Chapter 13: Development of an Acquired resistance In rabbits By repeated Infection with an Intestinal Nematode, Trichostrongylus Calcaratus Ransom, 1911.*

The early history of immunoparasitology in the United States

Contributions to the American Society of Parasitologists of some of these pioneers

Literature cited

Chapter 14: Some Practical Principles of Anthelmintic Medication

Chemotherapy of helminth infections: A centennial reflection

Stocking the armamentarium

Learning how medications work

Discovery and evaluation

Consequence and strategy

Overview, with lessons from a bygone century

Acknowledgments

Literature cited

Chapter 15: Anthelmintic drug discovery: Into the future

The future of drug discovery for parasitologists

Phenotypic screens

Mechanism-based screens

Looking ahead from behind: The lessons learned

Literature cited

Part IV: The First Figures Published in

The Journal of Parasitology

Part V: Overview and Conclusions

Chapter 16: Reflections: Closing comments for the centennial celebration of The Journal of Parasitology

Literature cited

Taxonomic index

Index

End User License Agreement

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Guide

Cover

Table of Contents

Preface

Begin Reading

List of Illustrations

Parasitic protozoology and the scientific lessons of intellectual elegance

Figure 1 G. Robert Coatney. Early in his career searching for avian malaria at Peru State College (left, from the 1936

Peruvian

) and 40 years later as President of the American Society of Parasitologists (right, from Coatney, G. R. 1976. Relapse in malaria: An enigma. Journal of Parasitology

62:

2–9). Reproduced with permission from: left—1936

Peruvian

, the Yearbook of Peru State College; and right—with permission of Allen Press Publishing Services.

Figure 2 Robert Hegner. In early mid-career (ca. 1920) at the Marine Biological Laboratory, Woods Hole, Mass. (left, from the Copeland/Bloom photograph album, History and Philosophy of Science Repository, URI: http://hdl.handle.net/10776/3270, Licensed as Creative Commons) and 16 years later as President of the American Society of Parasitologists (right, from Hegner, R. W. 1937. Parasite reactions to host modifications. Journal of Parasitology

23:

1–12). Reproduced with permission of Allen Press Publishing Services.

Figure 3 William Trager in his Rockefeller University Laboratory while President of the American Society of Parasitologists (right, from Trager, W. 1975. On the cultivation of

Trypanosoma vivax

: A tale of two visits in Nigeria. Journal of Parasitology

61:

2–11). Reproduced with permission of Allen Press Publishing Services.

Figure 4 Maynard Mayo Metcalf in a photograph distributed in the press by Science Service during the 1925 “Scopes Monkey Trial”. (Acc. 90–105—Science Service, Records, 1920s–1970s, Smithsonian Institution Archives.)

Figure 5 John Janovy

Jr in the Swallow Barn Laboratory, Cedar Point Biological Station, Keith Co., Nebraska (Courtesy of John Janovy, Jr)

A century (1914–2014) of studies on marine fish parasites published in The Journal of Parasitology

Figure 1 Number of papers on parasites of marine fishes contributed by country. (a) Number of papers on parasites of marine fishes published by country during the first 80 years (1914–1994) of

. (b) Number of papers on parasites of marine fishes published by country during the last 20 years (1995–2014) of

Figure 2 Average effect sizes ( intervals) of time on the number of citations for the sub-disciplines in which the

Journal of Parasitology

is divided. The effect size estimator was the Pearson's correlation coefficient . The values for overall effects are significantly different from zero if the confidence interval (CI) does not overlap zero. For each abbreviation (e.g., System-Phylo), the value of is presented, followed by the lower and upper limits of confidence intervals at 95%, the

-value and the

-value for . The symbol is the overall effect of time on the number of citations for all the sub-disciplines, that in this case was positive and significant (). Abbreviations: System-Phylo, Systematics-Phylogenetics; EcoEpiBent, Ecology, Epidemiology and Behavior; Life cycles, Life Cycle-Survey; Pathology; Therapeutics, Therapeutics-Diagnostics; Molecular Biology, Molecular-Cell Biology; Biochemistry, Biochemistry-Physiology; Functional Morphology; Genetics-Evolution; Invertebrates, Invertebrate-Parasite Relationships.

