मुख्य The Biology of Parasites
The Biology of Parasites
Richard Lucius et al.
This heavily illustrated text teaches parasitology from a biological perspective. It combines classical descriptive biology of parasites with modern cell and molecular biology approaches, and also addresses parasite evolution and ecology.
Parasites found in mammals, non-mammalian vertebrates, and invertebrates are systematically treated, incorporating the latest knowledge about their cell and molecular biology. In doing so, it greatly extends classical parasitology textbooks and prepares the reader for a career in basic and applied parasitology.
Categories: Medicine\\Diseases: Internal Medicine
प्रकाशक: Wiley-Blackwell
Parasitism: The Diversity and Ecology of Animal Parasites
Goater T.M., Goater C.P., Esch G.W.
parasites675
parasite507
hosts451
parasitic288
immune257
intermediate246
worms232
infections207
malaria183
plasmodium166
trypanosoma141
genome135
morphology131
intermediate host130
genes129
leishmania128
worm123
larva121
intestine120
tick117
cattle115
arthropods114
ticks110
proteins108
intestinal104
organs104
intermediate hosts103
protozoa100
pathogens100
mammals99
cysts90
parasitology89
infective89
immune responses89
larval87
membrane86
toxoplasma84
parasitic worms81
falciparum80
brucei77
nematodes77
sporozoites76
gondii75
cruzi75
parasitic protozoa74
infect74
feces74
lice74
mouthparts73
mites73
biology of parasitic67
eimeria66
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भाषा: german
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Richard Lucius, Brigitte Loos-Frank,
Richard P. Lane, Robert Poulin,
Craig W. Roberts, and Richard K. Grencis
Richard Lucius, Brigitte Loos-Frank, Richard P. Lane,
Robert Poulin, Craig W. Roberts, and Richard K. Grencis
With contributions of guest authors
Nina Papavasiliou, Rockefeller University, New York, USA
John Boothroyd, Stanford University, Stanford, USA
Kai Matuschewski, Humboldt Universität zu Berlin, Berlin, Germany
Translated by Renate FitzRoy and Ron Shankland
Prof. Dr. Richard Lucius
Humboldt University
Institute of Biology
Prof. Dr. Brigitte Loos-Frank
University of Hohenheim
Department of Parasitology
Emil Wolff-Straße 34
Prof. Dr. Richard P. Lane
Stonewall Holt
EX13 7RW Kilmington, Devon
Prof. Dr. Robert Poulin
Great King Sreet
Prof. Dr. Craig W. Roberts
Strathclyde Institute of Pharmacy and
Biomedical Sciences (SIPBS)
161 Cathedral Street
G4 0RE Glasgow
Prof. Dr. Richard K. Grencis
Life Sciences/AV Hill Building
M13 9PT Manchester
Renate FitzRoy
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This is a completely revised and updated
version of the second edition of
"R. Lucius and B. Loos-Frank: Biologie
von Parasiten" (ISBN 978-3-540-37707-8,
Springer-Verlag, Berlin, Heidelberg).
General Aspects of Parasite Biology 1
Richard Lucius and Robert Poulin
Introduction to Parasitology and Its Terminology 2
Parasites 2
Types of Interactions Between Different Species 5
Mutualistic Relationships 5
Antagonistic Relationships 6
Different Forms of Parasitism 10
Parasites and Hosts 11
Modes of Transmission 16
What Is Unique About Parasites? 18
A Very Peculiar Habitat: The Host 18
Specific Morphological and Physiological Adaptations 22
Flexible Strategies of Reproduction 27
The Impact of Parasites on Host Individuals and Host
Populations 30
Parasite–Host Coevolution 38
Main Features of Coevolution 38
Role of Alleles in Coevolution 42
Rareness Is an Advantage 45
Malaria as an Example of Coevolution 46
Influence of Parasites on Mate Choice 51
Immunobiology of Parasites 58
Defense Mechanisms of Hosts 60
Innate Immune Responses (Innate Immunity) 60
Acquired Immune Responses (Adaptive Immunity) 62
Scenarios of Defense Reactions Against Parasites 63
Immunopathology 67
Immune Evasion 68
Parasites as Opportunistic Pathogens 72
Hygiene Hypothesis: Do Parasites Have a Good Side? 74
How Parasites Alter Their Hosts 77
Alterations of Host Cells 78
Intrusion into the Hormonal System of the Host 79
Changing the Behavior of Hosts 82
Increase in the Transmission of Parasites by Bloodsucking
Vectors 83
Increase in Transmission Through the Food Chain 83
Introduction into the Food Chain 88
Changes in Habitat Preference 92
Biology of Parasitic Protozoa 95
Richard Lucius and Craig W. Roberts
Metamonada 99
Giardia lamblia 99
Further Reading 102
Parabasala 102
Trichomonas vaginalis 103
Tritrichomonas foetus 106
Amoebozoa 107
Entamoeba histolytica 108
Entamoeba dispar 114
Other Entamoeba Species 114
Further Intestinal Amoebae 115
Acanthamoeba 115
Euglenozoa 117
Cell Biology and Genome 118
Phylogeny 121
Trypanosoma brucei 121
Trypanosoma congolense 131
Trypanosoma vivax 132
Trypanosoma evansi 133
Trypanosoma equiperdum 133
Trypanosoma cruzi 134
Leishmania 141
Development 142
Morphology 143
Leishmaniosis 143
Cell and Immune Biology 143
Leishmania tropica 148
Leishmania donovani 150
Leishmania braziliensis and Leishmania mexicana 151
Alveolata 153
Apicomplexa 155
Cell Biology 160
Coccidea 165
Cryptosporidium parvum 166
Eimeria 169
Eimeria tenella 174
Eimeria bovis 175
Isospora and Cyclospora 175
Toxoplasma gondii 176
Neospora caninum 186
Sarcocystis 187
Haematozoea 190
Plasmodium 190
Plasmodium vivax, a Causative Agent of Tertian Malaria 199
Plasmodium ovale, a Causative Agent of Tertian Malaria 200
Plasmodium malariae, the Causative Agent of Quartan
Malaria 200
Plasmodium falciparum, the Causative Agent of Malignant Tertian
Malaria or Malaria tropica 201
Plasmodium species of Monkeys, Rodents, and Birds 210
Piroplasms 211
Babesia 211
Theileria 214
Ciliophora 218
Balantidium coli 219
Ichthyophthirius multifiliis 219
Trichodina 221
Parasitic Worms 225
Brigitte Loos-Frank and Richard K. Grencis
Platyhelminths 228
Digenea 230
Adults 234
Systematics and Evolutionary History 237
Schistosoma 238
Leucochloridium paradoxum 248
Diplostomum spathaceum 248
Fasciola hepatica 251
Opisthorchis felineus 254
Paragonimus westermani 257
Dicrocoelium dendriticum 259
Cestoda 263
Evolution and Origin of Life Cycles 266
Genome 269
Diphyllobothriidea 269
Mesocestoides 272
Cyclophyllidea 272
Moniezia expansa 273
Hymenolepis diminuta 274
Rodentolepis nana (Hymenolepis nana) 275
Taeniidae 277
Taenia saginata 281
Taenia solium 282
Taenia asiatica 282
Hydatigera taeniaeformis 283
Echinococcus 283
Echinococcus granulosus 283
Echinococcus multilocularis 285
Echinococcus vogeli and Echinococcus oligarthrus 286
Acanthocephala 288
Nematoda 294
Dorylaimea 300
Trichinella spiralis 300
Trichuris trichiura 305
Chromadorea 306
Strongyloides stercoralis 306
Ancylostoma duodenale and Necator americanus 308
Angiostrongylus cantonensis 311
Haemonchus contortus 312
Dictyocaulus viviparus 315
Ascaris lumbricoides 315
Ascaris suum 318
Toxocara canis 318
Anisakis simplex and Anisakis spp. 320
Dracunculus medinensis 321
Enterobius vermicularis 323
Filariae 325
Wuchereria bancrofti and Brugia malayi 326
Onchocerca volvulus 330
Loa loa and Dirofilaria immitis 334
Rodent Models of Filariosis 334
Arthropods 337
Brigitte Loos-Frank and Richard P. Lane
Vector Concepts 340
Impact of Bloodfeeding 343
Acari – Mites and Ticks 344
Anactinotrichida (= Parasitiformes) 347
Mesostigmata 347
Dermanyssus gallinae 348
Varroa destructor 348
Metastigmata (= Ixodida or Ixodoidea, Ticks) 350
Tick Bites and Saliva 353
Ixodidae – Hard Ticks 354
Argasidae (Soft Ticks) 358
Tick-Borne Diseases 359
Actinotrichida (= Acariformes) 361
Prostigmata = Actinedida = Trombidiformes 362
Trombiculidae – Harvest Mites, Chiggers 363
Astigmata = Acaridida = Sarcoptiformes 364
Crustacea 366
Argulus foliaceus 367
Sacculina carcini 368
Insecta 370
Phthiraptera – Lice 374
"Mallophaga" – Chewing Lice 375
Anoplura – Sucking Lice 375
Pediculus humanus capitis 377
Pediculus humanus humanus 378
Pthirus pubis 378
Disease Transmission by Lice 379
Heteroptera – True Bugs 380
Triatominae – Kissing Bugs 380
Cimicidae – Bedbugs 382
Cimex lectularius 383
Siphonaptera – Fleas 384
Biology and Development 384
Pulex irritans 387
Ctenocephalides: Cat and Dog Fleas 387
Tunga penetrans – Jiggers 388
Disease Transmission by Fleas 388
Diptera – Flies 390
Lower Diptera 390
Ceratopogonidae – Biting Midges, No-see-ums, Punkies 391
Disease Transmission 393
Culicidae – Mosquitoes 394
Simuliidae – Blackflies 401
Phlebotominae – Sandflies 404
Brachycera 408
Tabanidae – Horse Flies 408
Muscidae – House and Stable Flies 410
Calliphoridae – Blowflies, Screwworms 413
Oestridae – Bot or Warble Flies 413
Glossinidae – Tsetse Flies 415
Hippoboscidae, Nycteribiidae, Streblidae – Louse Flies, Keds and
Bat Flies 418
Answers to Test Questions 423
Parasitism is a specialized way of life, pursued by organisms that have evolved to
thrive at the expense of a living host. Therefore, in a broad sense, all pathogens like
viruses, bacteria, or eukaryotic infectious agents are parasites and thus share many
common features. However, they also have important differences. For example,
viruses and bacteria are genetically less complex and employ different strategies
for exploiting a host, leading to different disease syndromes. As a consequence,
different scientific fields have emerged, of which the discipline of parasitology is
one that deals with eukaryotic pathogens, namely, protozoa, worms, and arthropods. Parasites, in this narrower sense, are a huge burden to mankind, with billions
of infected people, mainly in tropical developing countries with relatively poor
hygiene. Along with their medical and veterinary importance, parasites have a
fascinating biology, which is the theme of this book. The Biology of Parasites is
based on an earlier German book (Lucius & Loos-Frank (2008), Springer Verlag,
Heidelberg), which has been extended and updated by the current team of authors.
