Ecology and Environmental Management of Lyme Disease 9780813556031

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ECOLOGY AND ENVIRONMENTAL MANAGEMENT OF LYME DISEASE

ECOLOGY AND ENVIRONMENTAL MANAGEMENT OF LYME DISEASE EDITED BY Howard S. Ginsberg

RUTGERS UNIVERSITY PRESS, New Brunswick, New Jersey

Library of Congress Cataloging-in-Publication Data Ecology and environmental management of Lyme disease / edited by Howard S. Ginsberg, p. cm. Includes bibliographical references and index. ISBN 0-8135-1928-4 1. Lyme disease. 2. Lyme disease—Environmental aspects. I. Ginsberg, Howard S. [DNLM: 1. Borrella burgdorferi. 2. Ecology. 3. Lyme Disease— prevention & control. 4. Tick Control. WC 406 E19] RA644.L94E26 1993 614.5'7—dc20 DNLM/DLC for Library of Congress

Copyright © 1993 by Rutgers, The State All rights

92-24221 CIP

University

reserved

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in the United States of America

Contents Contributors Introduction

Howard S. Ginsberg

I Ecology and Epizootiology 1 Natural History of Borrelia burgdorferi in Vectors and Vertebrate Hosts John F. Anderson and Louis A. Magnarelli 2 Population Ecology of Ixodes dammini Durland Fish 3 The Dynamics of Spirochete Transmission Between Ticks and Vertebrates Thomas N. Mather^ II Distribution and Spread 4 Geographical Spread of Ixodes dammini and Borrelia burgdorferi Howard S. Ginsberg 5 The Origins and Course of the Present Outbreak of Lyme Disease Andrew Spielman, Sam R. Telford III, and Richard J. Pollack

vii 1

11 25 43

63

83

III Environmental Management 6 Lyme Disease Surveillance and Personal Protection Against Ticks Dennis J. White 7 Vector Management to Reduce the Risk of Lyme Disease Mark L. Wilson and Robert D. Deblinger

126

Forum: Perspectives on the Environmental Management of Ticks and Lyme Disease Joseph Piesman; George W. Korch, Jr.; Sam R. Telford III; Richard C. Falco and Thomas J. Daniels; Gary A. Mount; Daniel E. Sonenshine; Kirby C. Stafford III

157

Conclusion: Natural Population Regulation and Management of Ixodes dammini

183

Glossary Literature Cited Index

Howard S. Ginsberg

99

187 191 219 v

Contributors John F. Anderson The Connecticut Agricultural Experiment Station P.O. Box 1106 New Haven, Connecticut 06504

Howard S. Ginsberg Vector-Borne Disease Research Group Department of Plant Sciences/ Entomology National Park Service Coastal Research Center Woodward Hall University of Rhode Island Kingston, Rhode Island 02881

Thomas J. Daniels Medical Entomology Laboratory Department of Community and Preventive Medicine New York Medical College Valhalla, New York 10595

George W. Korch, Jr. U.S. Army Medical Research Institute of Infectious Diseases Fort Detrick Frederick, Maryland 21702

Robert D. Deblinger Massachusetts Division of Fisheries and Wildlife Field Headquarters Westboro, Massachusetts 01581

Louis A. Magnarelli The Connecticut Agricultural Experiment Station P.O. Box 1106 New Haven, Connecticut 06504

Richard C. Falco Bureau of Disease Control Westchester County Department of Health 19 Bradhurst Avenue Hawthorne, New York 10595

Thomas N. Mather Vector-Borne Disease Research Group Department of Plant Sciences/ Entomology Woodward Hall University of Rhode Island Kingston, Rhode Island 02881

Durland Fish Medical Entomology Laboratory Department of Community and Preventive Medicine New York Medical College Valhalla, New York 10595

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viii Gary A. Mount Medical and Veterinary Entomology Research Laboratory Gainesville, Florida 32604 Joseph Piesman Division of Vector-Borne Infectious Diseases Centers for Disease Control U.S. Department of Health and Human Services Fort Collins, Colorado 80522 Richard J. Pollack Department of Tropical Public Health Harvard School of Public Health 665 Huntington Avenue Boston, Massachusetts 02115 Daniel E. Sonenshine Department of Biological Sciences Old Dominion University Norfolk, Virginia 23529 Andrew Spielman Department of Tropical Public Health Harvard School of Public Health 665 Huntington Avenue Boston, Massachusetts 02115