Figure 3 Comparison of journals similar in scope and impact factor publishing on parasites of marine fishes for the period 1996–2014 (information obtained from the web of science). (a) Percentage of papers published on parasites of marine fishes by five scientific journals with respect to their whole production between 1996 and 2014. (b) Percentage of citations acquired by the papers from (a) for the same time period. Abbreviations: Vet Par,

Veterinary Parasitology

, IJP,

International Journal of Parasitology

, Par Res,

Parasitology Research

, Paras,

Parasitology

, and

The Journal of Parasitology

Figure 4 The relationship between time (independent variable) and the number of citations received by the sub-disciplines in which

is divided (dependent variable) for the period 1914–2014. These models were chosen because they had the lowest values of the Akaike Information Criterion (AIC; data not shown).

Figure 5 Geographical distribution of

Oncomegas wageneri

(Cestoda: Trypanorhyncha) in the southern Gulf of Mexico. (a) Presence (+) and absences (o) of

O. wageneri

on the 162 sampling sites of the oceanographic expedition Xcambo 2 between September and October, 2005. (b). Total number of

O. wageneri

per sampling site. (c) Probability of occurrence of

O. wageneri

using a boosted General Additive Model for the “full area” (n = 162 sampling sites). (d) Probability of occurrence of

O. wageneri

using a boosted General Additive Model for the “polygon area” (n = 134 sampling sites 1500 m depth or above). (e) Probability of occurrence of

O. wageneri

using MaxEnt for the “full area.” (f) Probability of occurrence of

O. wageneri

using MaxEnt for the “polygon area.”

Figure 6 Geographical distribution of

Acanthocephaloides plagiusae

(Acanthocephala: Arhythmacanthidae) in the southern Gulf of Mexico. (a) Presence (+) and absences (o) of

A. plagiusae

on the 162 sampling sites of the oceanographic expedition Xcambo 2 between September and October, 2005. (b). Total number of

A. plagiusae

per sampling site. (c) Probability of occurrence of

A. plagiusae

using a boosted General Additive Model for the “full area” (n = 162 sampling sites). (d) Probability of occurrence of

A. plagiusae

using a boosted General Additive Model for the “polygon area” (n = 134 sampling sites 1500 m depth or above). (e) Probability of occurrence of

A. plagiusae

using MaxEnt for the “full area.” (f) Probability of occurrence of

A. plagiusae

using MaxEnt for the “polygon area.”

An overview of the history and advances in the population ecology of parasites

Figure 1 Schematic representation of the gains and losses in numbers of individuals for a direct life-cycle macroparasite (

) in a hypothetical host (

). Gains and losses in a hypothetical parasite population are defined by parasite birth rate , parasite death rate , transmission rate and by the death of hosts due to infection and other causes (

). (Figure courtesy of Lori Goater, from Goater, Goater & Esch 2014. Reproduced with permission of Cambridge University Press.)

Figure 2 Relationship between parasite intensity and total body lipid (a), and parasite intensity and survival following onset of dropping water temperature (b) for bluegill (

Lepomis macrochirus

) from Reed's Pond, November 1981 through October 1982. Data are for fish held in outdoor aquaria at ambient temperature or in live boxes in the littoral zone. All fish were naturally infected with

U. ambloplitis

. The dotted line indicates the maximum intensity observed for bluegill that overwintered successfully in Reed's Pond. (Reprinted from Lemly and Esch (1984); Reproduced with permission of Allen Press Publishing Services.)

Figure 3 Schematic representation of how host behaviour and parasitism with the nematode

Trichostrongylus tenuis

have direct effects on population processes in red grouse (

Lagopus scoticus

), as well as interactions between them. Solid lines reflect positive interactions and dashed lines reflect negative interactions. Indirect interactions, such as selective predation on parasitized individuals are not shown. Modified from Martínez-Padilla et al. (2014).

History of microevolutionary thought in parasitology: The integration of molecular population genetics

Figure 1 I conducted a Web of Science search on the terms “microsatellite” and either “fish” or “parasite” on March 6, 2014. The search was for each year separately. Extreme caution is advised in strictly interpreting results. All papers may not actually be population genetic studies or may not be using microsatellites in the respective organisms. Indeed, I know the three papers in 1995 under “parasite” are not studies on the population genetics of parasites two are not even on parasites. The Figure is mainly of exploratory value and, while the exact numbers are incorrect, I suspect an approximate 10-year lag would be present even if proper scientific scrutiny were used. Keep in mind the search was only for one group of vertebrates as no one uses “free-living” as a keyword. Inclusion of other vertebrates would only increase the discrepancy. Thus, if anything, I suspect the Figure gives a gross underestimate of parasites relative to free-living animals. I was not able to do a similar analysis for allozymes as Web of Science does not have abstracts or author provided keywords for most papers prior to 1995; thus, word searches will be less inclusive based on titles alone.