The living host is a very particular niche; it is not a neutral place at all. Parasites
are involved in a constant struggle with their hosts, who strive to rid themselves
of the unwanted company, deploying all sorts of mechanisms against them. These
range from defensive behavior to the effector molecules and cells of a complex
immune system. In spite of such defenses, an extraordinary number of animals
have adopted parasitism as a mode of life; some specialists believe that >50% of
animal species are parasites or have at least a parasitic phase in their life cycle.
It seems that the parasitic lifestyle is so rewarding that it has been worth the
great effort parasites have made to develop most intriguing means of locating
their hosts, survive within or on them, produce offspring, and ensure that the next
generation reaches a new host. To exploit a host, parasites may change their morphology beyond all recognition: they may trick and cheat by disguising themselves
or manipulate their host's cellular pathways or even their behavior. Because of
these extraordinary, bizarre, or seemingly "otherworldly" abilities, parasites have
always fascinated biologists and captured the attention of the general public.
The antagonistic relationship between pathogens and their hosts drives the evolution of both adversaries in a profound manner. This arms race has affected the
evolution of some of the most important processes of life, for example, sexual
reproduction and the immune system. It also shaped the genomes of both parties
to a degree that we have only recently discovered. Indeed, new molecular techniques developed in past few decades have opened an extraordinary range of perspectives on the interplay between eukaryotic parasites and their hosts. Genome
projects have cast light on the peculiarities of parasite genomes. For example,
we have learned that many protozoans and worms have undergone a reductive
evolution in their genomes, especially with regard to those functions they have
appropriated from their host, while other areas have been expanded, such as those
needed for the manipulation of the host. This explosion in genomic knowledge has
also provided us with the tools to discover and describe precisely parasite-specific
metabolic pathways. It has also facilitated the dissection of molecular mechanisms
used by parasites to detect host cues, invade host cells, or cope with immune effector mechanisms. This information has already allowed and will hopefully further
allow us to design specific measures against parasites and their vectors, ranging
from strategies to prevent infection, such as vaccines and pesticides, to drug development. However, it is not the sole goal of parasitologists to fight diseases, as
worthy as that is, but to understand the intricacies of the parasitic lifestyle and to
put them into a broader biological context. This greatly contributes to our wider
understanding of key biological processes, such as evolution, ecology, and generation of biodiversity. Last but not least, the simple wonder and awe the extraordinary biology of parasites instills in us makes their study worthwhile in its own
This book is designed to provide advanced information to students of biology,
medicine, or veterinary medicine and to interested lay persons. An introductory
chapter on general parasitology, addressing crosscutting topics of parasitology,
is followed by specific chapters on the biology of protozoan parasites, parasitic
worms, and parasitic arthropods. The focus is on parasites of medical or veterinary importance, as these are best known from intensive research and are of the
widest interest, although we also highlight parasites with interesting biological
adaptations to emphasize those traits most typical of the parasitic lifestyle. To
be concise, we discuss particular species as representatives of their taxon, while
related parasites are briefly mentioned or treated in tabular form. Inevitably,
the book cannot cover the entire field of parasitology. It does not give detailed
treatment of the therapy or control of parasitic infections, parasite ecology,
or evolutionary parasitology. Likewise, we have sparingly mentioned marine
parasites or parasitoids and their interesting biologies. To cover cutting-edge
topics, we have invited three renowned guest authors to contribute concise
information from their field of research, namely, John Boothroyd (parasite–host
interplay of Toxoplasma), Kai Matuschewski (vaccine development against the
malaria parasite Plasmodium), and Nina Papavasiliou (new developments in
trypanosome research).
We are thankful to many colleagues from different fields of parasitology and
beyond for their helpful discussions. We thank specifically those who provided
images of parasites or illustrative research data, in particular Oliver Meckes and
Nicole Ottawa from eye of science for fascinating electron microscope pictures,
Prof. Egbert Tannich for images of amoebae, and Dr. Heiko Bellmann for photos
of arthropods. We gratefully acknowledge the permission of the Departments of
Parasitology of University of Hohenheim and of Humboldt University to utlize
pictures from their archives. The life cycles and other drawings are based on the
painstaking work of Flavia Wolf, Dr. J. Gelnar, and Hanna Zeckau, which is gratefully acknowledged. A heartfelt thank-you goes to Christine Nowotny for her most
professional help with the organization of the manuscript and illustrations. This
work would not have been possible without the continuous support of Dr. Gregor
Cicchetti and Dr. Andreas Sendtko and their team from the publisher Wiley-VCH,
which is gratefully acknowledged.
Richard Lucius
General Aspects of Parasite Biology
1.1.1 Parasites 2
1.1.2 Types of Interactions Between Different Species
1.1.2.1 Mutualistic Relationships 5
1.1.2.2 Antagonistic Relationships 6
1.1.3 Different Forms of Parasitism 10
1.1.4 Parasites and Hosts 11
1.1.5 Modes of Transmission 16
1.2.1 A Very Peculiar Habitat: The Host 18
1.2.2 Specific Morphological and Physiological Adaptations 22
1.2.3 Flexible Strategies of Reproduction 27
The Impact of Parasites on Host Individuals and Host Populations 30
1.4.1 Main Features of Coevolution 38
1.4.2 Role of Alleles in Coevolution 42
1.4.3 Rareness Is an Advantage 45
1.4.4 Malaria as an Example of Coevolution 46
1.6.1 Defense Mechanisms of Hosts 60
1.6.1.1 Innate Immune Responses (Innate Immunity) 60
1.6.1.2 Acquired Immune Responses (Adaptive Immunity) 62
The Biology of Parasites, First Edition. Richard Lucius, Brigitte Loos-Frank, Richard P. Lane, Robert Poulin,
Craig W. Roberts, and Richard K. Grencis.
© 2017 Wiley-VCH Verlag GmbH & Co. KGaA. Published 2017 by Wiley-VCH Verlag GmbH & Co. KGaA.
1 General Aspects of Parasite Biology
1.6.1.3 Scenarios of Defense Reactions Against Parasites 63
1.6.1.4 Immunopathology 67
1.7.1 Alterations of Host Cells 78
1.7.2 Intrusion into the Hormonal System of the Host 79
1.7.3 Changing the Behavior of Hosts 82
1.7.3.1 Increase in the Transmission of Parasites by
Bloodsucking Vectors 83
1.7.3.2 Increase in Transmission Through the Food Chain 83
1.7.3.3 Introduction into the Food Chain 88
1.7.3.4 Changes in Habitat Preference 92
Introduction to Parasitology and Its Terminology
Parasites are organisms which live in or on another organism, drawing sustenance from the host and causing it harm. These include animals, plants, fungi,
bacteria, and viruses, which live as host-dependent guests. Parasitism is one of
the most successful and widespread ways of life. Some authors estimate that more
than 50% of all eukaryotic organisms are parasitic, or have at least one parasitic
phase during their life cycle. There is no complete biodiversity inventory to verify
this assumption; it does stand to reason, however, given the fact that parasites live
in or on almost every multicellular animal, and many host species are infected with
several parasite species specifically adapted to them. Some of the most important
human parasites are listed in Table 1.1.
The term parasite originated in Ancient Greece. It is derived from the Greek
word "parasitos" (Greek pará = on, at, beside; sítos = food). The name parasite was
first used to describe the officials who participated in sacrificial meals on behalf
of the general public and wined and dined at public expense. It was later applied
to minions who ingratiated themselves with the rich, paying them compliments
and practicing buffoonery to gain entry to banquets where they would snatch
some food.
Table 1.1 Occurrence and distribution of the more common human parasites.
Infected people (in millions) Distribution
Giardia lamblia
Entamoeba histolytica
Trypanosoma brucei
Trypanosoma cruzi
Leishmania spp.
Toxoplasma gondii
Plasmodium spp.
Paragonimus sp.
Schistosoma sp.
Hymenolepis nana
Taenia saginata
Trichuris trichiura
Strongyloides stercoralis
Enterobius vermicularis
Ascaris lumbricoides
Ancylostoma duodenale and
Necator americanus
Onchocerca volvulus
Wuchereria bancrofti
Worldwide in warm climates
Sub-Saharan Africa ("Tsetse
Belt")
Near + Middle East, Asia, Africa,
Africa, Asia, Central and South
Africa, Asia, South America
Asia, Africa, South America
Sub-Saharan Africa, Central and
Worldwide in the tropics
Source: Compiled from various authors.
*many of those asymptomtic or infected with the morphologically identical Entamoeba dispar.
The result was a character figure, a type of Harlequin, who had a fixed role to
play in the Greek comedy of classical antiquity (Figure 1.1). Later, "parasitus" also
became an integral part of social life in Roman antiquity. It also reappeared in
European theater in pieces such as Friedrich Schiller's "Der Parasit." In the seventeenth century, botanists were already describing parasitic plants such as mistletoe
as parasites; in his 1735 standard work "Systema naturae," Linnaeus first used the
term "specie parasitica" for tapeworms in its modern biological sense.
The delimitation of the term "parasite" to organisms which profit from a heterospecific host is very important for the definition itself. Interactions between
individuals of the same species are thus excluded, even if the benefits of such interactions are very often unequally distributed in the colonies of social insects and
naked mole rats, for instance, or in human societies. As a result, the interaction
between parents and their offspring does not fall under this category, although the
direct or indirect manner in which the offspring feed from their parent organism
can at times be reminiscent of parasitism.
