spotty occurrence of this type of parasitism in combination with rare circumstances allowing preservation of such fossils. as was suggested by Klompmaker et al. Excellent preservation certainly has helped in the case of Palaeozoic pentastomids and the Cretaceous fish parasite. 1989. Even though swellings in decapod crustaceans are the most common evidence of parasitism involving crustaceans. the length of larval pentastomids is 0. These examples have in common that the evidence for parasitism is small in size compared to the other examples in Figure 12.4 mm long (Cressey and Boxshall. Platyhelminth hooks in crustaceans and the inferred Devonian occurrence of copepods on fish are not without doubt. The discovery of additional infested taxa will help to refine and re-evaluate the trends shown in Figure 2. crusta are common. Walossek et al. Whether abun- dant species are more heavily infested than rare species. crusta are as yet not documented for many stratigraphic stages and even some epochs. very limited quantitative data exist per locality. assuming that parasitism occurred in the time in between the fossil and modern occurrences. Many opportunities for additional research exist. 2014.78 mm and platyhelminth hooks are only 0. The stratigraphic range of many other examples can be greatly extended because of their modern existence. The length of the only copepod body fossil in a fish is w1.

274 Adiël A. Boxshall . Klompmaker and Geoff A.

A question mark refers to uncertain evidence of parasitism of an example that has confirmed occur- rences.org). galls.3 (http://www.Figure 12 Stratigraphic ranges of examples of parasitism in or by crustaceans as recognized herein.2) is not Fossil Crustaceans as Parasites and Hosts included. domiciles and intersex evidence) induced by the inferred parasite. whereas the rest is based on structures (swellings. tscreator. 275 . The resolution used for determining first and last occurrences is the stage level if known (see text and tables for details). italic font are based on body fossil evidence of parasites. Grey bars represent probable occurrences based on modern or bracketing fossil occurrences in that host. Horizontal stippled lines mark boun- daries between the Phanerozoic eras. cysts. Categories in bold. The Devonian occurrences of copepods in fish are based on round traces on scales instead of copepod body fossils as in the Cretaceous. Timescale (left part) produced with TSCreator 6. Equivocal fossil evidence (3.

Many modern parasites stimulate localized tissue res- ponses in their hosts and some of the examples identified herein involve in- ternal skeletal elements or hard external body coverings that have potential for fossilization and could be the focus of targeted research. the following publishers. local small pits. not much is known about the prevalence of parasitism in nearly every example mentioned in Figure 12 except for isopod infestations in decapods. Furthermore.. Cristina Robins for reading and commenting on part of the text. 2014). Dieter Waloszek for Figure 8(a) and (c). A strategy to increase the number of fossil examples of parasitism involving crustaceans is to identify modern traces of parasitism that do not yet have a fossil record. Mark Wilson and Joachim Haug also kindly commented on earlier draft of this manuscript. . Other traces of parasitism are rather generic. ACKNOWLEDGEMENTS We are very grateful to Kenneth De Baets and Tim Littlewood for the invitation to contribute to this volume. but similar studies are lacking for other large taxa such as the copepods. Rodney Feldmann for the sug- gestion to work on this paper. We also thank John Jagt and Andrei Solovjev for providing useful literature. for their useful comments. Barry van Bakel for discussion about the specific placement of the Goniodromites specimen. G€unter Schweigert for useful literature and Figure 5(e). Andreas Kroh for museum numbers for the Ernstbrunn spe- cimens. This would help to pinpoint the earliest occurrence of parasitism for each group and may also serve as calibra- tion points for molecular studies of particular parasite clades. Sancia van der Meij for Figure 6. Furthermore. and the former also for useful literature suggestions. Systematic surveying of exist- ing collections and the collection of additional material in the field are likely to yield results. their comments are much appre- ciated.276 Adiël A. Klompmaker and Geoff A. Jesper Milan for the loan of a specimen from the Geomuseum Faxe. It is conceivable that the stratigraphic ranges of many exam- ples could be expanded considerably. René Fraaije for a museum number of Oertijdmuseum De Groene Poort. for example. Tsang et al. and will remain difficult to attribute to a particular parasite taxon. There is a continuing need for such molecular studies to complement palaeontological research focused on fossil parasites and their traces.. Sean Roberts and Alex Kittle for assistance with UF collections. the thoracican barnacles (Rees et al. Our gratitude goes to all these persons. Such data may help to evaluate the commonness of parasitism and its possible effect on the evolution of the infested group. It is apparent from Figure 12 that there is a long history of parasitism involving crustaceans. Divergence times indicating the putative origin of parasitism are available for some crustaceans. 2014. We recognize that size is an issue so special emphasis should be placed on submillimetre and millimetre scale features. Sten Jakobsen for information on Echinocorys from Denmark. Roger Portell. Boxshall of confirmed occurrences shown in Figure 12.

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003 All rights reserved. Donovan Department of Geology. Upper Cretaceous 313 4. j ISSN 0065-308X http://dx. Introduction 292 2. Not so the pursuit of ancient parasites in fossil organisms.org/10.3 Epizoobionts infesting a Mississippian crinoid 304 3. 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. A zaphrentoid coral on the camerate crinoid Amphoracrinus may have robbed food from the arms (Category 1 or 2B). Multiple Advances in Parasitology. 291 .Donovan@naturalis.1 Problems of interpretation 295 2. Interpretations and Confidence 294 2.5 Site selectivity of pits in echinoid tests. Volume 90 © 2015 Elsevier Ltd. CHAPTER SEVEN A Prejudiced Review of Ancient Parasites and Their Host Echinoderms: CSI Fossil Record or Just an Excuse for Speculation? Stephen K. Upper Palaeozoic crinoids and a Cretaceous echinoid (high confidence is 1. Of the five examples. The Netherlands E-mail: Steve.05.2 Limits of confidence 297 3.2015. 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).4 Platyceratid gastropods infesting Upper Palaeozoic crinoids 306 3. low confidence 7). Discussion 319 5.1016/bs.doi.apar.2 A growth deformity in a Mississippian crinoid 302 3. Naturalis Biodiversity Center.1 A coralecrinoid association from the Mississippian 299 3. the parasitic(?) organism is preserved in only two of them. Herein. a much more difficult proposition. Leiden. 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.nl Contents 1. Some Examples 298 3.

which almost invariably lacks a mineralized (and thus easily preserved) skeleton. This may or may not be associated with a growth deformation of the host. so our interpretation of its purpose (parasitism. as such traces of interaction can occur after the death of the echi- noderm.. the palaeoparasitologist works by necessity without . favourite pet dog or fish bought from a fishmonger. What commonly does not get preserved is the producer of the boring. The hunter of fossil parasites. Some specimens of the camerate crinoid Neoplatycrinites have circular grooves or depressions posteriorly. or something else) must be made in ignorance of the simple fact. Associated growth deformities show that the boring was engendered while the echino- derm was alive and able to react to the invasion. or failed or successful predation. this is preserved as some invasive structure (boring) into the echinoderm’s endoskeleton. Donovan. in ancient echinoderms. but it is more difficult to interpret (Category 4 or 7). Borings without growth deformities must be regarded as not proven parasitism. Donovan et al. mask such patterns. whodunit? The parasitologist looks for parasites. 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. where there is evidence of some interaction between an organism. but its presence is easily confirmed (or otherwise) using the wide range of biomedical. dense accumulations. In the twenty- first century. 2013). sheep. From these examples it is deduced that sparse infestations of borings or epizoozoic organisms permit a more confident interpretation of organism/organism in- teractions. Site selectivity of pits in the echinoid Hemipneustes places them preferentially adjacent to respiratory tube feet (Category 4). blood sampled or the fish cut open. 2014a) or mil- lions of years later (Donovan and Lewis. 1. has none of these advantages.292 Stephen K. Donovan pits in an Amphoracrinus theca are also associated with a deformed cup. 2014. and the hunt is on. either soon after (Donovan. Commonly. possibly following multiple spatfalls. but its life cycle elucidated and its genes sequenced. 2011. INTRODUCTION Consider the task of the parasitologist. and the host. presumably produced by coprophagic/parasitic platyceratid gastropods (Category 1). A stool is collected. Not only can the parasite be identified. in my own case. biochem- ical and gene sequencing tools currently available. There may or may not be an actual physical manifestation of the attentions of a parasite in a human being. parasite or not. Such navel contemplation is the easy part. all this can be done before lunch.