CONTRIBUTORS

Kirby C. Stafford III Department of Entomology The Connecticut Agricultural Experiment Station P.O. Box 1106 New Haven, Connecticut 06504 Sam R. Telford III Department of Tropical Public Health Harvard School of Public Health 665 Huntington Avenue Boston, Massachusetts 02115 Dennis J. White New York State Department of Health Bureau of Communicable Disease Control 651 Corning Tower, Empire State Plaza Albany, New York 12237 Mark L. Wilson Yale University School of Medicine Department of Epidemiology and Public Health P.O. Box 3333 New Haven, Connecticut 06510

Introduction HOWARD S. GINSBERG Our perception of Lyme disease seems to be changing. After the initial tendency to ignore the problem, there followed a sort of public hysteria in endemic areas (and in some not-so-endemic areas). Now we are settling down to the sober task of trying to deal with this disease over the long term. Unfortunately, Lyme disease is the human manifestation of a complex natural phenomenon. The diversity of symptoms is matched by the complexity of the transmission cycle in nature. Yet we must understand this natural cycle if we are to manage Lyme disease effectively. It is not possible to understand the epidemiology of this disease without a thorough understanding of its epizootiology in natural communities. Therefore, a collaboration is required between medical scientists and field biologists. The purpose of this book is to summarize the progress to date in understanding the natural history and epizootiology of Lyme disease. It is my hope that synthesis of this information will provide a useful starting point for efforts to manage the ticks that transmit Lyme disease. To this end, I have two goals. The first is to provide a focus for future research on the ecology of Lyme disease. The disease was recognized and the pathogen and vector described relatively recently. In the past 15 years a great deal has been learned about these organisms, but the research has been mostly descriptive and somewhat haphazard, and it has lacked a coherent direction. The contributions in this volume, written by some of the most talented investigators in the field, summarize and synthesize this earlier work. I hope these syntheses will provide a perspective on our current state of knowledge that will point to the most useful directions for future research. I have asked the chapter authors to not shy away from speculation, to try to identify the crucial questions that have not yet been answered satisfactorily, and to offer suggestions on how to go about answering them. 1

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H . S . GINSBERG

The second goal is to provide a resource for people who must deal professionally with Lyme disease. Currently, no single source allows a physician or nurse, field scientist, pest-control operator, town planner, or public health officer to get in-depth information about tick biology, Lyme disease infection rates, or tick management techniques. This book is meant to fill that gap. The book is divided into three sections, the first on basic ecology and epizootiology, the second on distribution and spread, and the third on environmental management of Lyme disease. The first chapter, by John Anderson and Louis Magnarelli, is a comparative look at the biology of Borrelia burgdorferi and the epizootiology of Lyme disease in different parts of the world. Most ecological research on Lyme disease has dealt with Ixodes dammini as a Lyme vector in the northeastern United States, and overall this book reflects that bias. This chapter highlights the ecological differences between this species and other tick species that can act as vectors of Lyme disease; I. scapularis in the Southeast, I. pacificus on the West Coast, I. ricinus in Europe, and I. persulcatus in Europe and Asia. These ecological differences illuminate interesting and important differences in the epidemiology of Lyme disease in these areas. Additional implications of these ecological differences are examined in some of the subsequent chapters. Chapter 2, by Durland Fish, summarizes our knowledge of the population dynamics of I. dammini. Chapter 3, by Thomas Mather, covers the ecology of transmission of Lyme spirochetes between vectors and hosts in natural communities. The second section is devoted to the origin and geographical spread of the pathogen, main vector, and vertebrate hosts associated with Lyme disease in northeastern and north central North America. In Chapter 4,1 discuss the evidence concerning the geographic spread of Lyme disease and speculate on the mechanism of spread. Chapter 5, by Andrew Spielman, Sam Telford, and Richard Pollack, provides an overview of the origin and spread of Lyme disease from a slightly different perspective and comments on several controversial issues in Lyme disease ecology. The third section covers environmental management. Chapter 6, by Dennis White, concerns surveillance and personal protection against ticks. In Chapter 7, Mark Wilson and Robert Deblinger discuss control of I. dammini and Lyme disease. Following this is the Forum section, where differences of opinion on the various management options are aired. The introduction to this section is by Joseph Piesman, who considers management of the