Figure 1.1 Parasitos mask, a miniature of a theater mask of Greek comedy; terracotta,
around 100 B.C. (From Myrine (Asia Minor); antiquities collection of the Berlin State Museums. Image: Courtesy of Thomas Schmid-Dankward.)
The principle of one side (the parasite) taking advantage of the other (the host)
applies to viruses, all pathogenic microorganisms, and multicellular parasites
alike. This is why we often find that no clear distinction is made between
prokaryotic and eukaryotic parasites. With regard to parasites, we usually do not
differentiate between viruses, bacteria, and fungi on the one hand and animal
parasites on the other; we tend to see only the common parasitic lifestyle. Even
molecules to which a function in the organism cannot be assigned are sometimes
described as parasitic, such as prions, for example, the causative agent of spongiform encephalopathy, or apparently functionless "selfish" DNA plasmids that are
present in the genome of many plants. Many biologists are of the opinion that
only parasitic protozoa, parasitic worms (helminths), and parasitic arthropods are
parasites in the strict sense of the term. Parasitology, as a field, is concerned only
with those groups, while viruses, bacteria, fungi, and parasitic plants are dealt
with by other disciplines. This restriction clearly hampers cooperation with other
disciplines, something that seems antiquated in today's modern biology, where
all of life's processes are traced back to DNA; it is gratifying that the boundaries
have relaxed in recent years. However, eukaryotic parasites are distinguished
from viruses and bacteria by their comparatively higher complexity, which
implies slower reproduction and less genetic flexibility. These traits typically drive
eukaryotic parasites to establish long-standing connections with their hosts,
using strategies different from the "hit-and-run" strategies used by many viruses
and bacteria. For these reasons, and for the sake of clarity and tradition, only
parasites in the stricter sense of the term, that is, parasitic protozoa, helminths,
and parasitic arthropods are dealt with in this book.
Types of Interactions Between Different Species
The coexistence of different species of organisms involves interactions among
them that take many different forms in which the benefits and costs are often very
unevenly distributed. Both partners benefit from mutualistic relationships, while
in antagonistic relationships the advantage lies with only one side. However, a
direct relationship between two species is seldom completely neutral. Different
types of interactions are not always easy to distinguish, such that transitions
between them are often fluid and the differences subtle. The spectrum of the
partnerships between different organisms can be best illustrated by the use of
concrete examples.
1.1.2.1 Mutualistic Relationships
If different partners rely on their coexistence and are limited in their viability or
even nonviable when separated, this close association is described as a symbiosis
(Greek: sym = together, bíos = life). For example, Lichens – a combination of fungi
and photosynthetically active algae – can only colonize completely new habitats in this combined form. Another example is the partnership of termites with
cellulose-digesting protozoa, which live in the intestinal blind sacs of the hosts.
The metabolites of the protozoa complement the hosts' rather unbalanced diet.
When the two partners benefit from coexistence without losing the ability to live
independently, it is known as mutualism. A close mutualistic relationship exists
between clown fish (anemone fish) and sea anemones: the fish can gain protection from predators by snuggling into the tentacles of the sea anemones without being attacked by the latter's poisonous stinging cells (Figure 1.2) and always
returns to the anemone when danger threatens. The sea anemone benefits in turn
Figure 1.2 A clown fish in the tentacles of a sea anemone. The partners form a mutualistic
symbiosis, but they can also survive independently. (Image: Richard Orr, courtesy of Random
House Publishers, Munich.)
Figure 1.3 The pearlfish Carapus (syn. Fierasfer) acus lives in the water lungs of sea cucumbers. (Edited from Oche G. (1966) "The World of Parasites", Springer-Verlag Heidelberg.)
from the food remnants of the fish. Another example of a less intimate mutualistic association is the interaction between Cape buffalo and the cattle egret.
While grazing, a buffalo flushes out insects, which are then snapped up by the
egrets – and the danger-sensitive birds warn the buffalo by flying up when they
spot big cats approaching.
Commensalism describes a feeding relationship, in which one partner benefits
without providing any reciprocal benefits nor imposing any cost to the other. The
commensal draws sustenance from the host's waste materials or from the components of the host's food, which are of no value to it. The flagellates that reside in
the anal canals of arthropods provide an example, because these are areas of the
digestive system where no more food absorption takes place.
However, there are symbiotic relationships in which a host is merely used as a
living place. This involves organisms settling on the external surfaces of a different
species (e.g., barnacles on crabs and shellfish), or even inside the host's body. One
example of this is the pearlfish, a member of the cod family, which can grow to a
length of approximately 20 cm. The fish lives in the water lungs of sea cucumbers
into which it skillfully wriggles, pointed tail first (Figure 1.3). Pearlfish only leave
their hosts to forage and reproduce.
1.1.2.2 Antagonistic Relationships
When a guest organism extracts nutrients from its host – and the host incurs a
cost from the relationship – it is known as parasitism. Parasites can also cause
damaging effects such as injury, inflammation, toxic metabolite, and other factors,
Figure 1.4 Coexistence of a typical parasite with its host. Tapeworms draw nourishment
from their host and exploit the host in the long term – they are, however, only moderately
pathogenic. (De bouche à Oreille by Claude Serre © Editions Glénat 2016)
and result in reduced evolutionary fitness of the host, even if the effects are only
slight. Adult tapeworms may be regarded as typical examples here: they absorb
nutrients from the digested food in the small intestine of the host, thereby harming
the host, but do not attack its tissues. The host is thus weakened a little, but not
killed, and the parasite lives of the interest without touching its capital. Claude
Serre expresses all these qualities very aptly in his cartoon (Figure 1.4). Parasites
are usually smaller and more numerous than their host, whereas predators are
larger and less numerous than their prey. When one parasite settles on another, we
call this hyperparasitism. Nosema monorchis, for example, a single-cell organism
of the phylum Microspora, parasitizes the digenean Monorchis parvus, which is
itself a parasite of fish.
We usually expect an intimate, physical relationship between parasite and
host. Intimate contact like this exists in endoparasitism and (in many cases)
ectoparasitism. There are also forms of parasitism in which the physical contact
between the partners is less intimate, where the parasite does not exist as a
pathogen, but exploits the host in other ways. The exploitation of interactions
between members of social organisms is defined as social parasitism. In the
case of social insects such as ants, the interactions of a host species are exploited
by a parasitic species. The spectrum of social parasitism ranges from food theft
to slavery and the targeted assassination of the queen, which is then replaced
by the queen of a parasitic species. One specific form of social parasitism is the
exploitation of a different species to rear one's own offspring, which is known
as brood parasitism. A well-known representative of the brood parasites is the
Figure 1.5 Brood parasitism: A young cuckoo is fed by a warbler. (Image: Courtesy of
Oldrich Mikulica.)
Figure 1.6 Phoresy: Mites latch on to a sexton beetle, "hitching a ride" to the nearest carrion. (Drawing from a photo by Frank Köhler.)
cuckoo (Cuculus canorus). The female of the species lays its eggs in the nests
of smaller songbirds to have them raise its young ones (Figure 1.5). The cuckoo
bee's behavior is very similar. Cuckoo bees account for 125 of a total of 547
species of bees in Germany – a fact that says much for the success of this form
of parasitism. Not only food but also functions such as transportation can be
exploited by parasites. For instance, some mites and certain nematodes latch on
to insects for transportation. In this type of parasitism, phoresy, the carriers are
referred to as transport hosts (Figure 1.6).
Parasitoidism occurs when the death of the host is almost inevitable following parasitic exploitation. One typical example of this involves ichneumon wasps,
which lay their eggs on caterpillars. When the young wasps hatch, they feed on
the host's tissues (Figure 1.7). The parasitic wasp larvae first devour the body fat,
and then eat the muscle tissue and finally kill their hosts by consuming the neural
Figure 1.7 Parasitoidism: A parasitic wasp of the genus Ichneumon lays its eggs in a caterpillar. (From a photo in "The Animal Kingdom," courtesy of Marshall Cavendish Books Ltd.)
tissue. The larvae finally break out of the caterpillar and pupate. A parasitoid like
this attacks the capital, rather than living of the interest. However, it does exploit
the host for a relatively long period of time and only kills it when the parasitoid is
finished with it.
The interaction between parasitoids and their host shows some similarities
to predator–prey relationships, for example, between a lion and wildebeest
(Figure 1.8). However, whereas the parasitoid only kills its host after eating most
of it, the prey is immediately killed by the predator and then eaten. In addition,
predators are typically larger than their prey, and consume more than one prey in
their lifetime, two features that separate them from parasites.
Figure 1.8 Predator–prey relationship: A lion attacks a wildebeest. (Image: Ingo Gerlach,
www.tierphoto.de.)
Different Forms of Parasitism
Organisms, which can live as parasites, but are not necessarily dependent on
the parasitic mode of life represent facultative parasites. One example is the
bloodsucking kissing bug, Triatoma infestans. It can also live as a predator by
sucking out the hemolymph of smaller insects. Obligate parasites have no
alternative other than their way of life. In the case of some organisms, only one
sex lives parasitically. In mosquitoes, for instance, only the females need a meal of
blood to produce eggs; the male feeds on the sap of plants. Permanent parasites
are parasitic in all stages of their development, while temporary parasites spend
only certain phases of their life in a host.
An ectoparasite attaches to the skin or other external surfaces (e.g., the gills) of
its host, where it subsists on hair or feathers, feeds on skin, or sucks blood or tissue
fluid substance. Included among ectoparasites are numerous temporary parasites (sometimes called micropredators), which only seek out their hosts to feed
(e.g., bloodsucking mosquitoes), and many permanent parasites that remain in
constant contact with their hosts (e.g., lice, or the monogeneans parasitic on fish).
Parasites that live inside their hosts are known as endoparasites. The worms living in the gut lumen of vertebrates illustrate the simplest form of endoparasitism.
The difference between rotting substances in the outside world and the contents of
the digestive tract is not particularly significant and it is relatively common to find
organisms that have adapted to endoparasitism of this type. One example of these
residents of the gut lumen is the nematode Strongyloides stercoralis, the life cycle
of which illustrates that it has the option of either the free-living or the parasitic
modes of life. Other endoparasites either live in organs (such as the great liver fluke
Fasciola hepatica), live freely in the blood of their hosts (such as Trypanosoma
brucei), or inhabit body tissue (such as the filarial nematode Onchocerca volvulus).