Donovan and Jagt. or disarticulated into just a few pieces. a senior synonym of the widely used Oichnus Bromley. 2014. bor- ings and related structures in ancient substrates. The study of trace fossils is ichnology. Most other . but all morpho- logically similar small round holes are more correctly referred to Sedilichnus M€ uller. it was suggested that borings in the echinoderm test that cause a range of growth deformations should be referred to Tremichnus Brett. involved in similar activities. the study of trace fossils. Only rarely is the producing organism preserved adjacent to a trace except in certain settings. 1985.. Trace fossils are given Latinized binomens. shelled cephalopods. that a given organism may have produced a range of trace fossils. but to the sedimen- tary structure that is the trace fossil. 2002). but these do not refer to an organism per se. That is. but these are pathologies of the echinoderm and are not part of the trace fossil (Donovan. 1990. 1994). trace fossils are named on morphology and not substrate (Pickerill. but it is incorrect to be too dogmatic about such assertions (Donovan. tube-dwelling worms. and that a particular morphology of trace fossil may have been produced by more than one group of organisms. 1977. either inhibiting growth or causing swellings of various mor- phologies. Linnean classification. brachiopods and ostracods. 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. 2010). such as gastropods. It is a com- mon ‘game’ in ichnology to speculate on the identity of producing organ- isms. Pits in live echinoderms commonly produce growth reactions in the endoskeleton. pp. what can we hope to achieve? As already intimated. see also Pickerill and Donovan. If this sounds daunting. 2013a). 1984. There are some organisms which have simple skeletons that are commonly pre- served whole. their classification as sedimentary structures is analogous to. Donovan and Pickerill. 32e34). for example. 2015). such as the shells of boring bivalves which may be preserved in their borehole in limestone (for example.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 293 parasites.. 1981 (Zonneveld and Gingras. 1998. 1976. Pits. foraminiferans and stony corals. Further. 1974 (Welch. representing evidence of ancient organic ac- tivity. the study of the preservation of our infested echinoderm. such as tracks. representing different activities. Boucot. but not part of. are trace fossils. Werle et al. It is a mantra of ichnol- ogy. including bivalve molluscs. then add to this the confusion introduced by the taphonomy. So. burrows and coprolites. many palaeon- tological investigations of echinoderms and putative parasites begin with the recognition of pits and boreholes in the echinoderm endoskeleton. trails.

parasites may produce distinctive galls or cysts in echinoid radioles (Warén and Moolenbeek. 248e250). one individual can be preserved as tens or hundreds of individual pieces. that an indication of disease or parasitism can be identified in the fossil record (Conway Morris. see Smith and Kroh (2011). 1990. arthropods. such as a fragment of crinoid column. describe some good examples that lead to reasonable interpretations. 1981. Commonly. plants and echinoderms. The morphological terminology of the crinoid endoskeleton is explained in Ubaghs (1978) and Moore et al.d). Leiden.294 Stephen K. and Natuurhistorisch Museum Maastricht. the Natural History Museum.c. asteroid arms. INTERPRETATIONS AND CONFIDENCE A great diversity of disease-carrying and parasitic organisms infest extant echinoderms (Jangoux. 1987a. although they are rarely para- sitic themselves (Rouse in Rhode. Boucot. Specimens discussed below are deposited in the following institutions: Department of Earth Sciences. Maastricht. or the exceedingly rare cases in which the infesting organism itself is fossilized. It is only in exam- ples where infestations of ancient echinoderms caused some recognizable deformity in skeletal growth. England (BMNH). multielement skeletons that fall apart soon after death. Donovan groups of organisms have complicated. 1989).b. If we accept this as the starting point for this paper. The producing organisms are not them- selves commonly preserved or otherwise identifiable (although two specific examples where the parasite is preserved are discussed below) and the echi- noderm may be preserved as only a fragment of endoskeleton that can only be classified to class level. pp. then we can. 2005. at least. Naturalis Biodiversity Center. And. So. 1988). The latter include the vertebrates. London. For example. it may be that the para- sitic infestation weakened the skeleton so that it is more prone to disarticulation postmortem than otherwise. 2. of course. and ophiuroids discs (Grygier. the Netherlands (NHMM). 2003). evidence of a possible parasitic interaction is found in a fragment of echinoderm that cannot be classified with any con- fidence any closer than class or order. Littlewood and Donovan. the Netherlands (RGM). crinoid pinnules and cirri. Examples of non-cyst-like structures produced by . (1978). for that of the echinoid test. palaeoparasitology of echinoderms most commonly involves recog- nizing pathological growth deformities produced in response to structures generated by parasitic(?) organisms.

Scale bar represents 1 mm. but certainly exotic. Figure 1 Figure 1 Phthipodochiton thraivensis (Reed. respectively.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 295 purported parasites which are considered below infest Upper Palaeozoic crinoid thecae and Cretaceous echinoid tests. BMNH G47258. lectotype. 1911) (see Sutton and Sigwart. Figures 2 and 3(c). For an example of the problem of interpreting ancient interactions with echinoderms which is not parasitism. 2. . (b) High-resolution X-ray microtomography image of the complete gut contents (valves removed). past the label and towards the top left.1 Problems of interpretation Interpretations of exotic interactions between ancient (or even extant) or- ganisms are commonly problematic and rarely leads to hard conclusions. from the Upper Ordovician of south-west Scotland. preserved as natural moulds and curving up from the lower centre to the right. 1911). Scale bar represents 10 mm. (2010). (After Donovan et al. apart from examples such as simple encrustations or boring invasions with numerous modern analogues.) (a) The specimen showing the valves of the chiton. consider the lectotype specimen of the primitive mollusc Phthipodo- chiton thraivensis (Reed. 2012.

it would more likely have harvested organic matter from finer grained sedimentary parti- cles. The speculation of predatory versus scavenging behaviour may appear trivial in this example. rex. The columnals represent ingested hard parts that were passing through the spiral gut of the chiton at the time of death. 2011b). Baumiller and Gahn. being unknown from extant chitons. 1905 e predator or scavenger e which have engendered a diverse correspondence (for a recent discussion. such crinoidivory in this ancient Scottish mollusc is unexpected. 2001). This revealed a string of shelly material preserved in a position that would correspond to the gut in an extant chiton. 2000). see Erickson. pp. we lack a modern analogue to provide an answer. Multiple lines of evidence indicate that this association is not a hydrody- namic accumulation (Donovan et al. Donovan herein) from the Upper Ordovician Lady Burn Starfish Beds of south-west Scotland. Determination of predation and scavenging of Ordovician crinoids has been mainly inferential. feeding on encrusting algae on rock surfaces. Latyshev et al. Mark Sutton and Julia Sigwart imaged the concealed structure of this specimen using high-resolution X-ray microtomography (for full details. scavenging or ingestion of sediment rich in crinoid bioclasts. 2010). 2010. 2014). like T. 2003). see Donovan et al. see below). unless the chiton was particularly unselective. Category 1 asso- ciations of crinoids as prey are rare throughout the fossil record. The last seems unlikely. Predation or scavenging is thus more probable. 1961 (Donovan et al. Whichever. a common taxon at Lady Burn. Almost nothing is known regarding the predators and scavengers of Ordovician crinoids (Meyer and Ausich. 1983. .. Chitons are commonly thought of as simple grazers.. 1975. and the example discussed herein is the oldest and the most unexpected. but many living chitons live on animal matter (Fulton. 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.. although there is suggestive evidence for pred- atory decapitation in some disparids (Donovan and Schmidt. 935e936). perhaps a Category 3 association sensu Boucot (1990. but it is analogous to the sometimes heated discussions of the habits of Tyrannosaurus rex Osborn.. but equally plausible. in some species highly specialized (Sirenko. 2004) and examination of gut contents in living species shows a variety of food preferences. Crinoid columnals may have been consumed by this chiton due to pre- dation.296 Stephen K.

although the reproductive season is only a month (Nichols. presumably to tempt predators and divert them from the visceral mass. personal communication) are of the opinion that predation on the arms of Palaeo- zoic crinoids may be evidence of predation. The evidence is good for the predation of the arms of Palaeozoic crinoids. Extant crinoids carry their go- nads mainly in their arms and pinnules (Breimer. an arm can be regenerated. These are commonly interpreted as evidence of successful predation on the arms of crinoids. What is needed at this juncture is some qualitative measure that re- searchers can apply to their deliberations to give their readers a ‘feel’ of the level of confidence with which they are made. October 2013. 1994). one general e demonstrate something of the difficulties of making a precise interpretation of the inter- actions between echinoderms and other organisms even when the data is good. as this tabulation is merely a brief abstract of a . although some taxa may have adapted their large anal sacs to bear the gonads (Lane. 2. admittedly preliminary. 9e10) original reliability classes which he applied to myriad examples that he examined for evidence of behaviour and coevolution in the fossil re- cord. 2004). 2003. 1777) is gravid throughout the year. 1978. If eaten.2 Limits of confidence The two examples given above e one particular. they may have been unmineralized and thus unlikely to be fossilized. but as of yet there is no entirely satisfactory explanation of why anything should have been eating such a poorly nutritious part of the animal. pp. consider the well documented record of otherwise well-preserved Palaeozoic crinoids that retain evidence of regeneration of one or more arms (see Baumiller and Gahn. Palaeozoic crinoids lacked this adaptation and it is assumed that the gonads were included within the cup. The reader is referred to the original publication for more explanation and many more examples. T18eT19). the comatulid Antedon bifida (Pennant.J. pp. is an adaptation of Boucot’s (1990. 1984). Both I and other authorities (V. This is entirely speculative as I am not aware of reports of likely prey organisms being preserved on the arms. but on some nutritious organism(s) or group(s) of organism(s) that lived on the arms. not on the innutritious arms of crinoids. making these nutritious organs the principal targets for predators.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 297 To give a further echinodermal example of an organismeorganism interaction that defies entirely confident interpretation. I suggest one way forward. but not good for the reason why. Syverson.