The worm's eye view of community ecology

Figure 1 Degree of infection of an individual fish. Redrawn from Figure 1 of Cross (1934) Journal of Parasitology 20: 244–245. Reproduced with permission of Allen Press Publishing Services.

Figure 2 Effects of concurrent infection on the intraintestinal distribution of

Hymenolepis diminuta

and

Monilformis dubius

. Light bars are single infections; dark bars are concurrent infections. Redrawn from Figure 1 of Holmes (1961) Journal of Parasitology 47: 209–216. Reproduced with permission of Allen Press Publishing Services.

Figure 3 Parasite community assembly is influenced by processes operating at a range of spatial and temporal scales. Parasite species are found within a regional species pool that is constrained by evolutionary processes. A subset of the species from the regional pool will colonize a particular site depending on dispersal and exposure probability. This, in essence, suggests that the observed parasite community within a host is the result of infective stages passing through abiotic and biotic filters. Modified from HilleRisLambers, J., P. B. Adler, W. S. Harpole, J. M. Levine, and M. M. Mayfield. 2012. Rethinking community assembly through the lens of coexistence theory. Ann. Rev. Ecol. Evol. Syst., 43: 227–248.

The iron wheel of parasite life cycles: Then and now!

Figure 1 Life cycle of

Haematoloechus parviplexus

Pneumonoecus parviplexus

). (

) 32-day-old adult

H. parviplexus

from the lungs of the bullfrog,

Rana catesbeiana

. (

) Bullfrog, showing the escape of the metacercariae from the dragonfly in the stomach and their migration to the lungs; adult worms depositing eggs and the route of the eggs to the external environment. (

) Egg. (

)

Gyraulus parvus

eating eggs; releasing cercariae. (

) Sporocyst from the digestive gland of

Gyraulus parvus

with cercariae in various stages of development. (

) Cercaria showing body, tail, stylet, oral sucker, pharynx and cecae, ventral sucker, and excretory bladder. (

) Larva of the eastern pondhawk dragonfly,

Erythemis simplicicollis

, showing the swimming cercariae being taken into the branchial basket respiratory organ of the larva. (

) Lamella from the branchial basket of eastern pondhawk dragonfly larva containing two encysted metacercariae. (

) Teneral eastern pondhawk dragonfly with encysted metacercariae within the vestige of the branchial basket of the larva. (

) Encysted metacercaria. Drawings not to scale. All drawings are original but modified after Krull (1930).

Figure 2 Original photomicrographs of the developmental stages of

Halipegus occidualis

. (a) Adult worm (arrow) under the tongue of a green frog,

Rana clamitans

. Scale bar = 1.0 cm. (b) Adult worm full of eggs. Scale bar = 1.5 mm. (c) Egg. Note the long abopercular filament and well developed miracidia. Scale bars = 20 µm. (d) Redia. Note the developing cercariae. Scale bar = 100 µm. (e–f) Cystophorous cercaria. Note the coiled cercaria body (cb), coiled delivery tube (dt), handle (h), encysted tail (t), and inner (iw) and outer (ow) membranes. Scale bars = 20 µm. (g–i) Expulsion of the delivery tube (dt) through the handle (h) followed by the cercaria body (cb) traveling through the delivery tube until its expulsion. Scale bars = 50 µm. (j–k) Metacercariae (arrows) within the hemocoel of

Cyclops

sp. and

Phyllognathopus

sp. copepods. Scale bars = 200 µm in (j) and 10 µm in (k). (l) Metacercaria removed from the intestine of a dragonfly larva. Scale bar = 85 µm.

Figure 3 Original photomicrographs of cercariae of

Haematoloechus

spp. in the process of attaching and penetrating a damselfly host. (a) Free swimming cercaria of

Haematoloechus coloradensis

. Note the stylet. Scale bar = 40 µm. (b–d) Attachment, crawling behavior and penetration of a cercaria of

Haematoloechus coloradensis

on the leg of a larval damselfly. Note the loss of the tail (small arrow) from the cercarial body (large arrow) in the process of penetration in (d). Scale bars = 200 µm. (e–g) Attachment, crawling behavior and penetration of a cercraira of

Haematoloechus longiplexus

on the anal gill of a larval damselfly. Scale bars = 300 µm.

Figure 4 Original photomicrographs of metacercariae of

Haematoloechus

spp. removed from larval dragonflies. (a) Encysted metacercaria of

Haematoloechus coloradensis

. (b) Unencysted metacercaria of

Haematoloechus longiplexus

. Scale bars = 20 µm.