Intracellular parasites induce very pronounced changes in the host cell: using
these highly specific mechanisms, these parasites (e.g., Leishmania and Plasmodium) invade host cells, reorganize them to fit their own needs, and exploit this
extreme ecological niche due to a multitude of adaptations.
As an adaptation to their modes of life, many parasites have evolved complex
life cycles, which include switching between multiple hosts and sexual and
asexual reproduction (Figure 1.9). In the simplest forms of parasitism, only
one host is exploited; these parasites as referred to as monoxenous (Greek
mónos = single, xénos = foreign). In this case, transmission from one host to the
next takes place among members of the same host species, and is referred to
as direct transmission. By contrast, indirect transmission occurs when the
parasite switches between two or more host species. These parasites are known
as heteroxenous (hetero = differing); their complex cycles require two or three,
sometimes even four, host species, depending on the parasite. By switching hosts
from one stage of their life cycle to the next, heteroxenous parasites achieve
greater overall fitness, or transmission efficiency, than they would by utilizing
a single host per generation. For example, the use of bloodsucking mosquitoes
Final host
Intermediate host
Monoxenous
Diheteroxenous
Figure 1.9 Life cycles of parasites. Left:
Monoxenous cycle with one host, for
example, Ascaris lumbricoides. Center: Heteroxenous cycle with final and intermediate
Triheteroxenous
hosts, for example, Trypanosoma brucei.
Right: Heteroxenous cycle with final host and
two intermediate hosts, for example, Dicrocoelium dendriticum.
as vectors, that is, carriers of the parasite between vertebrate hosts, results
in a much higher level of efficiency in the transmission of malaria than has
been measured in highly contagious viral diseases transmitted through direct
transmission. The evolution of complex life cycles from what originally were
simple ones has occurred in several unrelated parasite lineages, ranging from
microorganisms to multicellular parasites, through the stepwise addition of a
new host whenever this was favored by natural selection.
Modes of reproduction vary greatly among parasites, and many parasite
species can switch from one reproduction mode to another during their life
cycle. When a parasite alternates between sexual and asexual reproduction, this
is known as metagenesis. The Apicomplexa, alternating between schizogony
(asexual), gamogony (sexual), and sporogony (asexual), is a good example of
metagenesis. Switching from sexual to asexual reproduction (i.e., parthenogenesis = virgin birth) is also seen in some intestinal nematodes, such as Strongyloides
stercoralis, for instance; its life cycle illustrates a change between generations
of parthenogenetically reproducing parasitic females and free-living sexually
reproducing worms. Among sexually reproducing parasites, hermaphroditism is
a common strategy, in which individual parasites possess both male and female
reproductive organs. This is the case among platyhelminths such as tapeworms
and flukes (except the blood flukes, or schistosomes). Hermaphrodites have the
great advantage of being capable of reproduction even if they cannot find another
member of their species in a host, by self-fertilization.
Parasites and Hosts
In heteroxenous life cycles a distinction is first made between the final host
and intermediate host. Sexual reproduction takes place in the final (definitive)
host. Some confusion in terminology can occasionally arise with this definition;
for plasmodia, for example, the more important host from an anthropocentric
viewpoint is the human being. However, fertilization takes place in the mosquito,
and hence the insect must be regarded as the definitive host. Another part of
the life cycle of parasites takes place in the intermediate host, where significant
developmental processes or asexual reproduction occur. This is the distinguishing
factor between intermediate hosts and pure transmission agents (vectors), which
transmit pathogens mechanically (e.g., through the stylets of bloodsucking
insects). Several intermediate hosts may be exploited in succession during a
life cycle, and these are known as first or second intermediate hosts. In some
life cycles, a host individual plays the roles of the final and intermediate hosts
simultaneously, as observed in the case of the nematode Trichinella spiralis.
The trichina reproduces sexually in the gut of its host (final host function), and
then forms resting stages in a completely different compartment, the muscle cell
(intermediate host function). In many cases, transmission from intermediate to
definitive hosts occurs by predation of the former by the latter. The larval stages
of some parasites can also be transmitted from smaller to larger intermediate
hosts through the food chain, without any significant morphological changes
occurring. Such hosts, known as paratenic hosts, accumulate the larvae, and
their insertion in the life cycle facilitates transmission of these larvae to the
definitive host.
At each stage of their life cycle, many parasites are optimally adapted to a particular host species, which may represent their main host in fat, that is, the one
they have coevolved with for a long time. On this host, growth and reproduction
are optimal and the parasite enjoys a long life cycle. By contrast, living conditions
are worse for the parasite in alternative host in fat that nonetheless allow the survival of the parasite, with the result that these hosts play a less significant role in
the perpetuation of the life cycle. These alternative hosts, however, may serve as
reservoir hosts in fat and be of major epidemiological importance – when control measures have been used on the main host, for example, chemotherapy on
farm animals, the parasite cycle in wild reservoir hosts cannot be eradicated and
a reinfection may take place via these hosts. By contrast, parasite development
stages can sometimes occur in a wrong host or dead-end host, where no further
transmission can take place (e.g., Toxoplasma gondii in humans).
One indispensable basis for the establishment of a host–parasite relationship
is the susceptibility of the host. Susceptibility is essentially determined by the
behavioral, physiological, and morphological characteristics of the host, and
also by the host's innate and adaptive immune responses. Within a population, therefore, the host genotype often determines the individual degree of
susceptibility – certain hosts may thus be predisposed for infection. Acquired
characteristics, such as physical condition or age, can also affect an individual
host's susceptibility to parasites.
Host resistance to a parasitic infection can depend on the immune responses
of the host. This becomes clear when a host only becomes susceptible when elements of the immune system are disabled. For example, Aotus monkeys – used as
experimental animals in malaria vaccine research – can only be reliably infected
after splenectomy. However, resistance can also be defined by biochemical factors.
T. brucei, for instance, is killed by a protein in human serum, which is associated
with high-density lipoproteins. Immunity is the term used when a past infection
leaves behind protective immune responses. In the case of parasitic infections,
an existing infection often provides immunity to further infections. A concomitant immunity (premunition) like this permits already-established parasites to
survive, but leads to the elimination of new infective stages trying to infect the
host. This situation can cause parasite density to be downregulated to a tolerable level for the host. Hosts with defective immune systems are often more susceptible to parasites; these hosts may consequently be colonized by opportunistic pathogens, which are present only in low densities or not at all in immunocompetent individuals. Such opportunistic parasitic infections are common in
AIDS patients – and in many cases, these infections are the direct cause of death.
Examples of this are the frequent occurrence of Toxoplasma gondii, Cryptosporidium parvum, and Leishmania species in AIDS patients and other immunocompromised persons.
Parasites can specialize in varying degrees in the way they exploit their hosts.
The degree of specialization is expressed in the host specificity, which combines
the number of host species that can be used at any stage of the life cycle, and the
relative prevalence and intensity of infection by the parasite on these hosts. For
instance, parasites that can infect only one host species or infect a few host species
but achieve high prevalence and intensity on only one of these species have a high
degree of host specificity ("narrow host specificity"). Feather lice (Mallophaga, see
Section 4.4.2) are one example of highly host specific parasites. They are not only
adapted to a particular host species omit – they can only colonize certain parts
of the host bird's body (Figure 1.10). Other highly host-specific parasites include
omit the larval stages of digeneans (flukes) for their molluscan first intermediate
host. By contrast, parasites with wide host specificity can colonize a wide range of
hosts successfully, and often achieve high prevalence or intensity of infection on
many of these hosts. For example, certain stages of Trypanosoma cruzi and Toxoplasma gondii exploit almost all mammals as hosts and invade almost all types
of the hosts' nucleated cells. Relying on the host range combined with information on prevalence and intensity of infection as a measure of specialization can
be, however, misleading. Let us consider two related parasite species, A and B,
each using four host species and achieving almost equal prevalence and intensity in all their hosts. However, the hosts of parasite A belong to distantly related
families, whereas those of parasite B all belong to the same genus. Therefore, we
can easily argue that parasite B displays higher host specificity than A, since its
hosts are restricted to a narrower phylogenetic spectrum. Host specificity is the
outcome of colonization of new hosts and adaptation to these hosts over evolutionary time, and the more host-specific parasites are those that cannot make
the large jump necessary to colonize animal species not closely related to their
main host. In this context, several parasites have made the "jump" from wild or
domestic animals to humans; diseases caused by parasites transmitted between
vertebrates and humans under natural conditions are referred to as zoonoses (e.g.,
Figure 1.10 Distribution of various Mallophaga species on an Ibis (Ibis falcinellus),
an example of high specificity for particular habitats on a host individual. (a) Ibidoecus bisignatus. (b) Menopon plegradis.
(c) Colpocephalum and Ferribia species. (d)
Esthiopterum raphidium. (From Dogiel, V.A.
(1963) Allgemeine Parasitologie (General Parasitology), VEB Gustav Fischer Verlag, Jena.)
T. spiralis, transmission between pigs and humans; and Taenia saginata, transmission between cattle and humans).
The establishment of parasites in a susceptible host results in an infection. In
strict context, this term applies only if an increase in the number of parasites
occurs by replication of the original parasite within the host, as in the case of protozoa. However, the term is now widely used in the case of helminths (worms)
or arthropod parasites, too, where only one mature parasite develops from each
infective larva. The term formerly used for these groups is "infestation." The period
during which diagnostically relevant parasite stages appear, such as plasmodia in
the blood, is known as patency. The period from infection to patency is called
prepatency or the prepatent period, while the period until the onset of the first
symptoms is known as the incubation period. For helminth parasites, prepatency
corresponds to the period from initial infection of the host to the onset of egg production, when eggs start appearing in the feces or urine of the host; patency then
corresponds to the adult life of the worm, from the onset of egg production to
its death. In accordance with an international agreement, the infection and the
resulting disease are known by the name of the parasite with the suffix -osis, for
example, toxoplasmosis. However, for many diseases the suffix-iasis is in wide use.