298 Stephen K. It could have written as the echinodermal parts of Conway Morris (1981) brought up-to-date. lacked detail. SOME EXAMPLES The structure of this paper was determined by personal preference. Category 6 Fairly speculative. Briefly. Category 2B Arguments based on functional analogy with closely related taxa. preferring to focus on a few selected examples from my own experience rather than a review that attempted to be too broad and. 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. Of the two examples given above. . Rather. 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. Category 7 Highly speculative. Most of the examples lean heavily on my own research. 1991b) or a parasitism paper modelled on the review of predation on cri- noids by Baumiller and Gahn (2003). Category 2A Organisms preserved in close association. Predation on the arms of Palaeozoic crinoids is best assigned to Category 4 or. 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. I have something a little different in approach from all of these. little reliability. Category 4 Less certain due to the producer of evidence being unknown. Category 5A High degree of uncertainty about the maker. Donovan much greater body of argument and evidence. Donovan. perhaps. such as functional determinations of wholly extinct taxa. 5A. 3. but not actually in position. 1983. Category 3 Fairly certain. Category 5B Examples where modern biogeographic evidence is crucial. based on known behaviour of living analogues. My intention here is to demonstrate broad principles that can be extrapolated to a reader’s own investigations. Boucot’s categories are summarized thus: Category 1 The rare examples where the evidence is incontrovertible. which explains why they preponderantly concern my beloved crinoids. a revision of the parasitism parts of various reviews of echinoderm taphonomy (such as Meyer and Ausich. in consequence.

195) noted ‘. The most notice- able variance is that Wright (1955. in subsequent early growth stages) they were capable of cementation to a variety of hard sub- strates (see. The corallite is small (Figure 2(c)). could only be exposed by destructive techniques. The solitary rugose coral may be a zaphrentoid (Mitchell. The crinoid theca was found in the Cover Mudstone.1 A coralecrinoid association from the Mississippian (Figure 2) Material. The coral corallite is preserved more or less perpendicular to the surface of the crinoid calyx and has been pushed into it. Lancashire [SD 7550 4265]. assuming it to be present. More precise systematic identification has not been possible on the basis of this single section. 1970..0 mm high.) BMNH EE5797 is an undeformed calyx (Figure 2(a) and (b)) of the monobathrid camerate crinoid Amphoracrinus gilbertsoni (Miller in Phillips. although it has obviously been depressed into the crinoid calyx as indicated by a series of more or less concentric fractures. Description: (Based on Donovan et al.. Preserva- tion of camerate crinoids as their golf ball-like thecae. for example. 1836). the other three interrays are narrower and all of about the same width. Clitheroe. It is preserved in transverse section (Figure 2(c)) and is apparently less than 2. pp. 2005. The coral is situated in the AB interray. p. Kabrna. in close contact with the anterior branch of the B ray arm. locality and horizon: BMNH EE5797 (Figure 2) is from Salt- hill Quarry. is common at this locality. Hubbard. being surrounded by concentric cracks which have broken across plates. 2003.’ BMNH EE5797 has an AB interray that is almost as wide as the CD interray at the level of the base of the free arms. It is small in comparison to the crinoid calyx. lacking most if any of the contiguous arms and stem. as larvae (and. plainly.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 299 3. although an actual attachment area per se is not clearly apparent and. p. England. 2011). 2003). 2005). one of the most important localities for Mississippian (Lower Carboniferous) echino- derms in north-west England (Donovan et al. probably due to post-depositional . Discussion: There are a number of lines of evidence to indicate that the solitary coral was attached to the crinoid calyx in life (Donovan et al. posterior interbrachial area [¼ CD interray] much wider than the others .. 43e44. present at the top of the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Lime- stone Member. Although solitary rugose corals were typi- cally unattached in adulthood. 203).

Scale bar represents 5 mm. Synbathocrinus conicus Phillips. (def) BMNH E71430. 1836).) Scale bars represent 10 mm. dorsal cup and proximal column. (a) Theca of crinoid. Amphoracrinus gilbertsoni (Miller. . (After Donovan et al.300 Stephen K. CD interray (posterior) towards bottom of page. A ray (¼ anterior) central. (f) D ray. note the coral in the AB interray (left) at the same level as the base of the free arms. A ray (¼ anterior) towards top of page. showing the prominent boring in the R:R:B plate triple junction (compare with Figure 3(a)). showing slope of oral surface towards EA interray (compare with Figure 3(b)). Donovan Figure 2 (aec) BMNH EE5797. Note regular pentagonal outline of undeformed specimen. (c) The corallite of the coral. The anal pyramid is subapical and situated about mid-way between the apex of the tegmen and the arms on the opposite side of the specimen to the A ray (¼ CD interray). 1836. 1981). (d) Lateral view with E ray central. in Phillips. with single borehole of Sedilichnus paraboloides (Bromley. (2005). 1821. (b) Apical view. encrusted by a solitary rugose coral. (e) EA interray central. to left). Figure 1. AB interray upper right. Note how the curved breakage of the crinoid around the coral follows the outline of the coral theca and has not resulted in disarticulation of plates. Note that the AB interray is broader than the EA interray (right of A ray arm). Note boring and oral surface sloping anteriorly (that is.

The close association of A. 1999). gilbertsoni with a solitary rugose coral would thus be worthy of comment under any circumstances. . 1974). that is. the coral would have been directed into the clean water currents. so Category 1 is at least plausible. 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. p. The importance of feeding is further emphasized by the corallite being hard against the B ray arm in the AB interray. 1983). it is more common to find crinoids. 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. particularly their columns. 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. too.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 301 compactional strain. Donovan and Lewis. but it is the position with respect to the crinoid calyx and the presumed life orientation of the latter that excites particular comment. The available evidence is at least highly suggestive that this coral was both a filter feeder and a parasite on the crinoid. this supposition is supported by the unusual width of the AB interray. But other groups of crinoids and stony corals are extant and well known. Although the position of the coral on the crinoid could be merely coincidence. which we interpret as growth rather than postmortem deformation (Figure 2(b)). the unusual width. Boucot (1990. so water currents would have been essentially sediment free. 2002) on the living crinoid. In attaching to the calyx of a crinoid. Reliability: Category 1 or 2B. the living coral was an epizoozoan (sensu Taylor and Wilson. The A ray is anterior and. All these lines of evidence support the supposition of an original biotic relationship between the host crinoid and its attached coral in life. being posi- tioned up-current from the anal pyramid. In the Mississippian of the British Isles. Although obviously speculative. encrusted by colonial tabulate corals than by either solitary or colonial rugose corals (see. the solitary coral has gained an advantage from its elevated position would have been above the turbid bottom layers of the water column. gilbertsoni formed a parabolic filtra- tion fanlike modern rheophilic crinoids (Macurda and Meyer. 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’. for example. if A.

England (Donovan et al. Clitheroe. Kabrna. but the cup is less developed on the bored side. 2. Figure 2. (b) DE interray central. The cup has been bored once. 1836. 134e136. showing how the oral surface slopes down towards the region of infestation. with the two most proximal columnals of the column. pp. X is the po- sition of the anal series (¼ posterior). Figures 10. Lancashire [SD 7550 4265]. BB ¼ basal circlet.1 herein).2 A growth deformity in a Mississippian crinoid (Figures 2(def) and 3) Material. in the EA interray. . Synbathocrinus conicus Phillips. Key: RR ¼ radial circlet. the cavity is a conical. Figure 3. and the basal in the EA interray (Figures 2(d) and 3(a. 2011. Current flow would have been from the top of the page. 2 ¼ adjacent to the anal series. 1836 (Wright.) The specimen is a dorsal cup. 3 ¼ distant from the anal series. large arrows mark positions of prominent R:R:B plate triple sutures. b) Camera lucida drawings of the dorsal cup and proximal column. p. locality and horizon: BMNH E71430 (Figures 2(d) and 3) is from Salthill Quarry. 1981). (a. Key: 1 ¼ in the same position of the anal series. of the disparid crinoid Synbathocrinus conicus Phillips. The boring is circular with a rounded margin.) Carpenter rays (AeE) indicated. Description: (Based on Donovan. Section 3. COL ¼ most proximal part of column. the oral surface sloping towards the EA interray (Figures 2(f) and 3(b)). unlike the common reaction to borings seen on some crinoid columns from the same site. (a) EA interray central (compare with Figure 2(e)). flat-bottomed pit which does not break through into the body cavity and is assigned to Sedilichnus paraboloides (Bromley. pl.. b)). Figure 3 BMNH E71430.302 Stephen K. * ¼ position of boring. (After Donovan (1991a). (After Donovan (1991a). 2003. showing the position of the boring. The crinoid theca was found in the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Limestone Member. 1952. corresponding to the positions of the arms. 36. Donovan 3. presumably a growth reaction to the distur- bance. (c) Schematic oral view based on BMNH E71430. Small arrows mark positions of cryptic B:B:R plate triple sutures. 1991a.) Scale bar represents 5 mm. at the triple suture between the E and A radials. 21 and 22). The cup is not swollen around the excavation.