Figure 5 Arthropod host specificity, metacercaria type, and geographical distribution among species of

Haematoloechus

indicated on a phylogenetic tree derived from internal transcribed spacer rDNA data by Snyder and Tkach (2001) and Bolek (2006). Generalist parasites have the ability to form metacercariae in odonate and non-odonate arthropods. Species in gray indicate that the life cycle is unknown. NA = North America; E = Europe.

Figure 6 Variations on the life cycle of

Gorgoderina attenuata

and the anuran hosts which are infected. (a) Line drawing of an adult

G. attenuata

from the urinary bladder of a northern leopard frog,

Rana pipiens

. (b) Truncated two host life cycles where the cercaria is ingested by a tadpole. This transmission strategy is used to infect newly metamorphosed leopard frogs and Woodhouse's toads. (c) Three host life cycle where the cercaria is ingested by an odonate second intermediate host. This transmission strategy is used to infect adult leopard frogs and adult bullfrogs. (d) Three host life cycle using a tadpole as a transport host. This transmission strategy is used to infect adult bullfrogs. Adapted from Bolek, Snyder & Janovy, Jr (2009a). Reproduced with permission of

Journal of Parasitology

, Allen Press Publishing Services.

Transmission of Toxoplasma gondii—From land to sea, a personal perspective

Figure 1 Sugar fecal float of cat feces showing unsporulated oocysts of

T. gondii

(arrows),

Cystoisospora

(

Isospora) felis

(f), and C.

rivolta

(r).

Toxoplasma gondii

oocysts are the smallest of all feline coccidia, averaging .

Cystoisospora felis

oocysts are pear-shaped and average .

Cystoisospora rivolta

oocysts are ovoid and measure about . All three coccidian oocysts are compared to the size of a

Toxocara cati

Giardia intestinalis biochemistry and regulation: An evolutionary tale

Figure 1

Giardia

glucose metabolism in trophozoites. 1. hexokinase; 2. glucose phosphate isomerase; 3. pyrophosphate-dependent phosphofructokinase; 4. fructose biphosphate aldolase; 5. glycolytic enzymes- (glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase, phosphoglycerate mutase, enolase); 6. pyruvate kinase; 7. Pyruvate; orthophosphate dikinase; 8. Phosphoenolpyruvate carboxyphosphotransferase (GTP dependent); 9. aspartate aminotransferase; 10. malate dehydrogenase; 11. malate dehydrogenase (decarboxylating); 12. Alanine aminotransferase; 13. pyruvate: ferredoxin oxidoreductase; 14. acetyl-CoA synthetase; 15. primary alcohol dehydrogenase (NAD); 16. hydrogenase. Abbreviations used; oxidized ferredoxin (Fdo), reduced ferredoxin (Fdr)

Figure 2 Arginine dihydrolase pathway in

Giardia

trophzoites. 1. arginine deiminase 2. ornithine transcarbamoylase 3. carbamate kinase.

Figure 3 Model polysaccharide chains constructed from disaccharide and linkage information randomly selected from appropriate conformational regions. All polysaccharides contain 30 monosaccharide residues. The polymer constructed from region Ia forms a right-handed (clockwise) helix, whereas the polymer built from region Ib has a left-handed helical conformation. The polysaccharide assembled from regions Ia and Ib (4:1) shows a random coil conformation. (Gerwig et al., 2002. The

Giardia intestinalis

filamentous cyst wall contains a novel β(1–3)-N-acetyl-D-galactosamine polymer: A structural and conformational study. Glycobiology

: 499–505. Reproduced with permission of Oxford University Press).

Figure 4 Giardan synthesis pathway. 1. glucosamine 6-P deaminase; 2. glucosamine 6-P N-acetylase; 3. phosphoacetylglucosamine mutase; 4. and UDP-N-acetylglucosamine pyrophosphorylase; 5. UDP-N-acetylglucosamine 4'-epimerase; 6. cyst wall synthase (β 1, 3 GalNAc transferase).

Figure 5 Mechanism(s) for the reduction and activation of metronidazole and other nitroimidazoles in

Giardia.

Metronidazole and nitroimidazoles (NO-R) are pro-drugs activated by cellular reduction. It is suspected that the nitro radical anion species R-NO

is responsible for toxicity. Three mechanisms of drug reduction are proposed; 1. Interaction of drug with reduced ferredoxin (Fdr) linked to pyruvate: ferredoxin oxidoreductase activity (PFOR), 2. The action of a nitroreductase (NR) and 3. Via an FADH

linked thioredoxin reductase (TrxR).