The term used when an infection with the same pathogen occurs after a
parasitosis has healed is reinfection. An infection contracted in addition to
an existing parasitosis and caused by the same species of parasite is known as
superinfection. Simultaneous infections with multiple pathogen species are
known as mixed infections. Both superinfections and mixed infections have
consequences for host welfare, as the overall harmful effect on the host may
depend on additive or synergistic effects between the different infections. If a
host infects itself with stages that originate from its own infection, it is called
autoinfection; an example of this is autoinfection with the pinworm Enterobius
vermicularis.
The harmful effect which the host suffers from parasites may have different
causes and manifestations, and is measured in different ways by different groups
of researchers. As a measure of the impairment caused by parasites, evolutionary biologists use the reduction in the host's genetic fitness attributable
to infection. This decrease in host fitness is referred to as the virulence of the
parasite, and is quantified as the relative difference between the reproductive
capacity of the infected host compared to what reproduction it could achieve
without the infection. In the assessment of medical importance, the parameters
morbidity (incidence of disease) and mortality (incidence of death) are used. A
quantification is determined by calculating the disability-adjusted life years
(DALYs); this is a WHO index into which up to 140 individual parameters
flow for the assessment of a disease. Finally, the harmful effect of parasitic
infections in livestock is calculated by determining the loss of productivity (e.g.,
milk yield in cows and wool production in sheep) and the cost of infection
At a physiological level, parasitic infections usually have a pathogenic impact
or effect; this is generally described as pathogenicity and the defined molecular
factors that are important in this context are called pathogenicity factors. The
amoebapore protein produced by Entamoeba histolytica is a pathogenicity factor,
since it plays a crucial role during tissue invasion. The term used for the quantitative expression of pathogenicity is virulence (Latin virulentus = full of poison),
which was originally a means of assessing a pathogen's degree of aggressiveness.
Unfortunately, the same term is used by evolutionary biologists to refer to the parasite's effect on host genetic fitness. From a physiological perspective, the host is
therefore not only harmed by food deprivation – the destruction of cells or tissues
through the action of toxic metabolic products and immune responses that harm
the host's own tissue (immunopathology) also cause damage. It used to be thought
that phylogenetically ancient parasite–host relationships should be characterized
by a relatively low pathogenicity, since parasites which only minimally harm their
hosts may persist longer over the course of evolution. However, following both
theoretical work and experimental studies with fast-evolving pathogens, it is now
accepted that the pathogenicity (or virulence in its evolutionary sense) of parasites can increase over the course of evolution. Indeed, under a range of circumstances, natural selection can favor aggressive exploitation of the host, resulting in
high parasite replication and transmission rates, at the expense of long-term host
survival.
Modes of Transmission
Due to the different varieties of parasitic organisms, modes of transmission are
very diverse. The simplest form of transmission is by direct contact, for example,
through contact with the skin, such as in mites or lice. One special case of contact infection is sexual transmission, as in the case of infections caused by Trichomonas vaginalis and Trypanosoma equiperdum.
Many life cycles of parasites are based on oral infection, that is, the intake
of infective stages via the mouth. Intake can occur via the food chain and foodstuff – a process known as alimentary infection, or in ecological terms, trophic
transmission. Some of these cycles are based on a predator–prey relationship
between the intermediate and definitive hosts (e.g., catching of mice by the
final host, the fox, which simultaneously ingests metacestodes of Echinococcus
multilocularis, the fox tapeworm). Transmission from an intermediate host to
a plant-eating definitive host requires a slight adjustment; here, the parasite
stages leave the intermediate host to encyst on food plants (Fasciola hepatica:
encystment on wetland plants). Infection by fecal-oral contamination occurs
when infective stages derived from feces (e.g., amoeba cysts, coccidia oocysts,
and nematode eggs) are ingested orally; diverse media such as contaminated
water, food, and air (airborne transmission) can be used as transmission media.
Since transmission is usually left to chance in fecal-oral infections, large numbers
of infective stages are typically produced by parasites using this route (e.g.,
several billion Cryptosporidium parvum oocysts per kilogram of cattle dung).
Infections occurring through other body orifices such as the nose, ear, eye,
rectum, genital apertures, and wounds are less common. One important decisive
factor in whether or not infective stages are successful in transmission is their
persistence in the external environment, that is, the infective stages' resistance to
environmental influences such as extremes of temperature, desiccation, salinity,
and the effects of chemical exposure.
Percutaneous infection or skin penetration plays an important role, particularly in helminth infections. In these cases, infective stages in the soil or water
actively bore into the skin of the final or intermediate host (e.g., the cercariae of
schistosomes and other digeneans, the infective larvae of the hookworm Ancylostoma duodenale).
One highly targeted and therefore extremely efficient mode of transmission
occurs through the use of vectors (Latin vectus = carried) in the life cycle of many
parasites, mostly those living in the blood of vertebrates. This may be purely
mechanical, such as the transmission of Trypanosoma equinum via the lancets
of tabanid flies. More commonly, however, the transmitting organisms have a
function as hosts, for instance bloodsucking arthropods that ingest the parasites
with their blood meal, with part of the parasite's development occurring inside
the vector (e.g., malaria parasites inside the mosquito). Other bloodsucking
animals can also serve as vectors of parasites, including leeches and vampire bats.
Many of the aforementioned transmission modes (direct contact, sexual transmission, fecal-oral contamination, transmission by vectors) enable transmission
from one host individual to any other within a population, which is known as
horizontal transmission. By contrast, vertical transmission occurs when the
infection is passed on to the offspring from the mother, that is, across generations. In congenital infection, parasites infect the offspring of a host in the womb
or during birth. For example, some parasites migrate through the placenta to the
fetus (e.g., Toxoplasma gondii).
The transmission pattern characterizing the spread of diseases and the quantification of all processes associated with transmission of parasites are studied in
the science of epidemiology (Greek epí = via, dē mos = people). If a specific study
involves animal diseases, the veterinary term epizootiology (Greek zō on = living
creatures) is used. One commonly used measure of infection is its prevalence,
that is, the proportion of individuals in a population that are infected at a particular point in time. The incidence of an infection refers to the number of new cases
occurring over a period of time. The intensity of infection indicates the number
of parasite stages per host. In recent years, the science of epidemiology has relied
increasingly on mathematical models to predict the spread of diseases through
a population, given some basic parameters such as host population density and
parasite transmission efficiency. This growing theoretical framework provides us
with the means to forecast the potential effects of climate change and other environmental factors on the future dynamics of diseases.
Goater, T.M., Goater, C.P., and Esch,
G.W. (2014) Parasitism: the Diversity and Ecology of Animal Parasites,
2nd edn, Cambridge University Press,
Cambridge.
Loker, E.S. and Hofkin, V. (2015) Parasitology: A Conceptual Approach, Garland
Mehlhorn, H. (ed.) (2007) Encyclopedia
of Parasitology, Springer-Verlag, Berlin,
Heidelberg, New York.
Poulin, R. (2007) Evolutionary Ecology of
Parasites, Princeton University Press,
Princeton, NJ.
Poulin, R. (2011) The many roads to parasitism: a tale of convergence. Adv.
Parasitol., 74, 1–40.
Test Questions
How is the term parasite defined?
Which major groups of eukaryotic parasites are generally recognized?
What is the difference between symbiosis and parasitism?
Give examples of temporary parasites and permanent parasites.
What is the difference between monoxenous and heteroxenous parasites?
Which phase of a life cycle takes place in the final (definitive) host?
What is a paratenic host?
Does a parasite with narrow host specificity infect many or a few species?
How do we refer to the phase during which parasite stages are detectable in
the host, like in the blood, for instance?
10. What is a zoonosis?
11. What is the difference between horizontal and vertical transmission?
What Is Unique About Parasites?
A Very Peculiar Habitat: The Host
Parasites, in contrast to free-living organisms, occupy a very special ecological
niche, namely a living host. On closer inspection, the host is, particularly in the
case of endoparasites, an extreme habitat, which, in relation to its inhospitality,
can doubtlessly be compared to a salt spring or deep-sea vent. The environment
of the small intestine, for instance, in which tapeworms and other parasites live,
is characterized, among other things, by oxygen deficiency, high concentration
of active digestive enzymes, high osmolarity, and immune responses of the host.
Yet, apparently compensating for these harsh conditions is the high abundance
of nutrients. In order to be able to exploit such a habitat in the long run, morphological, physiological, and other adaptations are necessary. Such adaptations
either existed as preadaptations before the ancestral switch from a free-living
existence to a parasitic one, or they evolved rapidly after the transition to parasitism, through intense natural selection. Preadaptations would have originally
evolved in free-living organisms in response to the demands of their particular
habitat; they may have included morphological structures allowing attachment
inside the host intestine, a tough cuticle to resist immune attack, or a metabolism
capable of handling low oxygen availability. Further evolution after switching to a
parasitic mode of life has lead to a strong specialization for parasitism, a universal
feature of parasites. As specialists they exhibit a close relationship with their host.
Therefore, the evolution of parasites proceeds jointly with that of their hosts, while
the hosts, too, are reciprocally influenced by their parasites. This closely coupled
evolution of two species is termed coevolution.
The distinctive feature of parasite–host coevolution is the fact that hosts
respond to infection with parasites, for instance, by developing defense reactions. This is the reason why parasites not only have to adapt to inhospitable
surroundings, but additionally have to evade the host's defense reactions if they
are to survive and reproduce. Thus, an especially strong evolutionary pressure
is exerted on parasites. As they are adapted very specifically to their hosts, they
cannot easily evade this pressure by, for instance, infecting other host species
with lesser defense reactions. Therefore, parasites are forced not only to adapt to
the particular physical and physiological conditions associated with the host, but
also to evade its defensive attacks that are flexible and change over the course of
time (see Section 1.6). Hence, a typical feature of parasite–host interactions is
the antagonism between the partners.
Parasites lower their hosts' genetic fitness and quality of life, acting as competitors for nutrients and exerting pathogenic effects due to lesions, inflammations,
toxic metabolic substances, or merely by occupying space within the body cavity
of the host. In contrast to most viral and bacterial pathogens exploiting their host
only temporarily, the typical eukaryotic parasites persist in their hosts for long
periods of time. For example, intestinal nematodes often live several years in their
hosts, hardly inducing any pathology as long as the worm burden is low. For such
parasites, a high prevalence is typical, meaning a high percentage of infected individuals within a host population over a long time. By contrast, in flu epidemics,
the susceptible individuals of a population become infected, produce viruses for a
short time, and transmit these to their conspecifics, until the germs are eliminated
by the immune system. As soon as protective immunity has developed in a sufficiently large number of individuals, the transmission practically ceases and the
pathogen disappears from the population, only to perhaps reappear later, usually
in an altered form.