just below the oral surface and the arms. and always orientated into the prevalent current by the crinoid. Brett (1978) suggested that pit-forming organisms on Palaeozoic crinoids were host spe- cific. they are also the potential borehole sites most removed from the anal series (X). Sutures between plates. the position of S. C and E rays are cryptic and can only tentatively be distinguished. paraboloides is interpreted as a choice made for ease of infestation by the boring organism. No determina- tion of the borer can be made apart from that it was small. The most probable life strategy of the pit-former was as a hard substrate dweller that fed by filtration (compare with Brett. would have been easier to bore into. and the Permian of Timor. the five R:R:B sutures are readily apparent (Figures 2(def) and 3(c)). bonded together by collagenous ligament fibres. all sides of the cup would have been equally available for infestation by borers and encrusters with the crown elevated above the substrate. It would be attached to the highest ‘fixed’ point of the crinoid. 9). in the EA and AB inter- rays.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 303 Discussion: Borings in the cup of Synbathocrinus are rare. It is presumed to have removed part of the suspended particulate food that would otherwise have been ingested by the crinoid. 1985). therefore. That the boring was made in a live crinoid is undoubted. rather than at one of the four other triple plate sutures? The sutures labelled 3 in Figure 3(c). In life. I have looked at hundreds of specimens of this genus. in contrast. from the Missis- sippian of North America and Europe. This suggests that the pit-forming organism was not a coprophage. ‘For some types of behavioral evidence there is an even larger degree of uncertainty about the maker of this evidence. 1978. Reliability: Category 4. The three B:B:R triple junctions. thus. The boring was made precisely at the triple suture between two radial (R) and a basal plates (B) (Figures 2(d) and 3(a)). are the most up-current (¼ anterior) plate triple junctions and. p. unmineralized and probably a filter feeding invertebrate. for almost 25 years and have failed to find a second bored specimen. Why bore into the EA interray. than the solid calcite of the plates. in the A. with growth pro- ceeding with greater vigour on the side opposite to the pit (Figures 2(f) and 3(b)). . This is particularly true for many trace fossils’ (Boucot. the identity of which remains unknown. 1990. either mechanically or chemically. Whether this contrib- uted to the deformation of the cup or it was mainly a reaction to the forma- tion of the pit must remain uncertain. The excavating organism selected its site with some precision.

Section 3. England (Donovan et al. (c) Enlarged lateral view of (mainly) dorsal cup. Kabrna. E-ray central.304 Stephen K. locality and horizon: BMNH EE8728 (Figure 4) is from Salthill Quarry. Lancashire [SD 7550 4265]. not crossing sutures. Scale bars represent 10 mm (a. 2011. same orientation as (c). (b) Enlargement of (a). d) or 5 mm (b. Specimen whitened by ammonium chloride. showing sub-horizontal arrangement of closely spaced pits.1 herein). D-ray to- wards top of page. (d) Theca in lateral view. (After Donovan et al. BMNH EE8728.3 Epizoobionts infesting a Mississippian crinoid (Figure 4) Material. c). showing how pits are concentrated on plates. . The crinoid theca was found in the Cover Mudstone. present only at the top of the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Limestone Member. 1836).. 2003. Note absence of pits above the line of the arm facets.) (a) Base of dorsal cup. (2006). Figure 4 Multiple Sedilichnus paraboloides (Bromley. 1981) infesting the dorsal cup of the Lower Carboniferous crinoid Amphoracrinus gilbertsoni (Miller in Phillips. Donovan 3. Figure 1. Clitheroe.

conicus described above (Section 3. the embedding organisms had access to the entire lower half of the theca. there is evidence for a growth deformity. Sedilichnus paraboloides is found on all plates of the dorsal cup (basal and radial circlets). These are situated on the adoral surface of the free arms. There are no pits on the tegmen above this level (Figure 4(d)). that is. the proximal column and aboral sur- faces of the free arms. fixed arms and tegmen. and on interbrachial plates up to just above the mid-height of the facet for the free arms (Figure 4(c). gilbertsoni and S. paraboloides (see above). which is analogous to the specimen of S. 2006. paraboloides on the substrate (see above). The base of the cup is angled to the long axis of the theca and slopes up towards the CD interray. even if its identity remains obscure. The hemispherical pits may be close packed together on individual plates.2). Discussion: This infestation occurred while the crinoid was alive. Most obviously. This description will concentrate on the pattern of infestation of pits on the crinoid theca (Figure 4).) The reader has already been introduced to A. The absence of pits on the tegmen above the level of the arms is most easily explained by the crinoid itself keeping this region free of any infestation by the action of the tube feet. Thus. enabling them to ‘clean’ the tegmen. upper left). but not the region below arm level. on fixed brachial plates (Figure 4(c)).. that is. the sloping base of the theca. in part. pp. could also have been infested. they do not occur on the depressed sutures between thecal plates. decipherable. Presumably. central areas of plates (Figure 4(b) and (c)). which are not preserved. The palaeoecology of the pit-forming organism is. are . Further. they occur on the more concave. all c.2). Pits (n > 50.1 mm diameter) are common throughout the defined area and ‘bald’ areas seen on some parts of the specimen are covered with pits elsewhere in analogous positions in relation to the arms. The plate sutures. but are rarely in con- tact. The theca preserves the dorsal cup. which would presumably be easier regions for embedment (Section 3. through 360 . 43e44. The pits are concentrated on the more elevated parts of the lower half of the theca. There is the obvious segregation of S. pits are distributed on the theca. below the level of arms. that is. not including the articular facet for the column (Figure 4(a) and (b)). but are not found on articular facet of the column. indicating that they were unable to survive the attentions of the tube feet. those of the dorsal cup and proximal fixed brachials (Figure 4(c)).A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 305 Description: (Based on Donovan et al. but the column facet would have been covered by the column in a living crinoid.

32842[1]. The pit producer may have been conspe- cific with that in Section 3. pp. ‘Discussion’.2. N. 3. above. the specimens are from the same locality.4 Platyceratid gastropods infesting Upper Palaeozoic crinoids (Figures 5 and 6) Material. 1916. West Timor (pre- sumably about sites 6e8 of Webster. herein.3851[1].) The gross morphologies of the Neoplatycrinus crinoid species from West Timor were described in Wanner (1916). Neoplatycri- nus dilatatus Wanner. 2013. no associ- ated locality data. cf. from Basleo (Charlton et al. RGM T.. RGM T. one centred below (Figure 5(a)) and the other centred on the periproct. Neoplatycrinus major Wanner (Figure 5(a) and (b)). below). 2010). locality and horizon: All specimens are members of the mono- bathrid camerate genus Neoplatycrinus Wanner. 2002. with the theca heavily covered by borings below arm level. conicus. there seems little connection between a growth deformity and an infestation through 360 . suggesting that this represents a gregarious accumulation of an organism that thrived on elevated calcareous substrates. Reliability: Category 4 (compare with Section 3. S.’ (Boucot. 9). This strongly supports a suggestion that they were fil- ter feeding. RGM B9 has a theca .4439[1]. so it is probable that the small difference in height between sutures and plate centres was impor- tant to the producers. so highly speculative as to have little reliability at all . In the pre- sent example. dilatatus Wanner (Figure 6(aec)). there being no obvious preference for anterior (A-ray) or posterior (CD-interray) (but see Section 4. and is apparently not selective with respect to the life orientation of the crinoid. Noil Tonini. RGM B9. in which a single pit is interpreted as engendering the aberration. Neoplatycrinus sp. from the Permian of West Timor. ‘. Two broad morphologies are identified. N.2) or 7. p. Interestingly. paraboloides is distributed on the lower part of the theca through 360 . comes from Toenino. RGM ST. but any evidence that the association may have been parasitic is masked by the dense accumulation of pits. 1990. only the modifications to the ge- ometry of the form of the CD (posterior) interray in a few specimens are described. no associated locality data.306 Stephen K. Figure 2). Pits are close packed. The sloping base of the theca is analogous to the example of S. 1998). but in only very few instances overlap. Description: (After Donovan and Webster. dilatatus Wanner (Figure 5(g)). Donovan avoided. The pits would have gained advantages attached to an elevated cup. rather than successive pits formed by one or a few individuals (compare with Donovan and Lewis. 990e991. these sutures are sunken between the plates. 1916 (Figure 5(cef)).

posterior towards top of page.) on Permian platycrinitid crinoids from West Timor. RGM ST. All scale bars represent 10 mm. dilatatus Wanner. 1916. dilatatus Wanner. Neoplatycrinus dilatatus Wanner.) (a. b) RGM B9. 1916. A ray central.4439[1]. Note deeply sunken homing scar. (g) RGM T. (cef) N. note posterior flat- tening of theca (right).A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 307 Figure 5 Homing scars of platyceratid gastropods (Lacrimichnus? isp. CD inter- ray viewed slightly obliquely from below and showing deep depression in radials.32842[1]. . (d) Lateral view. cf. Figure 1. posterior (CD interray central) and anterior (A ray central) views of theca. Neoplatycrinus sp. Spec- imens uncoated. N. (f) Basal view. (c) Posterior view. B ray slightly left of central. (After Donovan and Webster (2013). respectively. depressed CD interray central. 1916. (e) Anterior view.