Figure 6 Graphic representation of alanine, ornithine and acetate concentrations from

Giardia

trophozoites metabolism as determined by GC-MS/MS analysis of growth medium after 8hr incubation. Each data point was compiled from a minimum of five independent replicates. Each spot represents one isolate and the two spots circled are results obtained from two metronidazole resistant isolates (determined by MIC). The data from these two are significantly different (

= 0.01). Alanine and acetate are products of glucose fermentation in

Giardia

and ornithine is produced via the arginine dihydrolase pathway. Values presented are in nmol h

−1

−6

cells.

The early history of immunoparasitology in the United States

Figure 1 (A) Emil von Behring, (B) Paul Ehrlich, (C) Ilya Mechnikov, (D) George Nuttall, and (E) Almroth Wright.

Figure 2 Robert Hegner (

Journal of Parasitology

:1 (1937). Reproduced with permission from

The Journal of Parasitology

, Allen Press Publishing Services.)

Figure 3 William Walter Cort (

Journal of Parasitology

:4 (1953). Reproduced with permission from

The Journal of Parasitology

, Allen Press Publishing Services.)

Figure 4 Norman R. Stoll (

Journal of Parasitology

:1 (1947). Reproduced with permission from

The Journal of Parasitology

, Allen Press Publishing Services.)

Figure 5 William H. Taliaferro (

Journal of Parasitology

20.3 (1934). Reproduced with permission from

The Journal of Parasitology

, Allen Press Publishing Services.)

Figure 6 Asa C. Chandler. (Courtesy of Woodson Research Center Fondren Library, Rice University. Reproduced with permission.)

Chemotherapy of helminth infections: A centennial reflection

Figure 1 Some anthelmintics used in the twentieth century for treatment of nematode infections.

Figure 2 Some anthelmintics used in the twentieth century for treatment of trematode and cestode infections.

List of Tables

A century (1914–2014) of studies on marine fish parasites published in The Journal of Parasitology

Table 1 Environmental variables, nutrients and pollutants selected by the boosted general additive model for the “full area” and “polygon area” models for

Oncomegas wageneri

(

O. wageneri

) and

Acanthocephaloides plagiusae

(

A. plagiusae

). The mboost algorithm uses bootstrap estimates to undertake a cross-validation to prevent overfitting. This cross-validation generates a variable selection process that provides the frequency (Fr (%)) at which each variable is selected during a bootstrap process. These frequencies are a proxy of the importance (expressed in percentage) of each variable within the model. Abbreviations were as follows: bbs = a penalized regression spline base learner, bspatial = a bivariate tensor product P-spline base learner, DD = decimal degrees, PAHH = polyaromatic hydrocarbons of high molecular weight, PAHL = polyaromatic hydrocarbons of low molecular weight, S = sediment, W = water. The principal coordinates of neighbour matrices (PCNM) variables were used to factor the contribution of unknown environmental variables acting at three different spatial scales (see Santana-Piñeros et al., 2012 for a detailed explanation)

Table 2 Performance statistics of the GAMmboost and MaxEnt models for

Oncomegas wageneri

(

O. wageneri

) and

Acanthocephaloides plagiusae

(

A. plagiusae

) for the “full area” (n = 162 sampling sites) and the “polygon area” (n = 134 sampling sites). Acronyms are as follows: Kappa = Cohen's Kappa, AUC = Area under the curve, pROC = Partial receiver operator curve. Kappa ranges from −1 (total disagreement) through 0 (random classification) to 1 (total agreement). For AUC and pROC curves, values below 0.5 indicate a performance no better than random, values between 0.7 and 0.8 are considered useful, and values >0.8 are excellent (Hosmer and Lemeshow, 2000)

Tick paralysis: Some host and tick perspectives

Table 1 Tick species reported to cause tick paralysis.

A Century of Parasitology

Discoveries, Ideas and Lessons Learned by Scientists Who Published in The Journal of Parasitology, 1914–2014

EDITED BY

John Janovy, Jr and Gerald W. Esch

Registered office: John Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK

Editorial offices: 9600 Garsington Road, Oxford, OX4 2DQ, UK

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111 River Street, Hoboken, NJ 07030-5774, USA

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A catalogue record for this book is available from the British Library.

Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books.