The typical long-term strategy of parasitic worms, therefore, is in contrast to
the hit-and-run strategy of many smaller pathogens. However, it should be mentioned that the persistence of parasitic worms in their host is not a singular feature,
as there are also multicellular parasites relying on short-time exploitation, while
some viruses and bacteria live for a long time in their hosts.
Still, why do typical eukaryotic parasites prefer long-term strategies? It is often
claimed that protozoa and particularly helminths, due to their larger body size
and complex genome, have long replication times and thus are less flexible genetically than viruses and bacteria. Although there are counterexamples, it is evident
at first glance that organisms with a small genome and body size replicate more
rapidly – and consequently can also change their genome more rapidly – than
very large creatures (Figure 1.11). As a rough estimate, typical viruses usually possess several dozen genes, bacteria a few thousand, and eukaryotes around 10,000
or more (see also Table 1.2). While Escherichia coli has a generation time of 20 min,
trypanosomes divide only every 6 h and some nematodes need more than 1 year
to attain sexual maturity. Such a long development is not compatible with a hitand-run strategy, but instead favors a long-lasting exploitation of the host.
A parasite's optimal level of virulence may be completely altered when the parasite encounters a novel host species. For instance, an infection with T. brucei, the
causative agent of "Nagana," usually proceeds asymptomatically or with only few
symptoms in wild ungulates, in which the parasite experienced a long coevolution. By contrast, the infection often leads to death in horses and donkeys to which
the parasites are not adapted, as these host species have been relatively recently
introduced into the endemic regions.
The regulation of the parasite population density prohibiting an overcrowding of the host is another requirement for the long-term exploitation of the
host. It has been suggested that some unicellular parasites (e.g., plasmodiids
and trypanosomes) self-regulate their population density to achieve an optimal
utilization of the host, although the underlying mechanisms and molecules are
not yet known. In many species of tapeworms, there exist density controlling
mechanisms, which govern the number or size of the worms. These operate either
by induction of host immunological responses or via molecules secreted by the
tapeworms themselves, which act against their conspecifics. The outcome is that
infections by few worms generally produce of large ones, whereas infections by
many worms result mostly in very small individuals (crowding effect). Besides, it
10 μm
Parasitic
Figure 1.11 Dimensions of various parasitic organisms.
Table 1.2 Genome size and number of protein-encoding genes of some viruses, bacteria,
and eukaryotes.
Escherichia coli (K12)
Encephalitozoon cuniculi
Leishmania major
Cryptosporidium parvum
Babesia bovis
Theileria parva
Schistosoma mansoni
Haemonchus contortus
Brugia malayi
Anopheles gambiae
Number of protein coding genes
Genome size
∼11 500
has been shown in many worm infections that established adult parasites induce
immune reactions to repel superinfections without themselves being damaged.
This premunition ("concomitant immunity") protects already-established parasites against conspecific competitors and simultaneously spares the host from
overwhelming damage.
An infection of long duration requires the correct balance between exploitation
of host resources on the one hand, and parasite growth and reproduction on the
other. Highly pathogenic parasites that quickly kill their hosts have no chances
to exploit them for prolonged periods of time, although they may achieve high
replication rates during their brief use of the host. By contrast, parasites hardly
impairing their host are more likely to prevail for a long time, but their less aggressive exploitation of host resources may only support modest replication rates. The
evolution of parasite virulence toward its host may settle anywhere between these
extremes, depending on the host–parasite association, as natural selection favors
the combination which yields the highest overall transmission success.
Even if many parasites are amazingly well adapted to their hosts, infection
results in a considerable burden for the host, as measured by reduced fitness
(Section 1.3). Consequently, hosts strive to eliminate their parasites. They have
evolved complex defense systems, for instance, innate immune responses or the
adaptive immune system, which, however, cannot provide a complete protection.
Yet, a small number of parasites may not critically diminish host fitness. On the
other hand, parasites are absolutely dependent on their hosts and have to be able
to cope with their defence systems. Thus, the parasite–host relationship is an
asymmetric arms race, in which the benefits of staying ahead appear greater
for the parasites than for the host. As stated earlier, the necessity to adapt to
their host has lead to such a pronounced specialization of parasites that life with
another host species is not possible any more, let alone a return to a free-living
existence (with very few exceptions). Hence, for most parasites, the way back is
blocked and they depend on the host for better or worse.
Specific Morphological and Physiological Adaptations
Parasites have specialized very successfully and accomplished some remarkable
feats of adaptation while doing so. However, these achievements cannot often be
measured accurately against the current benchmarks, so they are seldom appreciated. Konrad Lorenz proposed that parasites do not need to acquire properties
which have been developed by their hosts. They do not have to sing well, for
example, or look attractive or be successful in capturing prey – they have more
subtle skills which, upon closer inspection, are just as impressive as those of their
hosts. For instance, a detailed look at the antigenic variation of trypanosomes or
the induced behavioral changes of the intermediate host, which enable the transmission of the lancet fluke Dicrocoelium dendriticum to its definitive host, reveals
that these parasites deserve the same level of interest as the evolutionary achievements of higher organisms. Parasites have often abandoned the features required
by their free-living ancestors, because the host has taken over the relevant tasks
for them. For instance, consider the loss of the intestinal tract of tapeworms and
acanthocephalans; they can absorb their food from the host in solubilized form
via their outer surface. This loss of features has often led to the assumption that
parasites were simplified versions of their free-living relatives. Indeed, genome
projects have actually shown that increasing specialization is often accompanied
by a reduction of the genome size and the number of protein-coding genes, and
hence well-adapted parasites transfer more tasks to the host. However, there are
counterintuitive examples as the one of Trichomonas vaginalis, with one of the
largest known parasite genomes, coding for 59 681 predicted protein genes. Given
the complex mode of life of certain parasites, we may assume that a general tendency toward a reduction of genomic complexity is accompanied by the acquisition of new functions by the expansion of certain gene families. Any accurate
statement about a possible genomic simplification of multicellular parasites will
only become possible when sufficient genomes have been sequenced to enable
us to compare the complexity of parasites and their free-living relatives with one
In the course of coevolution with their hosts, many parasites have lost structures
that their free-living ancestors still required. The more intimate and prolonged is a
Figure 1.12 Louse flies with varying degrees of wing reduction. (a) Lynchia maura (continuously flight-capable). (b) Lipoptena cervi, sheds its wings when it has alighted on a host.
(c) Melophagus ovinus, wingless. (Compiled from various authors.)
host–parasite association, the more pronounced are the changes. Among insects,
temporary ectoparasites generally have all of their nonparasitic relatives' locomotor organs, while permanent ectoparasites tend to possess reduced wings and their
legs have either been modified into clasping organs or lost completely. Louse flies
are an example of this type of evolutionary change. While Lynchia maura, the
pigeon louse fly, remains winged throughout its life, transferring among hosts at
the adult stage, the deer ked or deer fly, Lipoptena cervi, sheds its wings immediately after finding its host. The sheep louse fly, Melophagus ovinus is stationary,
completing its entire development on the host. It is transmitted by direct contact
and therefore develops no wings at all (Figure 1.12). Similarly, the extremities of
arthropods can be modified and are eventually largely lost with increasing intimacy of the host–parasite association. This can be seen in Demodex folliculorum,
commonly referred to as the eyelash mite, whose grub-shaped body possesses
extremely stubby limbs (see Section 4.2.4.1).
The best example of an extreme loss of morphological characteristics is the parasitic crustacean Sacculina carcini of the order Cirripedia (barnacles). They infest
the European green crab, Carcinus maenas. The female parasite transforms itself
into a network of roots, which pervades the entire body of the crab, absorbing
nutrients which contribute to the development of the parasite's brood sac, the
"externa." This sac-like organ replaces the female crab's egg case under its anal
segments. The host keeps it clean and supplies it with fresh oxygenated water as if
it were its own egg case (Figure 1.13). Male Sacculina larvae penetrate the young
externa and change into extremely reduced dwarf males inside the female. In its
adult stage, Sacculina therefore displays none of the characteristics of a free-living
crustacean. This morphological degeneration has long been considered to be typical of parasites and as such has been given the name "sacculinization." However,
when we consider the complex life cycle of Sacculina – a cycle which has been
only fully understood relatively recently – we realize that this animal is not simplified, but highly specialized. The mode of life of Sacculina is an extreme form of
Figure 1.13 Beach crab with the externa of Sacculina carcini. The brood sac – the only
externally visible part of this extremely modified barnacle – juts out under the anal
segments of the crab. (Image: Courtesy of M. Grabert)
Figure 1.14 Transition to endoparasitism in
barnacles. (a): Barnacle on a firm surface. (b)
Whale barnacle on whale skin. (c) The shark
parasite Anelasma squalicola, forming rootlike extensions that extend into the host's
skin and absorb nutrients. (d) The root system of Sacculina carcini runs throughout the
entire body of the host; the externa is under
the anal segments. (Compiled from various
sources.)
a development which can also be found in other Cirripedia (Figure 1.14). Many
of these barnacles are stuck to rocks and other objects and strain their food from
water, such as the common barnacle Chthamalus stellatus. Related species have
specialized in attaching to moving surfaces, where they live as external symbionts,
such as the "crown" barnacles Coronula diadema, on the skin of whales. Other Cirripedia, for example Anelasma squalicola, which inhabits the skin of sharks, have
evolved into genuine parasites, branching out into the host tissue to absorb food.
The highly specialized endoparasitic lifestyle of Sacculina probably developed in
similar steps.
Reduction or total loss of organs, however, is not exclusive to parasites, but also
occurs in free-living animals. Similar to the gradual loss of wings in ectoparasitic
insects, the loss of legs in whales and snakes is an adaptation, not a retrogressive simplification. Even the gut can be reduced among free-living animals, as
the example of the Pogonophora illustrates. These marine tube worms are related
to the acorn worms. They live in deep-sea vents, where the main food source is
chemotropic bacteria. Pogonophora have lost their gut – they absorb their food
through a tentacle crown. In addition, the loss of sight organs in endoparasitic
flatworms parallels the loss of eyes in fish and crustaceans inhabiting the complete darkness of underground rivers. Thus, basic structures have been reduced
in a range of other free-living as well as parasitic organisms – natural selection
indiscriminately favors the loss of any feature that has become useless ballast due
to a new mode of life. Parasites are not less complex than free-living animals, but
are complex in different ways.