.s. and on the C and D radials.3851[1]. (After Webster and Donovan (2012). extending onto basal circlet. (c) Lateral view. note posterior flat- tened in this view (left) and sloping towards base. RGM T. Scale bars represents 10 mm. 1916.) (a) Posterior view (CD interray central) showing depressed area around periproct. A ray central. (e) B and C interray. Figure 1(aec).. Donovan Figure 6 Platycrinitid crinoids and platyceratid gastropods. (f) Oral view.308 Stephen K.) (d) Posterior view. 1916). Figure 3. Permian of West Timor. (aec) Neoplatycrinus dilata- tus Wanner. (def) Platyceratid gastropod pre- served on the tegmen of Platycrinites s. wachsmuthi (Wanner. Specimens uncoated. Lacrimichnus? isp. (b) Anterior view. (After Donovan and Webster (2013). BC interray central.

1990.7 mm in diameter. g) and 6(a)). a comparable structure was illustrated by Wanner (1916. These structures do not encroach onto the basal circlet. 1998. but otherwise slightly raised. for example. 1983. Eckert. 8. These three thecae are distinctly truncated posteriorly (Figures 5(d. The central area is flattened on the C side and onto the D. Outside the groove. Rather. with the lateral extent determined by the positions of the arm facets. c. . pp. albeit a little different from RGM B9. Donovan. slightly protruding just below the level of the arms. Grygier and Nomura. 1993. 99. and the supporting CDeDeDE basal are depressed. 1981. RGM T. 2006. 1991b. The other three thecae (Figures 5(ceg) and 6(aec)) have a similar structure to each other. 251e252. Grygier. These depressed regions are approximately parallel-sided to convex below the arms (Figures 5(c. pl. the gastropod being a coprophage. as is also RGM B9). 32842[1] (Figure 5(c) and (g)). The radials in the CD interray form a depressed region below the periproct. the CD interray is flattened and slopes down to the basals. It persisted from at least the Middle Ordovician to Permian (Bowsher. viewed from the side (BC and DE interrays). but. 2003. Sutures between the radials are poorly apparent in this region. The radials of the CD interray bear a prominent sub-circular groove. Meyer and Ausich. Discussion: The coprophagic/parasitic relationship between the platy- ceratid gastropods. Bowsher (1955) consid- ered the platyceratidepelmatozoan association to be obligate commensalism. Boucot. 1988. like an inverted triangle with bowed sides. 2002).A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 309 that is typically bulbous anteriorly (Figure 5(b)). Figure 1(a)). amongst many others). The plate triple junction between the C and D radials. f) and 6(c).9e9. 1955. The mollusc is commonly preserved surmounting the anal opening (Figure 6(def)) where it produces no stereom overgrowth (but sometimes a ‘scar’). pp. presumably because the platyceratid is vagile. the test is sculpted by two (D) or three (C) sub-concen- tric raised ridges. sub-circular groove appar- ently extending around the periprioct. 1988.3851[1] (Figure 6(aec)) has the most rounded depressed region with a shallow. Conway Morris. Gahn and Baumiller. p. 1990. Baumiller. This suggests that they were not produced by the shell of the epizoozoic snail (sensu Taylor and Wilson. they are more likely a stereom response to gastropod infestation (compare with. Figure 5. and Palaeozoic crinoids and blastoids has been recognized for over 140 years. Comparable structures are not apparent on RGM T. feeding on the echinoderm’s excrement. 401e403. which would not have been so careful as to avoid adjacent plates in this manner. amongst others). becoming constricted towards the base of the thecae.4439[1] and ST. situated below the periproct and more on the D than C radial (Figure 5(a)). 499.

In these associations. the crinoid thecae show distinct modi- fied morphologies.. whether these changes also altered the feeding capa- bilities of the crinoids is equivocal. 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. which further suggests a parasitic association (see also Baumiller. 48). pp. the circular scars indicate the homing positions of the producing gastropods (compare with Boucot. 1993. One of the common associations by platyceratids in the Late Palaeozoic was with the platycrinitid monobathrid camerates. Most obviously.310 Stephen K. . or extending between the C and D arms to include the periproct. Figure 1. either below the periproct. para- sitic. 393e395. Specimens from Timor discussed by Webster and Donovan (2012) either preserved (or. presumed to have been formed in response to the gastropod infestation. 1999).g. Baumiller et al. Donovan Yet Rollins and Brezinski (1988) demonstrated that crinoids with platycera- tid infestations tend to be smaller than those without associated gastropods. 1937. Baumiller (1990) demonstrated that some platyceratids drilled into the crinoid tegmen. Webster and Dono- van. pl. The specimens described above do not retain any platyceratid shells. Baumiller et al. due to the posterior position of the peri- proct of Neoplatycrinus. 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. 1937. The platyceratid may have utilized the detritus concentrated by the filtration fan of the crinoid. but instead show evidence of different patterns of infestation in the CD interray of the theca first discussed by Donovan and Webster (2013). Wanner. Donovan and Webster. The circular structures (Figure 5(a)) and depressed areas (Figures 5(c. 2004. 2003. 2013). The Permian of West Timor has provided some of the youngest specimens to demonstrate this interaction (e. 2012. Figures 7 and 8... that is. Part of the fascination of this association is its age. ‘Hard substrate communities are poorly known in the Permian’ (Taylor and Wilson. preserved evidence of) platyceratids on the tegmen or along the radial summit of the platycrinitids Platycrinites Miller and Neoplatycrinus Wanner (Figure 6(def)). 2004. these snails were attached subapically in the CD interray rather than apically on the tegmen or adjacent to it. Figure 6(def) herein). p. thus indicating that the association was detrimental to the host. Unlike other examples known from the Permian of West Timor (Wanner. 11. at least. This was undoubtedly. Further. Baumiller et al. at least in part. Note that these patterns of infestation are differently positioned.

faintly in RGM T. irregular growth of stereom as a reaction to this by the crinoid or. Lacrimich- nus? isp. Commonly. except posteriorly. slightly inflated morphology of the crinoid theca is retained. but these modifications to the crinoid suggest that it was at least likely. 463). but typically has an undulating outer furrow.. Figure 8). most prob- ably. Jagt (2007) identified an older Lacrimichnus? isp. p. raised above the level of the adjacent theca. 2005.3851[1] (Figure 6(a)). but without obvious homing scars except. Whether the gastropod remained in this position at least semipermanently is unknown. although they could reflect the growth of a single individual gastropod. Although produced by acorn barnacles rather than gastropods. the gross.. The second morphology described above involves the CD interray of the crinoid being depressed. The round groove in the radials in the CD interray is a trace fossil that is close in morphology to Lacrimichnus Santos et al. Figure 6(def) shows a platycer- atid gastropod from this locality so that its size and shape e low. its position on the theca is in sharp contrast to where snails must have infested in Figures 5 and 6(aec). p. It is considered unlikely that these concentric structures represent occupancy by successively larger platyceratids through time. 2004. 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. For example. They may be the result of abrasion by the edge of the aperture of the gastropod shell or chemical etching (Bromley. such as the specimens illustrated herein and by Boucot (1990. Infested tests retain this geometry in anterior . is also applied as an ichnotaxonomic name to the round scars pro- duced by Permian capuliform platyceratid gastropods. on a barnacle plate from the upper Maastrichtian of the type area. but also concentric raised ridges outside it. more so than in RGM B9. a combination of all of these. conical or bowl-shaped. is broadly similar to Lacrimichnus. The gastropod must have stood proud of the surface of the theca. These scars are prominent external modifications of the cri- noid’s endoskeleton. 2003. moderately broad and cap-like e may be compared to the other illustrations herein. an inflated appearance in life. Despite these modifications. circular groove (situated below the periproct. The former is presumably produced (mainly) by the gastropod. the latter by the crinoid. 2004. the test of uninfested Neoplatycrinus is bulbous. 483). Figure 8). based on Neogene gastropod attachment scars. RGM B9 (Figure 5(a)) has both a deeply depressed.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 311 1990. possibly. presumably giving the CD interray. contrast with Figure 6(a)). the ichnoge- nus Anellusichnus Santos et al.

the former showing large thecal modifications to accommodate the snail. . as I suggest. then the more or less restored hydrodynamics of the crown would have engendered more efficient suspension feeding by the crinoid. Figure 6(def) herein). and the modifications of the theca that favoured this crinoidegastropod association were probably devel- oped early and retained throughout life. posteriorly. giving the test a prominent anteriore posterior asymmetry. Boucot. but. If this supposition is accepted as possible. The shells of these gastropods are low and cap-like (Bowsher. in life. 1955. f) and 6(c)). Webster and Donovan. made as a response by the crinoid to the snail’s presence in the CD interray. the shell of the coprophagic platyceratid would have been positioned here. coprophage or both? The gross morphology of the crown presumably played a part in ensuring water currents for feeding reached the arms (Jefferies. Such a relationship was more than casual. The depressed CD interray produces a marked change in thecal gross morphology. the combined morphology of crinoid þ gastropod may have approximated that of an uninfested theca. g) and 6(a)) suggest a mode of infestation in which the gastropod extended between the C and D arms. with a shell in place in the depressed CD interray. in other views. although remaining bilaterally symmetrical along a mirror plane AeCD (that is. Figures 10e13. This would have resulted in greater production of faeces which. perhaps covering the periproct. in turn. Donovan view (Figures 5(e) and 6(b)). The two morphologies of CD interray seen in Neoplatycrinuseplatyceratid associations are indicative of two different patterns of infestation. overall. the question must be asked why was it advantageous to host. anterioreposterior). Figures 1(aec) and 2(deh). 1990. would have benefitted the gastropod. The depressed CD interrays (particu- larly Figures 5(c. Such flattening is only developed in the CD interray. presumably filling the depression. If. there is a marked flattening posteriorly (Figures 5(d. The same may be true for the (less depressed) RGM B9. 1989). This is interpreted as a different expression of infestation by a platyceratid.312 Stephen K. 2012. But. That is. This arrangement suggests a long-term relationship between crinoid and gastropod. This interpretation is speculative. It may have been that the gastropod in part ‘restored’ the gross morphology of the theca with its shell by filling the depressed area. but could be tested by a carefully defined experiment in a flume tank. that is. the relationship was probably more parasitic than mutualistic. the platyceratid ‘filled the gap’ in the theca. but.