As co-Editors, we are honored to dedicate this book to the memory of our mentor, \hbox{Professor} J. Teague Self, a long-time member of the Department of Zoology, University of Oklahoma. We were privileged to secure our M.S. and Ph.D. degrees with the guidance of this man. Yes, he taught us a lot about parasitism and parasitology. But, one of our favorite memories was the real excitement of attending our annual ASP meetings because we knew Dr. Self would offer to introduce us to our heroes, e.g., people like Ray Cable, Norman Stoll, William Trager, Clark Read, Theodore von Brand, and so many others of their generation. It was always such a huge treat!

We also agree that his wisdom in dealing with people and his consistency as a professional were equally important to whatever success we have had over the past 50+ years. He was a true ``giant'' in our careers, and we thank him for helping us to focus in the right direction.

John Janovy, JrGerald W. Esch

List of contributors

M. Leopoldina Aguirre-Macedo

Laboratorio

de Parasitología, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional. México, U.S.A.

Omar M. Amin

Institute of Parasitic Diseases. Arizona, U.S.A.

Tavis K. Anderson

Virus and Prion Research Unit National Animal Disease Center, U.S.A.

Matthew G. Bolek

Department of Integrative Biology, Oklahoma State University, U.S.A.

Conor R. Caffrey

Center for Discovery and Innovation in Parasitic Diseases, Department of Pathology, University of California, San Francisco, U.S.A.

Janine N. Caira

Department of Ecology and Evolutionary Biology, University of Connecticut, U.S.A.

William C. Campbell

Research Institute for Scientists Emeriti, Drew University, U.S.A.

Richard E. Clopton

Department of Natural Science, Peru State College, U.S.A.

Charles D. Criscione

Department of Biology, Texas A&M University, U.S.A.

J. P. Dubey

United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, U.S.A.

Lance A. Durden

Department of Biology, Georgia Southern University, U.S.A.

Gerald W. Esch

Department of Biology, Wake Forest University, U.S.A.

Timothy G. Geary

Institute of Parasitology, McGill University, Canada.

Cameron P. Goater

Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, St. Lawrence Centre, Canada.

Kyle D. Gustafson

Department of Integrative Biology, Oklahoma State University, U.S.A.

John Janovy, Jr

School of Biological Sciences, University of Nebraska-Lincoln, U.S.A.

Edward L. Jarroll

Department of Biological Sciences, Lehman College, U.S.A.

Kirsten Jensen

Department of Ecology and Evolutionary Biology and the Biodiversity Institute, University of Kansas, U.S.A.

Raymond E. Kuhn

Department of Biology, Wake Forest University, U.S.A.

Ben J. Mans

Agricultural Research Council, South Africa Onderstepoort Veterinary Institute Pretoria, South Africa

David J. Marcogliese

Aquatic Biodiversity Section, Watershed Hydrology and Ecology Research Division, Water Science and Technology Directorate, Science and Technology Branch, St. Lawrence Centre, Canada.

Timothy A. Paget

Sunderland School of Pharmacy, University of Sunderland, Sunderland, U.K.

Judy Sakanari

University of California San Francisco,

California, U.S.A.

Heather A. Stigge

Department of Integrative Biology, Oklahoma State University, U.S.A.

Michael V.K. Sukhdeo

Department of Ecology, Evolution, and Natural Resources, and Center for Research on Animal Parasites, Rutgers University, U.S.A.

Edgar Torres-Irineo

Laboratorio de Parasitología, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional. México, U.S.A.

Victor Manuel Vidal-Martínez

Preface

The idea for this book, as well as for the reviews published in Volume 100 of The Journal of Parasitology (2014), originated with Gerald Esch, editor of the Journal for 20 years. Dr. Esch picked a group of potential authors and subjects, a list that expanded and contracted over a period of several months as we contacted individuals, answered their questions, and at times twisted their arms (gently). He envisioned a celebration of the long shelf life and intellectual breadth of this journal, along with the rich history of parasitology, especially as manifest by American parasitologists and their colleagues from around the world. An initial gathering of potential authors was held in 2013 in Quebec City, during the annual American Society of Parasitologists meeting. There was considerable discussion about the scope of such an edited volume, and during the next few months there were extensive communications between authors and editors on a variety of topics. Dr. Esch initiated discussions with Ward Cooper, Commissioning Editor at Wiley, and eventually those talks led to a draft contract for the project. That's when the real work started.

Both of us express our deepest appreciation to the parasitologists who contributed to this book and who put up with the requests involved. Everyone associated with this project has learned quite a bit about the history of parasitology, as well as the history of ideas, the manner in which technology has shaped research in our discipline, and how research experiences lead to life lessons. Thus after reading the initial contributions, we decided to ask authors for comments on lessons learned, not only from their own work, but from an examination of history. The 2014 ASP President's Symposium in New Orleans consisted of papers delivered by the authors, and their chapters are elaborations of those talks.