Indeed, some structures that have evolved in parasites are not present in their
free-living relatives, particularly structures serving for anchoring or attachment
to the host. Across all parasite taxa, we find a wide array of impressive hook and
anchor structures or adhesive disks and suckers with which parasites anchor
themselves to the surface of their hosts, in mucous membranes or within cells
(Figure 1.15). The entire body is often flattened to offer as little resistance as
possible. Noteworthy in this respect is the formation of analogous structures
in very different organisms. The common fish louse or carp louse, Argulus, an
ectoparasitic crustacean and the single-celled intestinal parasite Giardia lamblia,
for example, have a plate-shaped flattened body, which is held on the surface
of the fish or the lining of the intestine by suction cups or a suction plate. A
very different convergent development is found in the prehensile legs of true
lice and the ectoparasitic crustaceans (Amphipoda) of whales, the "whale lice."
These analogous structures also reflect the need for the parasite to anchor itself
on the host animal. These are just some of the examples of clear morphological
convergence among unrelated parasite lineages facing similar challenges.
Another striking feature of many helminth parasites is their larger body size
than their free-living relatives. While soil-inhabiting nematodes rarely grow larger
than a few millimeters in length, Placentonema gigantissima, a parasite of the placenta of the sperm whale, reaches a size of between 6 and 9 m. The nematodes
Dioctophyme renale from the kidney of the dog and the Guinea worm, Dracunculus medinensis can grow up to a length of 1 m. In tapeworms, the broad fish
tapeworm Diphyllobothrium latum (up to 20 m in length) is one of the record
holders for length (Figure 1.16, see Section 3.1.2.5). Similarly, a digenean parasitic in the sunfish, Mola mola, reaches length of more than 10 m, dwarfing any
of its free-living flatworm relatives. This evolutionary increase in body sizes is
most apparent in endoparasitic helminths, but is also evident in copepods, where
those taxa ectoparasitic on fish are orders of magnitude larger than their freeliving relatives. These extraordinary body sizes can only come about if nutrients
Figure 1.15 Adhesive and clasping organs
in parasites. (a) Scolex of the pig tapeworm
Taenia solium, front view. (b) Monogenean Gyrodactylus elegans. (c) Monogenean
Polystomum integerrimum. (d) Acanthocephalan, or spiny-headed worm Acanthorhynchus.
(e) Fish leech Piscicola geometrica. (f ) Front
end of the pentastomid, or tongue worm
Leiperia gracilis as seen from the abdomen.
(g) Larva of the pond mussel Anodonta
cygnea. (h) Front end of the larva of a deer
botfly (Cephenomyia). (i) Front end of a Gregarine (Stylorhynchus) from the intestine of a
dragonfly larva. (j) Argulus foliaceus, a crustacean fish louse. (k) Crab louse (Insecta)
of humans (Pthirus pubis). s: Sucker. (From
Hesse-Doflein (1943) Tierbau und Tierleben,
Verlag Gustav Fischer, Jena).)
are present in abundance, and they are seemingly the product of strong selection
for increased gonad tissue and high reproductive output. Given the high mortality
of eggs and larvae that fail to find a host, the reproductive strategy of many parasites is the mass production of offspring. Females of the nematode genus Ascaris
(see Section 3.3.4.6) can each lay up to 200 000 eggs daily – around 70 million
every year. This corresponds to 1700 times the female's body weight – in human
terms, a woman weighing 60 kg would have to produce 102 tons of offspring per
year – and that represents around 25 000 human babies of 4 kg each.
The beef tapeworm Taenia saginata produces up to 10 billion eggs during its
20 years of life, and a large body is necessary for this type of mass production.
Figure 1.16 Length of Diphyllobothrium latum
compared to a medium-sized woman. (Image:
Archive of the Department of Molecular Parasitology, Humboldt University, Berlin.)
Parasites that produce few offspring are usually smaller; one example of this is the
intestinal nematode genus Trichinella. The female has a maximum length of 3 mm
and only produces up to 2500 larvae. In fact, it is the size of reproductive organs in
relation to body size that really matters, as shown by the nematode Sphaerularia
bombi that lives in the body cavity of the bumblebee – the uterus grows outside of
the female and becomes huge, while the rest of the body remains tiny. Since size is
associated with the production of eggs, this also explains the fact that male worms
are often smaller. A well-known example of dwarf males is seen in the nematode
Trichosomoides crassicauda, which is found in the urinary bladder of the rat; the
tiny male is rooted in the uterus of the female. Similarly, in parasitic copepods, the
males are often minuscule compared with the females, being nothing more than
mobile testes.
Flexible Strategies of Reproduction
Parasites that have found a suitable host are generally guaranteed an abundance of
food for the rest of their life. Finding a mate, however, is not always so easy. Given
the relative rarity of hosts and the difficulty involved in infecting them, it is common for a host individual to harbor only a single or very few parasites of a given
species. A solitary life like this is basically unproblematic for unicellular parasites
that can reproduce asexually. For multicellular parasites with sexual reproduction,
finding a mate can be a major challenge, and evolution has favored different solutions to this problem in different taxa. For example, in some types of helminth or
arthropod parasite, once two sexual partners encounter each other, they remain
together and thus avoid the struggle of finding another mate in the future. In schistosomes (blood flukes), the larger male worm fits the smaller female in a special
groove along its ventral surface and keeps it lodged there, allowing the pair to mate
continuously. The female may eventually be usurped by another single male, or
leave its own, but the long-term pairing nevertheless serves to facilitate mating in
conditions where potential mates do not encounter each other often. In some fish
parasites, including copepods (family Chondracanthidae) as well as monogeneans
(family Diplozoidae) and digeneans (family Didymozoidae), the two mates physically fuse together when they first meet, forming a permanent mating association.
There are other adaptive solutions to the problem of rare mating encounters resulting from the uneven distribution of parasites among their hosts. Indeed, some
parasites develop into hermaphrodite adults capable of self-fertilization (selfing),
whereas others have adopted parthenogenesis. The latter mode of reproduction
can also contribute to the rapid development of a population, since there is no
investment in the production of males, which do not produce progeny.
Tapeworms are a good example of hermaphroditism. As protandrous
hermaphrodites, the male sex organs develop first in the young proximal proglottids, while the female reproductive organs only become sexually mature in older,
distal proglottids. This is why a single adult tapeworm can mate with itself. In a
study of Schistocephalus solidus, a tapeworm of the order Diphyllobothriidea, the
reproductive success of selfing was compared with that of cross-fertilization. The
cestode larvae of S. solidus produced by selfing individuals were less successful in
infecting a copepod intermediate host when compared with parasites produced
as a result of cross-fertilization. With regard to infecting copepods, offspring
produced from selfing achieved a lower prevalence and intensity of infection
and a smaller body volume than that achieved by the progeny produced by
cross-fertilization. This difference shows that the genetic quality of offspring
produced by selfing is inferior – for a tapeworm isolated in a host without a
partner, however, this type of reproduction can serve as a stopgap measure for
producing offspring.
Various parasites can make their propagation more flexible through parthenogenesis, such as nematodes of the Strongyloides genus. These nematodes are an
exception to the helminth norm – they are capable of the autoinfection of a host,
which means that a self-perpetuating population can persist in the same host.
The threadworm (pinworm) of the rat, Strongyloides ratti, inhabits the mucosa of
the upper small intestine and, depending on current requirements, can change its
mode of reproduction from producing parthenogenetic, parasitic females to producing dioecious individuals. At the beginning of the infections, parthenogenetic
females are formed almost exclusively; this enables many offspring to be created
when food availability is optimal and immune responses are low. The proportion of
dioecious worms increases with the duration of the infection. The likely explanation for this is that increasing immune responses require greater genetic flexibility.
This has been substantiated in experiments using immunosuppressive treatment
with corticosteroids: In immunosuppressed rats, S. ratti produces more offspring,
in which the proportion of parthenogenetic forms is significantly greater than that
in untreated rats. Parthenogenesis not only solved the potential problem of mate
finding in this nematode, but also allowed it to optimally exploit its host thanks to
the flexibility of its reproductive strategy.
Asexual reproduction is also a major reproductive strategy in a wide range of
parasites. In unicellular organisms, asexual reproduction is often predominant
and may lead to large numbers of offspring. For example, an infection with a few
sporozoites of Plasmodium falciparum, the causative agent of tropical malaria,
may give rise to 1011 merozoite stages. In other unicellular parasites, asexual
reproduction has been considered as the only way of reproduction, but the recent
identification of meiosis-associated genes in some of those protozoans challenges
this view. Asexual reproduction is not restricted to unicellular parasites. In some
platyhelminths, it is used to amplify the number of individuals early in the life
cycle, perhaps as an adaptation to counter the losses incurred during the many
transmission steps of a complex life cycle. Digeneans use asexual multiplication to
increase larval stages in their snail intermediate hosts. In the case of Schistosoma
mansoni, it has been calculated that one miracidium can produce 40 000 cercariae through asexual reproductive steps. In some tapeworms, the metacestodes
have the ability to reproduce asexually, such as the fox tapeworm Echinococcus
multilocularis. Several thousand protoscolices can occur in its larval mass,
each of which will form a very small and relatively short-lived tapeworm in the
intestine of a fox that eats an infected field mouse. In these cases, the parasite
has thus shifted a significant part of its reproduction to the asexual phase in the
intermediate host.
Combes, C. (2005) The art of being a parasite. The University of Chicago Press,
Harvey, S.C., Gemmill, A.W., Read, A.F., and
Viney, M.E. (2000) The control of morph
development in the parasitic nematode
Strongyloides ratti. Proc. R. Soc. London,
Ser. B, 267, 2057–2063.
Kurtz, J. (2003) Sex, parasites and
resistance–an evolutionary approach.
Zoology, 106, 327–339.
Toft, C.A., Aeschlimann, A., and Bolis, L.
(1991) Parasite-Host-Associations. Coexistence or Conflict? Oxford University Press,
Wedekind, C., Strahm, D., and Schärer, L.