that is.D. this may not have brought to an end this biotic association that spanned over 200 million years. there is enough information provided by a wealth of spec- imens preserved in situ to leave little doubt about the reliability of the basic coprophagous relation. Upper Cretaceous (Figure 6) Material.. Taylor.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 313 In contrast. and that only those platyceratid taxa actually found in situ on a host pelmatozoan may be safely considered to have been coprophages’ (Boucot. 2007. It is an axiom within the life sciences that.5 Site selectivity of pits in echinoid tests. in maturity. positioned below the periproct and not between the arms. The two specimens discussed in detail below are bored and encrusted tests from the uppermost Maastrichtian (Upper Cretaceous) of southern Limburg. It appears most reasonable to conclude that only those platy- ceratid taxa closely associated with pelmatozoans were potentially coproph- ages. so does its biota of parasites and commensals specific to that host (Vickery and Poulin. Despite the fact that the platyceratids and their host pelmatozoan taxa are extinct. although their associations with Mesozoic crinoids. if any. 1778) infested by the non- penetrative pit Sedilichnus excavatus (Donovan and Jagt. P. locality and horizon: Many specimens of the holasteroid echinoid Hemipneustes striatoradiatus (Leske. 1998. 1992. 3. when a host goes extinct. 26). compare Figure 5(a) with Figures 5(c. including those discussed and illustrated by Donovan and Jagt (2002. written comm. platyceratids persisted at least until the Late Triassic (Bandel. Dunn et al. Reliability: ‘Category 1 for those taxa found in place on a host pelma- tozoan. NHMM RZ . Specimens described herein with gastropod shell scars in the CD interray might be considered Category 3 based on the above arguments. 2008. However. If. Figure 7 herein). Bandel and Frýda.. somewhat different in gross form (for example.). other Neoplatycrinus grew to produce a typically radially sym- metrical theca with no depressed regions in any ray. presumably so did the associated platyceratids. such a theca became infested. 1999) or even Mid Jurassic (Carmel Limestone of Utah. When the camerate crinoids went extinct at the end of the Palaeozoic. are equivocal. Although the camerates became extinct. the Netherlands. Dobson et al. 2002) in the NHMM collections. g) and 6(a)). 1990. 2005. Platyceratids found unassociated with pelmatozoans pose the serious question concerning whether or not all platyceratids were coprophages. the thecal outline could not be modified as much and the CD interray developed a homing scar morphology. 2009). p.

314 Stephen K. probably Caulostrep- sis isp. (Figure 8(b)). (d) Paratype with outline partly controlled by adjacent ambulacral column. 00162 (Figure 8(aee)) is from the base of subunit IVf-6 of the Meersen Member. profile (test external surface to left) and internal surface. profile (test external sur- face to left) and internal surface. c). (After Donovan and Jagt (2002. . i) NHMM RN 452b. more than three poorly preserved spirorbid worm tubes. 2002). striatoradiatus. a cheilostome bryozoan colony in the depressed region anterior of the peristome. (c) Holotype (arrowed) with two paratypes. Donovan Figure 7 Holasteroid echinoid Hemipneustes striatoradiatus (Leske. Figures 2(a. 2011a. at the former Blom quarry. Figure 1). (a) Apical view. right lateral view. NHMM MA 0234-1 (Figure 8(feh)) is from the same subunit (IVf-6). h) NHMM RN 452c. pp. Description: (Based on Donovan and Jagt. (e. Scale bar represents 5 mm. 3(a. Scale bar represents 5 mm. figure- of-eight boring aperture just posterior of the peristome. (f. note the linear ar- rangements of some groups of borings. Maastricht Formation. Spirorbid worms occur at or just above the ambitus. (g) NHMM RN 452a. Scale bars represent 10 mm unless stated otherwise. b) and 5(aee). 113e114) The test of H. and a slot-like. now defunct. Berg en Terblijt (for locality map. was used as a substrate by a va- riety of encrusting and boring invertebrates. see Donovan et al. paratypes. The oral surface bears three attached pycnodonteine oyster valves in close association. all Upper Cretaceous (Maastrichtian) of the Netherlands and Belgium. (b) NHMM 699. NHMM RZ 00162. 1778) and the pits Sedilichnus excavatus (Donovan and Jagt.. but from the nearby Ankerpoort-Curfs quarry.) (a. d) NHMM MK 4689. 2013b. internal surface. c. near Geulhem. showing holotype (arrowed) and paratype borings.

Specimens uncoated. S. excavatus (far right). e). (g) Ambulacrum IV (left anterior) right of centre. situated poste- riorly. other specimens are in interambulacrum 4 (left lateral). partly overgrows a S. 2002). all Upper Cretaceous (Maastrichtian) of the Netherlands and Belgium. IeV) and interambulacra (Arabic numerals. Caulostrepsis isp. bryozoan colony. e) Two views of S. (b) Oral surface showing episkeletozoans (oysters. (d) Sedilichnus excavatus in ambulacrum V. (c. excavatus. excavatus in the upper part of the ambulacrum and two further pits. excavatus in ambulacrum 4. An encrusting oyster. (feh) NHMM MA 0234-1. excavatus pits. compare rounded outline to (c. excavatus between the columns of pore pairs. Figure 1. Scale bars repre- sent 10 mm. .A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 315 Figure 8 Holasteroid echinoid Hemipneustes striatoradiatus (Leske. with one poorly developed S.) (a) Apical surface with the positions of four pits. in interambulacrum 3 (left anterior). marked by asterisks (*). in close association. (h) Ambulacrum V (left posterior) right of centre with S. (After Donovan and Jagt (2013b). (f) Ambulacrum II (right anterior) central with closely group- ed pair of S. (After Donovan and Jagt (2013b). Figure 2. spirorbids) and annelid boring. (aee) NHMM RZ 00162. 1e5) is provided as an explanation of the notation used in the text. The numerical designation of ambulacra (Roman numerals. 1778) and the pits Sedilichnus excavatus (Donovan and Jagt.) All oblique views of the apical surface.

). supra-ambitally) are small pits and borings (S. straddling the adradial suture with interambulacrum 1 (Figure 8(a)). cee)). excavatus is in close association with an ambulacrum of the echi- noid. 1981). the central boss being elongated. The second specimen. pores or pore pairs are only weakly developed adapically. Each S. Donovan a small circular hole in the posterior column of plates in ambulacrum V (left posterior) is Sedilichnus simplex (Bromley. In ambulacrum V (left posterior). Pore pairs in the anterior ambulacral column are only strongly developed abapically of this pit. whereas ambu- lacrum II (right anterior) has two S. excavatus in close association (Figure 8(f)). In ambulacrum I (right posterior). 1975.316 Stephen K. is not apparent. but abutting the anterior pore column with a straight side (Figure 8(a. excavatus (Figure 8(a. Only S. This is the furthest away from a pore column of any of the four pits. simplex. and referred to S. it occupies a central posi- tion in the ambulacrum. Ambulacra IV and V (left anterior and posterior. Other scratch marks and excavations of (mainly) ambulacra in this region are probably the spoor of grazing regular echinoids. Other traces include some small pits and perforations. 4 of which are closely associated with ambulacra (Figure 8(feh)). NHMM MA 0234-1 (Figure 8(feh)) is less mark- edly encrusted. The posterior column of pores is strongly deflected towards this pit. respectively) . excavatus. excavatus is considered a pre-mortem infestation. Only S. situated adjacent to the adradial suture with interambulacrum 4 (Figure 8(a) and (d)). the adjacent pores appear to be normally developed. ambulacrum I (right posterior) is not infested. Anterior pores or pore pairs appear weakly developed adapically of the pit. e)). S. On the apical surface (that is. c. Again. Sedilichnus excavatus occurs within ambulacrum II (right anterior). The ambulacral infestations are high on the test. situated apically. excavatus is lower on the test than either pit on the right side and is anterior to the anterior column of pore pairs. although typical Gnathichnus pentax Bromley. Sedilichnus excavatus is moderately common on this test with 11 pits. However. simplex and Caulostrepsis? isp. unlike that specimen. but more heavily pitted by S. Each of these first three pits is shallow. they are rounded to subangular rounded in outline. four specimens of S. excavatus oc- curs on the upper half of the test. S. strad- dling the perradial suture between the two plate columns (Figure 8(a)). Sedilichnus excavatus in ambulacrum IV (left anterior) is deeper and has straighter walls. straddling the perradial suture. spirorbids and a fragment of a shell that may or may not be encrusting. as in NHM RZ 00162. excavatus is anterior to the anterior pore pairs. probable Caulostrep- sis isp.