All of the contributed chapters except the last one by Timothy Geary, Judy Sakanari, and Conor Caffrey are preceded by what the authors believed to be the first paper published in The Journal of Parasitology (JP) in their particular subject areas. We were all impressed with the insight, and sometimes foresight, of these parasitologists, some whose work appeared in Volume 1. Because JP is such a visually rich publication, we also looked for some representative first figures, for example, the first drawing of a new species, or the first transmission electron micrograph, and have included a number of those figures along with their original legends and some commentary.

We would also like to thank Mike Sukhdeo and Vickie Hennings for help with material derived from The Journal of Parasitology, and in particular the chapter entitled “Antihelmintic drug discovery: Into the future,” by Timothy Geary, Judy Sakanari, and Conor Caffrey. After reading the initial draft of their manuscript, we both felt it would be an excellent review article in JP, so recommended that it be expedited through the publication process. We also felt that this final chapter was such a logical extension of the one by Bill Campbell that it didn't need a “first JP paper” beyond the one by Maurice Hall.

While reading through this volume, including the Table of Contents, you may find scientific names that are not italicized in some of the publication titles. In reprinting those original papers from JP, we kept the fonts, spelling, and nomenclature exactly as they were published in the journal when we listed those items in the Table of Contents.

The Wiley editor who took over this project from Ward Cooper is Kelvin Matthews. He has been a patient, communicative, and helpful editor and we greatly appreciate his work on this book.

Finally, we would like to thank Talia Everding, an undergraduate at the University of Nebraska-Lincoln, who served as an editorial assistant, reading all the chapters, often more than once, doing research in the back issues, and suggesting numerous ways to clarify the wording. We may have turned her into a parasitologist, in spirit if not in kind, with this assignment!

John Janovy, Jr and Gerald W. Esch

Chapter 1A century of parasitology: 1914–2014

John Janovy, Jr

School of Biological Sciences, University of Nebraska-Lincoln, U.S.A.

The hundred years between 28 June 1914, when the assassination of Austrian Archduke Franz Ferdinand precipitated World War I, and 27 July 2014, closing day of the American Society of Parasitologists' 89th annual meeting, represent one of the most stressful, complex, yet in some ways wondrous, periods of human history. Samantha Power (2002) called this time the “Age of Genocide;” Albert Einstein's equations completely re-structured our image of the universe; nuclear weapons entered our political negotiations; and, molecular biologists obliterated some of our most cherished views of nature. A decade after the Wright brothers' first sustained flight in a heavier-than-air craft, in December 1903, military airplanes took to the skies over Europe; today, some authors claim that airports are our current versions of the thirteenth-century cathedrals (Binney, 1999). Robert Goddard began his experiments with solid-fueled rockets in 1915 (Lehman, 1963); by 2014, intercontinental ballistic missiles were hiding in silos scattered across the Great Plains of North America, an International Space Station circled Earth, and the first Apollo moon landing was a mostly forgotten historical event. Even as we spent the past century obliterating much of Earth's terrestrial biological diversity by clearing tropical forests, satellite telescopes were discovering exo-planets at an increasing rate. In 1914, a successful scientist like H. B. Ward, founder of the American Society of Parasitologists as well as driving force behind a new scientific journal, The Journal of Parasitology, could buy a new Royal Model 10 typewriter; a century later we stop teaching cursive to elementary school students largely because kids are communicating via QWERTY keyboards (designed in 1873) on hand-helds with temperature-sensitive screens. Senior citizens today can recite, largely from personal experience, the origin and impact of what we now call the “Information Age.”

The new century in which we live should be an interesting one too, with projected climate change potentially wreaking havoc on coastal ecosystems and human populations expected to (phrased euphemistically) “level off.” Some things have not changed very much, however; parasitic organisms still infect not only humans and our domestic animals, but also, to our knowledge, virtually every eukaryotic species on planet Earth. Despite Ronald Ross' (1902) claim, in his Nobel Prize acceptance speech—“It is my privilege in this lecture to describe particularly the steps by which this great problem has at length received its full solution”—malaria remains one of humanity's most persistent scourges. Schistosomiasis, filariasis, and geohelminth infections still cause untold misery, along with their protistan counterparts such as leishmaniasis and amebiasis, especially in the tropics. But these infectious diseases also have inspired generations of parasitologists to apply their time, talents, and intellectual resources to find cures, or develop control methods, and thus provide relief from the economic and social burdens caused by parasitic organisms (Kuris, 2012; Loker, 2013).