(1998) Evidence for strategic egg production in a hermaphoditic cestode.
Parasitology, 117, 373–382.
1. What is the relationship between genome size, and the reproductive behavior
of parasites?
2. Which mechanisms regulate the population density of parasites?
3. Give examples of a reduction of morphological structures in parasites.
4. Why is Sacculina carcini regarded as being a drastically simplified parasite?
5. An increase in parasitic worms' body size provides them with what kind of
6. What is the disadvantage of parthenogenesis?
The Impact of Parasites on Host Individuals and Host Populations
Many ecologists still believe that animal populations are controlled by food abundance, competition, predation, and abiotic factors. They tend to dismiss parasites
as unimportant: parasites are small, hardly visible, and therefore assumed not to
unduly affect the host. The opposite is true, however, as recent research has shown
conclusively. Even parasitoses with low mortality and morbidity, such as flea or
nematode infections, can have a massive impact on the host and its reproductive success – and even affect the structure of host populations as a result. Only
by realizing the extent of this effect, can we understand the evolutionary pressure exerted by parasites on their hosts – and also understand the coevolutionary
processes that have shaped the interaction between parasites and their hosts.
Depending on the particular type of parasite and the intensity of infection, the
effects of a parasitosis vary. These effects are essentially determined by the virulence of the parasite, the susceptibility of the host species, the condition of a
host individual, and its instant response situation. While some parasitoses, such
as sleeping sickness in humans (caused by T. brucei), can induce a very high mortality rate, the impact of other parasite infections is usually so slight that it may be
unnoticed. The skin of around 30% of all people is home to eyelash mites (Demodex
folliculorum), for instance – and they are hardly ever noticed. These widely differing impacts on hosts make it extremely difficult to derive any general conclusion
on the harmful effects of parasites. In addition, parasites such as helminths and
arthropods are not evenly distributed among individual hosts in a population, and
thus not all hosts incur the same effects from the same parasite species. Typically,
a small proportion of hosts in the population harbor large numbers of parasites,
whereas most of the others harbor few or no parasite (see Section 1.4.2). This
aggregated distribution of parasites results from behavioral or physiological variability in the host population, leading to differences among individual hosts in
either their exposure to infective stages, susceptibility to infection, or ability to
mount immune responses following infection. This is why in what follows, we use
some examples to illustrate the impact parasites can have on the performance of
their hosts and on the hosts' progeny – and how they can consequently affect
entire populations. Although these examples do not illustrate universal effects of
parasitism, they nevertheless show the type of impact parasites can sometimes
have on their hosts.
In a series of exemplary studies, researchers led by H. Richner from Bern,
Switzerland, have illustrated the effects of an infection of great tits with the bird
flea Ceratophyllus gallinae. Great tits are particularly suitable for such studies,
because these cavity nesters are often plagued with fleas and the size of their
Not infested
Number of young
Hatched
Figure 1.17 Reproductive success of great tits from nests infected/not infected with Ceratophyllus gallinae. (According to data from Richner, H., Oppliger, A., and Christie, P. (1993) J.
Anim. Ecol., 62, 703–710.)
egg clutches is easily manipulated. Under natural conditions, the number of eggs
varies between 6 and 12, but eggs can easily be removed or added to the clutch.
Tits also readily accept artificial nest boxes. The boxes are first placed into a
microwave oven to remove any flea that is present. A predetermined number of
fleas can then be put into each box for experimental purposes.
The effects of infection by ectoparasites are usually considered to be relatively
low. The behavior of tits searching for nesting cavities shows, however, that flea
infection in a nest box significantly reduces the box's attractiveness to the birds. In
the case of heavily infected nest boxes, fleas surround the entrance hole, forming
a dark ring, ready to infect the bird immediately. Tits in search of nesting opportunities try to avoid nest boxes like this. If a shortage of nesting sites forces a tit
to accept a flea-ridden nesting site, its offspring will have significantly fewer red
blood cells. They are also skinnier and their mortality rate is higher than that of tit
offspring from nests with no flea infection (Figure 1.17). In fact, more eggs are laid
by adults in flea-infected nests than in clean nests to compensate for the higher
mortality of the nestlings, but a significantly smaller proportion of those will survive fledging (Figure 1.17). On average, one more young bird will fledge and leave
a clean nest than a flea-infected nest. In infected nests, the breeding success rate
(measured by the number of fledged young) was only 53% compared with 83%
in clean nests. A pair of great tits which adopts a flea-infected box has therefore
significantly fewer offspring; infection by these ectoparasites – contrary to the
general opinion that they are relatively harmless – considerably diminishes the
fitness of their hosts.
The parent birds also suffer from the consequences of flea infection. In the
experiments, the indirect effects of infection were studied after the female tits
were stimulated to lay an extra egg, corresponding to the situation in a flea-ridden
nest. The additional stress resulted in an increase of 30% (from 20% to 50%) in
Figure 1.18 Scottish grouse, Lagopus lagopus scoticus.
the prevalence of avian malaria in the females, suggesting that the combined
effects of fleas and increased investments in egg production and care caused a
drop in vigilance against mosquito bites or resistance to malaria itself. Similarly,
the male great tits significantly expanded their foraging area when the brood was
artificially increased by two additional hatchlings. The additional effort involved
resulted in the percentage of male great tits infected by Plasmodium increasing
to 40% for flea-free birds and 80% for flea-infested birds. It appeared that few
of the infested males survived through to the following year. They therefore had
significantly lower chances of reproduction than birds in nests without fleas.
Similar experiments with barn swallows and other birds have shown that the
Swiss great tits are no exceptions.
The above experiments show the effect of parasitism at an individual level – but
the impact on host populations can also be impressive. One famous experiment
on host populations was conducted with the Scottish red grouse (Lagopus lagopus
scoticus), which are widespread in the mountain heaths of the Scottish Highlands
(Figure 1.18). The annual Red Grouse hunt is a popular social event. It has always
been celebrated by Scottish landowners, as guests and tourists shooting grouse on
their land provide a tidy income. Records have been kept of the numbers of birds
shot each year, providing long-term data on changes in grouse population abundance. These data show that the population densities of grouse vary considerably
over time, making hunting almost pointless during some seasons. A long-term
study of 175 populations of grouse in different regions of Scotland showed that
population density of grouse goes through a cycle with periods varying between 4
and 8 years (Figure 1.19a). Interestingly, the population density of the grouse was
negatively correlated with infection intensities by the nematode Trichostrongylus
tenuis, which also show variations over time. This parasite is monoxenous, so that
transmission depends heavily on the density of the bird population. The parasite
Number of birds shot
Figure 1.19 Fluctuation in the population
of Scottish grouse due to infection with
the intestinal nematode Trichostrongylus
tenuis. Deworming (arrow) of a proportion
of the birds prevents the decline of populations. (a) Course of events with two control populations; (b) Course of events in
two populations after a single treatment; (c)
Course of events in two populations after
two treatments. (From Hudson, P.J., Dobson,
A.P., and Newborn, D. (1999) Science, 282,
2256–2258 with kind permission of the publisher.)
load of adult birds had a decisive impact: heavy worm infection – as occurs in
dense host populations when transmission conditions are favorable – resulted in a
high mortality rate of the young birds. The intensity of infection with T. tenuis was
obviously reaching a point where the fitness of the birds was decimated, resulting
in a population collapse.
In order to confirm these relationships experimentally, adult birds from six sample grouse populations were caught with nets before the beginning of the breeding
season. The birds in some populations were then given a drug orally to rid them
of worms, whereas birds from control populations were not treated. The grouse
caught amounted to between 15% and 50% of each bird populations. Even this limited action yielded amazing results – in the treated populations, the deworming of
some of the birds prevented the collapse of the populations seen in control populations (Figure 1.19). A mathematical model showed that a single annual deworming
of >20% of the animals was sufficient to prevent population declines and ensure a
relatively high population density. Therefore, there seems to be a critical infection
threshold, above which we observe instability in the host population; it is therefore clear that in this host–parasite system, the parasite regulates the density of
the host population. A similar periodicity is also found in some insect populations, which achieve high densities, only to collapse when parasitoids enter the
equation. These provide real-world examples of the regulatory capacity of parasites predicted by the classical modeling work of Anderson and May in the late
1970s, and echoing back to the earlier demonstration of the potential of predators
to control prey populations provided by Lotka and Volterra in the 1920s.
In cases where populations are regulated by parasites, however, the aforementioned marked periodicity is very rare. This is partly due to the influence
of factors obscuring the influence of infection, such as climate, vegetation, and
human actions. On the whole, however, density regulation by parasites and
other pathogens can play an important role in natural animal populations. It is
noteworthy that in some cases, relatively minor changes to the balance can have
disproportionately strong impact. This finding is important for the design of control programs: if we can keep the prevalence of parasites below a certain threshold
and reduce transmission as a result, a significant decline in parasitosis or even its
eradication can be achieved – and this perhaps with only a modest effort.
In view of the serious effect of parasitic infections on the fitness of hosts
(described above), it is not surprising that the loss of a parasite can be a huge
advantage for a population. Introduced species often bring with them fewer
parasites than they harbored in their original habitats. The house sparrow,
introduced to North America, is infected by only 35 ectoparasite species on
that continent – whereas in its home territory of Europe it has 69 species with
which it must contend. The potential increase in fitness resulting from the loss of
parasites indicates that invasive species are often more successful than in their
original habitat and can spread rapidly as a result. One striking example of this is
the European green crab Carcinus maenas – it has spread all over the world from
its original habitat on the North Sea and Atlantic coasts. In Europe, the growth
and spread of this crab is mainly restricted by the parasitic castrator, Sacculina
Average weight per trap (kg)
Average width (mm)
Figure 1.20 Development of green crabs
from areas with and without their original parasites. (a) Width of shell. (b) Average
weight of crabs in a trap (kg). (From Torchin,
M.E., Lafferty, K.D., and Kuris, A.M. (2001) Biol.
Invasions, 3, 333–345, with kind permission
of the publisher.)
carcini and the feminizing parasitic isopod Portunion maenada. These parasites
do not occur in the new distribution areas and no native parasitic crustacean has
so far switched to exploit C. maenas. Certain trematodes, cestodes, and acanthocephalans – the larvae of which