All encrustations on these tests are interpreted to have occurred after the death of H. most notably. excavatus. provide stronger indica- tions that the settling behaviour of the infesting organism was site selective. some of which were densely infested. in the posterior interambulacrum (5. most particularly by the growth of internal blisters within the test and beneath the pits (Donovan and Jagt. raised central boss. pits are vertically one above the other (Figure 8(g) and (h)). p. excavatus. was alive. 2002. In life. and walls concave’ (Donovan and Jagt. 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. 69). far right.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 317 each have one associated pit (Figure 8(g) and (h). the oral surface would have been in intimate contact with the sediment. pre- cluding infestation of the oral surface of either specimen by oysters. the tests would have been protected by both densely packed spines and pedicellariae which would have prevented such varied infesta- tions. there was not any strong indication of site selectivity. striatoradiatus (Leske). Sedilichnus excavatus was diagnosed as ‘Circular to elliptical. The two analogous specimens of H. striatoradiatus would not have been a deep burrower. Thus. rather. which probably lived more or less epifaunally. although some pits did occur in linear associations (Figure 7(b)) and most infested the test supra-ambitally. striatoradiatus described above. almost invari- ably with a broad. The occurrence of a partial marginal (subanal) fasciole under the periproct points to such a mode of life. bryo- zoans. high. Figure 8(h). In two inter- ambulacra. Donovan and Jagt (2002. the tests preserve no evidence of the growth of the echinoids being adversely affected by any boring or attachment. Figure 7(eei) herein). 69. Despite this wealth of material. Ample evidence was presented to indicate that this association occurred while the echinoid. A holasteroid such as H. with the exception of S. 2005. Thus. possibly furrowing through the sediment at the surface. Aperture of boring overhanging. striatoradiatus. striatoradiatus (¼ episkeletozoans sensu Taylor and Wilson. and partly overgrown by an oyster. excavatus included pits in numerous tests of H. Figure 2(c)) counted ‘at least 61 individual borings’ on NHMM JJ 699. Figure 2. pl. although relatively sparsely infested by S. The type series and related material of S. or spirorbid or serpulid annelids (Figure 8(b)). . Further. 1. oblique view) a pit sits on the interradial suture at about mid-height of the test. 2002). non-penetrative Oichnus. it would have lived epifaunally. respectively). p. about as far as it is possible to be situated away from an ambulacrum.

in this example at least. But if a close association with a respiratory ambulacrum was advantageous. IV) the pores/pore pairs are weakly developed. pp. II. That is. either between columns of pore pairs (II. This may be because other specimens are either too densely (Figure 7(a) and (b)) or too sparsely infested. lower right. Whatever. It is notable that the only ambulacrum (anterior. However. 2000. V). but. 24. This association was presumably advantageous to the organisms forming certain S. II. Although more densely infested by S. 2000. Donovan the only borings interpreted to be pre-mortem are those of S. V) or anterior to the anterior column of pore pairs (I. These observations are supported by the second specimen. centre of image) are located towards the middle of an interambulacrum. far right) and all but two (Figure 8(g). this test supports four pits in close association with three respiratory regions of ambulacra (II  2. IV. 1984. IV. excavatus. the posterior plate column in ambulacrum IV is deflected towards the pit (best seen in Figure 8(e)). infestations seem to be associated with reactions by the test. S. Most notably. Figures 4 and 5). particularly as S. as noted above. striatoradiatus with precision. 2013b). more densely bored specimens (such as Figure 7(b)) distracted them from recognizing an associ- ation between ambulacra and S. excavatus infested interam- bulacra. excavatus. pl. These are on the upper half of the test and in po- sitions analogous to those of NHMM RZ 00162 (compare Figure 8(aee) and (feh)). Two pits are on the interradial suture (Figure 8(f). but this must be speculative. V). Figure 7(a) shows an analogous specimen to NHMM MA 0234-1. each S. excavatus is only associated with ambu- lacra bearing well-developed respiratory tube feet. in NHMM RZ 00162. excavatus . Jagt. which selected positions to settle on live H. it is unknown why seven other O. III) on the apical surface that was not infested is also functionally different from all the others (Smith. excavatus is associated with a different ambulacrum (Figure 8(a)). p. striatoradia- tus. 281). excavatus. excavatus. NHMM MA 0234-1 (Figure 8(feh)). although. This pattern begs a palaeoe- cological explanation. Figure 8(h).318 Stephen K. this may equally be a preservational artifact or an inac- curate observation. or it may be that the present example preserves a rare behaviour (but see Jagt. a deduction which is in agreement with the observations on other specimens infesting this echinoid species by Donovan and Jagt (2002. 2005. as these are invariably less prominent than those of the posterior pore pairs. 93e95. There is also a suspicion that in some ante- rior plate columns of ambulacra (I. excavatus on NHMM RZ 00162 (Figure 8(aee)) show a distinct pattern of infestation not otherwise noted on H. The four examples of S.

and crinoid pin- nules and cirri (see. but selective. But similar pits and swell- ings may be the result of embedment by an organism that is merely seeking elevation above the substrate. 9). tenta- tively. Although such structures are locally common. thus. for example. excavatus is uncertain. 294e295. 2011)? Pits in the endoskeleton in crinoids and blastoids (such as Figure 9(a)) are difficult to interpret. Grygier. some modern parasites produce identifiable galls and cysts in echinoid spines. 1918). 1990). ‘For some types of behavioral evidence there is an even larger degree of uncertainty about the maker of this evidence. pp. 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. Five specific examples are given in this essay. I have aimed to be expansive. 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. All S. on echinoids). 2003. but may have been protective in part. The function that the respiratory tube feet performed for the producer of O. A crinoid column would provide very little nourish- ment.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 319 also successfully infested other areas of the test. ophiuroids discs. We suggest. excavatus in advantageous positions to feed on plankton. 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. excavatus in Figure 8 are above the mid-height of the test and. It will gain an advantage. p. but is it parasitism (Zapalski. 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. Certainly. that this pattern of infestation may have placed the producers of O. 1990. This is particularly true for many trace fossils’ (Boucot. so a bored fossil pluricolumnal should best be interpreted as an . 4. anterior of the tube feet on an echinoid moving slowly across the seafloor. Other reviews of para- sitism on echinoderms have tried to do too much in a restricted space (such as Kowaleski and Nebelsick. I suggest that they are more difficult to interpret than some of the examples discussed in detail herein. asteroid arms. were presumably above the sedi- ment surface in this shallowly furrowing echinoid. Reliability: Category 4. 1988).

ankylosed structure would be further protected. 1983. Even though I have specialized in the systematics and palaeobiology of the crinoid stem for 35 years. If you want to read further on such ancient cysts and galls (reviewed in Conway Morris. Shropshire [NGR SO 588 980]. RGM 791 727.320 Stephen K.) Salthill Quarry. Figure 4(g). England. Specimen whitened with ammonium chloride for photography. Much Wenlock Limestone Formation. Lancashire [SD 7550 4265]. Clitheroe. England. tegmen (including the anal tube) and arms.) An embedding organism that elicited a reaction by the host to induce stereom growth and produce a more robust. are more circular and assigned to Sedilichnus paraboloides (Bromley). (b) A strongly swollen pluricolumnal. I trust it is now obvious why I have included no bloated and bored crinoid stems in the examples that I have given above. Note the irregular outline of the pluricolumnal. I have concentrated herein on examples of ectoparasites in which there are obvious interactions with the crinoid theca by organisms . 1981.). and the large size and irregular outline of the pit in the centre. (The latter could also be provided by the dead parts of a dead crinoid. Meyer and Ausich. RGM 544 426 (After Donovan and Lewis (2010). (After Donovan et al. This surely is not what is commonly interpreted as parasitism. and may be overly speculative. the other two pits. and would have perforated the endoskeleton (Baumiller. interaction with an unmineralized invertebrate seeking elevation above the substrate and protection from the environment. a boring/ embedding parasite sensu stricto would be more likely to infest a crinoid through the more nutritious dorsal cup. 1990) rather than just embedding in it. lower Viséan (¼ upper Chadian) Salthill Cap Beds. their literature is both broad and diffuse.) sp. Instead. Figure 2. pp. Donovan (a) (b) Figure 9 (a) Pentagonocyclicus (col. Bellman Limestone Member. Lower Silurian (Wenlock. Reasonably. 412e414). in which the living crinoid grew over an encrusting coral. Wenlock Edge. Homerian). including one at the top. Scale bars represent 10 mm. due to swelling. (2014b). perforated by three pits..

provide data on the nature of these associations additional to than commonly available. perhaps the multiple pits in this specimen represent more than one spatfall. But if the earliest pit(s) was solitary or sparse and concentrated on one side of the cup. The coprophagic/parasitic association of platyceratid gastropods and Palaeozoic crinoids is one of the best known organism/organism associations in the fossil record. 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)). It is apparent from the above examples that sparse infestations provide a more cogent tale of organic interactions than dense infestations.2 (Figures 2(def) and 3). that is. The circular scars on or below the anal pyramid in a posterior position on Neoplatycrinus from Timor. All pits are of similar size and spacing. which are more likely to confuse the issue.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. There are strong indications that the coral was interfering with the crinoid’s feeding. as in the title of this paper. The inter- action between a solitary stony coral and a crinoid theca (Section 3. with the snail astride the anal pyramid on the apical surface. Lacrimichnus? isp. If we think in terms of a progressive . including its situation at the level of the base of the crinoid arms and the unusual width of this inter- ray. it may have produced the sloping base as a growth reaction analogous to that in Section 3. suggesting that growth of the crinoid was minimalizing the interference by the parasite.1) in the Mississippian is an unexpected one. In two examples we actually know (or at least have a very strong suspicion of) the producing organism. The pits of dead producers may even have been recycled by juvenile settlers. 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. Later.4).A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 321 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. being based on many hundreds of specimens worldwide. The crinoid theca with multiple pits through 360 (Section 3. 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. (Section 3.