In their quests to develop treatment and control technologies, parasitologists have indeed produced some major successes over the past century, but in the process they also have made conceptual contributions that might arguably be described as “metaparasitology”—an intellectual realm that includes the “rules” for pursuing the discipline. Although it may not always have been their intent, parasitologists have done research that in turn shapes our ideas about interactions between hosts and parasites. Excellent examples, among many, of concepts published very early if not originally in The Journal of Parasitology, include molecular mimicry in schistosomes (Damian, 1962, 1964, 1987), the relative immortality of cestodes (Read, 1967), and amphiparatenesis in Alaria marcianae as demonstrated by Shoop and Corkum (1987), who then extended the concept to those nematode species known to exhibit developmental arrest and transplacental transmission. With time, sometimes a surprisingly short time in historical terms, these kinds of contributions become principles of parasitism—the most common way of life among animals and animal-like eukaryotes.

Our goal in assembling this volume of contributed chapters is to bring the phenomenon of concept-driven research to the forefront, especially in the minds of younger readers. We also hope to provide historical perspective in the form of lessons learned from both successful and unsuccessful research endeavors. Thus, our contributing authors have been asked to step outside their immediate comfort zones, those places so often constructed and constrained by legitimate demands of proper methodology, statistical analysis, correct identification, and anonymous reviewers, and instead reflect on the historical development of their subjects. To quote from an early memo to our authors:

In most of the correspondence and discussion so far, we've mentioned the hope that these chapters would be heavy on ideas, and that authors would show us how research has inspired further work, how concepts demonstrated by particular papers have served a heuristic role in parasitology, and how historical precedents have been established. Our hope is that this volume will be unique in its role as a demonstration of how parasitologists think about their discipline and sub-disciplines, and how our material provides so many research opportunities yet can be quite uncooperative in sometimes unexpected ways. In the best of all worlds, students read this book, and come away with new ideas about their current research, an expanded view of how parasitologists pursue their careers, and a feeling that their own work, sometimes with obscure organisms that have little economic importance, has the potential to open up new areas of investigation. In other words, we understand that the subject is science, but we encourage all of you to think in terms of the history of science and what we have learned about how to do our science from having done it for years, if not decades.

Nobody needs reminded that mid-career scientists are fully occupied, and that statement certainly applies to the authors who have contributed to this volume. It is true, as Asa Chandler noted in his Presidential address during the 1945 American Society of Parasitologists meeting (Chandler, 1946), that parasitologists are “slow in going to seed,” so even our retired colleagues are busy with projects that consume their time and energies. Therefore, as must be the case for all such ambitious endeavors, this particular volume is not as inclusive as it might have been. But in our defense, after reading the initial chapter drafts, we editors came to the conclusion that it would require a whole shelf of such books to truly do the subject justice. We expect that some of you will take on this future task!

We also hope that this book sells enough copies to generate some net income. By written agreement between the editors and publisher, such “profits” have been assigned to the American Society of Parasitologists for support of The Journal of Parasitology, and especially to defray page charges for authors who have accepted papers, but are not in a position to pay costs for longer articles or essential color figures. The Journal of Parasitology is indeed an amazing publication with very long shelf life, rather like some of the authors who have published in it. If a student is able to read through a single issue, for example, and both understand and appreciate most of the work reported, that student will be broadly educated in a decidedly empowering manner. So our real dream, beyond some welcome support for authors who publish in the Journal, is that these chapters, which are mostly senior scientists' reflections on how our research has been shaped by ideas, will serve as conversation starters for younger scientists.

Literature cited

Binney, M. 1999.

Airport builders

. Academy Editions, Chichester, U.K., 223 p.

Chandler, A. C. 1946. The making of a parasitologist.

Journal of Parasitology

: 213–221.

Damian, R. T. 1962. A theory of immunoselection for eclipsed antigens of parasites and its implications for the problem of antigenic polymorphism in man.

Journal of Parasitology

: 16.

___________. 1964. Mimicry: Antigen sharing by parasite and host and its consequences.

American Naturalist

: 129–149.

___________. 1987. The exploitation of host immune response by parasites.

Journal of Parasitology

: 1–13.

Kuris, A. M. 2012. The global burden of human parasites: Who and where are they? How are they transmitted?

Journal of Parasitology

: 1056–1064.

Lehman, M. 1963.