1988). but no qualitative differences are obvious. indicated by the uneven growth of the cup. striatoradiatus and the producer of S. excavatus are each closely associated with an ambulacrum. The four individual pits of S. Perhaps comparing infested and nonin- fested tests from a single horizon may indicate a size variance (compare with Rollins and Brezinski. excavatus were formed while the host echinoid was alive by the evidence of the thickened ‘blisters’ of test calcite beneath them (Figure 7(eei)). the only advantage available is elevation. when first described.2 and 3. Thus. Certainly. excavatus were ‘hitching a ride’ on H. partic- ularly in NHMM RZ 00162 (Figure 8(aee)). The pits themselves are of more complex morphology (Figure 7(c) and (d)) than those infesting either of the pitted crinoids (Sections 3. the single pit in Synbathocrinus represents the start of an infestation (Figures 2(def) and 3) whereas the densely bored Amphoracrinus is an end point (Figure 4). remained without an associated pit (Figure 8(a)). Donovan invasion by pit-forming organisms. which produces a growth deformity in the crinoid theca and quite rightly may be regarded as a parasitic reaction. only the ante- rior ambulacrum. Figure 8 here- in). was this parasitism or not? The Maastrichtian echinoid H. Donovan and Jagt (2013b) deduced that the close association of the pit-forming organism and echinoid . it was plainly apparent that the pits of S. as well as elevation above the substrate. the ‘record’ being 61 individual pits. of different gross morphology and function. When originally described by Donovan and Jagt (2002). a hard substrate that elevated them above the seafloor (in most examples) and permitted them to feed by whatever means. including 2. there was no suspicion of a host/parasite relationship between H. early spatfalls gain a feeding advantage in an optimum position. excavatus. particularly the upper two thirds (Figure 7(a) and (b)).3) and it can be more confidently proposed that they were produced by members of a single species of unmin- eralized invertebrate showing a particular boring behaviour. Contrast these early deliberations with the sparsely infested tests of H. The earliest invaders can be selec- tive and gain a feeding advantage. Individual echi- noid tests are more or less well infested on the apical surface. striatoradiatus described later by Donovan and Jagt (2013b. striatoradiatus.322 Stephen K. on the oral surface. Whether this was parasitism and how so is difficult to determine. unusually. striatoradiatus (Leske) allows a similar anal- ysis to be made on one species. It was readily apparent that the producers of S. one or two spatfalls later. Take away the ‘noise’ of dense infestation and a pattern appears. Later spatfalls (this may all have happened over a few weeks or months) did not produce an obvious growth deformity in the cup.

but being little removed behaviourally from an encruster attached to the outside of the test which would rarely. London) and Kenneth De Baets (Friedrich-Alexander Universit€at. in the absence of the producing organ- ism in many examples. probably represent dwelling traces. Cassian Formation and the evolutionary history of the Neritomorpha (Gastropoda). Geosci. Paul Kabrna (Barnoldswick. 66. namely John Jagt (Natuurhistorisch Museum Maastricht). what was the parasite. Bandel. at least. but difficult to interpret. Pal€aontol. 231e240. The evidence provided by the endoskeletons of fossil echinoderms may be particularly rich. we are forced to speculate not just on whodunit. . London). for inviting me to contribute to this volume. p. a sedimentary structure. Lancashire) and Gary Webster (Washington State University. Dense infestations may mask patterns that are apparent in weakly infested specimens. Most. 215e274. but also what it was that they were doing. CONCLUSIONS ‘The fossil record contains many examples of the interactions that occurred between organisms . K. Description and classification of Late Triassic Neritimorpha (Gastropoda. Pullman). 2007. be thought to be truly parasitic.. 2003. are difficult to explain and probably do not represent parasitism per se. And. 136). 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. David Lewis (the Natural History Museum. none more so than the evidence of ancient para- sitism’ (Littlewood and Donovan. Italian Alps. Mollusca) from the St Cassian formation. REFERENCES Bandel. I also thank my co-authors of the papers that form the backbone of this contribution for their collaboration and collegial companionship. if ever. Erlangen). Bull. evidence of interactions may be . particularly where the ambulacral morphology was deformed as a response (Figure 8(cee)). 5. ACKNOWLEDGEMENTS I thank the editors. such as deformities in the crinoid column. K. Z. 82. either interpretation might be regarded as parasitic. the pit or gall produced looking like parasitism. Tim Littlewood (The Natural History Museum.. which is represented by its trace fossil. 1992. Too rarely is there a good answer to basic questions. cryptic or difficult to interpret.A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 323 ambulacra provided some feeding or protective advantage to the borer. Platyceratidae from the Triassic St.

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doi.6 Pyrgomatid barnacles 339 3. it is notoriously difficult to identify whether the symbioses are parasitisms (þ/) or mutualisms (þ/þ). j ISSN 0065-308X http://dx. notably corals.1 Recognition of parasitism in fossils 333 3.2015. Discussion 342 Acknowledgements 343 References 343 Abstract Colonial species occur in a wide range of aquatic invertebrates. some having excellent fossil records. Colonial Animals 331 3.2. some of which may be parasitic.apar.2. Taylor Department of Earth Sciences. Natural History Museum. Soft-bodied symbionts in such intergrowths are Advances in Parasitology.002 All rights reserved. The ability of colonies to endure partial mortality and the typically plastic growth of benthic colonial species facilitates the formation of macrosymbiotic associations. Intergrowths between host colonies of stromatoporoid sponges. Volume 90 © 2015 Elsevier Ltd. Fossil Colonial Animals as Parasites 341 5. UK E-mail: p. corals or bryo- zoans.5 Celleporaria and Culicia 338 3. and skeletal or soft-bodied symbionts are particularly common in Ordoviciane Devonian shallow-water deposits.1016/bs.taylor@nhm. bryozoans and graptolite hemichordates.3 Chaetosalpinx and other bioclaustrations 336 3.4 Cornulitids and colonial hosts 338 3.1 Caunopores 335 3. Putative Parasites of Fossil Colonial Animals 333 3. London.5 Supposed parasites of graptolites 341 4. In contrast to unitary animals. 329 .uk Contents 1. Introduction 330 2. However.2.2.2.2 Symbiotic intergrowths and bioclaustrations 334 3.2 Rugose corals and stromatoporoids 336 3. colonial animals grow by adding repetitive modules known as zooids.05.ac.3 Galls 340 3. CHAPTER EIGHT Differentiating Parasitism and Other Interactions in Fossilized Colonial Organisms Paul D.2.org/10. as with unitary fossils.4 Borings 340 3.

Colonial animals are characterized by a modular construction. 2007. and Boero and Bouillon. including corals and bryozoans (see Hughes. 1989 for a good introduction to colonial and other clonal animals).330 Paul D. however. Myxozoans are now considered to be cnidarians and impact their bryozoan hosts by reducing colony growth. INTRODUCTION Coloniality has evolved on multiple occasions in invertebrates (Blackstone and Jasker. Hooper. 2005). 2003). Taylor represented by moulds in the host skeletons. Lorenz. 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. comprising repetitive clonal units called zooids. Relatively little is known about the parasites of colonial animals living today (e. sponges and cnidarians can be important parasites of colonial organisms themselves (e. Some of the most-studied endoparasites of extant colonial organisms are myxozoans parasitizing freshwater bryozoans (Okamura et al. Boxshall. Direct fossil evidence of microbial parasites in colonial . All colonial animals are aquatic and most are marine.g. 2013). causing periodic castration and zooid gigantism (Hartikainen and Okamura. 2005 for sponges. Pelagic graptoloid hemichordates from the Early Palaeozoic occasionally contain cysts or tubes that have been attributed to parasites on the grounds that they would have adversely affected the hydrodynamics of the floating colonies. there is a lack of convincing data showing that any of these symbionts were parasites. Even less is known about parasites of ancient animal colonies found in the fossil record. some fossil galls provide more convincing examples of parasitism. a process of preservation termed bioclaustration. L€ utzen. 2012.g. Boero and Bouillon. 2005). Hill and Okamura. 2005. Grygier and Hoeg. In some cases. which have not yet been reported from the fossil record. Future studies should test for para- sitism by comparing the sizes of colonies hosting symbionts with those lacking symbionts. 2003. By comparison with modern analogues.. 2005.. but see Hooper. achieving a range of sizes and shapes. 2003).g. molluscs (e. As yet. which is usually indeterminate and plastic: different colonies belonging to the same species may grow for different lengths of time and in different patterns. 1. 2015).g. New zooids are budded to bring about colony growth. Hartikainen et al. 2005) and various arthropods (e. and t