INTRODUCTION

3

tick vectors of Lyme disease from the perspective of the Centers for Disease Control. The purpose of the forum is to provide opinions on various management techniques by people actually working with these techniques in the field. Some of these methods, especially deer management and the use of targeted pesticides, are somewhat controversial. Herein are authoritative commentaries that lay out the reasons for honest disagreement about the efficacy and desirability of the various techniques. My hope is that this forum will clear away much of the misinformation that has somehow gotten out to the public and will provide a basis for enlightened decision making by the people who must deal with Lyme disease in our towns, suburbs, and parks. To help readers who are not Lyme disease researchers, an overview of Lyme disease ecology precedes the main discussion, and a limited glossary follows it. I think the chapter authors have done an excellent job of synthesizing the currently existing information on Lyme disease, its ecology, transmission, and management. I hope this book will be useful to people working in a variety of fields and that it will also provide a sense of the fascination we all feel as we try to unravel this most complex natural system. As a naturalist, I find ticks, and for that matter spirochetes, to be every bit as interesting and awe inspiring as, say, wolves or eagles. The public, after all, seems to have a powerful fascination with parasites, both natural and human. Perhaps the initial revulsion that many feel toward ticks and spirochetes can give way to a fuller understanding of the interactions among these species and can lead to an appreciation of these organisms as regular elements of the broader natural world.

Overview of Lyme Disease Ecology This section is provided for readers who are not already familiar with the basics of Lyme disease ecology. The life cycle of the vectors of the disease and the transmission cycles in nature are reviewed. This information is organized in terms of region of the United States and the world, emphasizing the particular geographical areas affected and how the pattern of disease varies due to differences in vectors and hosts in each area. Lyme disease is caused by the spirochete Borrelia burgdorferi (Burgdorfer et al. 1982, Benach et al. 1983, Steere et al. 1983a, Johnson et al. 1984b) and is transmitted to humans by tick bites. The major vectors

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H . S . GINSBERG

are in the Ixodes ricinus group, with the northern deer tick, I. dammini, accounting for most cases in the northeastern and north central United States. In 1990, the states with the highest incidence of cases per capita were Connecticut, New York (especially Suffolk and Westchester counties), New Jersey, Rhode Island, Delaware, Wisconsin, Maryland, and Pennsylvania (CDC 1991b). Ixodes dammini is the major vector in all these states. In California the vector is 1. pacificus; in Europe, I. ricinus; and in Asia, 1. persulcatus (Anderson 1989a).

Transmission in the Northeastern and North Central United States Ixodes dammini has a two-year life cycle in most areas (Spielman et al. 1985). Eggs are laid in the spring, and the six-legged larvae eclose by midsummer (Yuval & Spielman 1990a). Transovarial transmission of spirochetes is inefficient, so typically less than 1% of the free-living larvae are infected with B. burgdorferi (Piesman et al. 1986a, Piesman 1989). The larvae take a blood meal and emerge the following spring as eight-legged nymphs, which are active from May through July in the Northeast. In typical endemic areas, one-fifth to one-third of the nymphs are infected with spirochetes (Falco & Fish 1988a, Piesman 1989). The nymphs take a blood meal and molt to the adult stage. Adult ticks are active from fall through spring, with sharply curtailed activity during cold weather. Typically, about half of the adults in endemic areas are infected (Anderson 1988). The nymphal stage is responsible for most human cases of Lyme disease because of the small size of the ticks (they are difficult to spot), clustered distribution, high spirochete prevalence, and phenology coinciding with the season of greatest human outdoor activity (Piesman & Spielman 1979, Hanrahan et al. 1984a, Spielman et al. 1985). Adults feed primarily on large and medium-sized mammals (Anderson 1988) and seek hosts in wooded habitats and thickets, especially along animal trails (Ginsberg & Ewing 1989a). Immatures attach to a tremendous variety of mammal and bird species, especially small mammals (Anderson 1988, 1989a), and dwell primarily in leaf litter and ground-level vegetation in the woods (Ginsberg & Ewing 1989a, Maupin et al. 1991, Siegel et al. 1991). Since larvae are rarely infected, while nymphs are responsible for most human cases, the ecology of the larval feeding period in mid- to late summer is the key to understanding the epidemiology of Lyme disease, because larval feeding

INTRODUCTION

5

patterns determine the prevalence of Lyme spirochetes in questing nymphs. The percentage of larvae that pick up the spirochete depends on several factors, including the proportion of hosts infected, the reservoir competence of each host species (efficiency of a host, after being infected with Lyme spirochetes, of transmitting the infection to previously uninfected attached ticks), and the proportion of larvae that feed on each host species (Ginsberg 1988, Mather et al. 1989b). The inverted phenology of life stages, with nymphs of one generation active earlier in the year than larvae of a different generation, results in a potentially explosive increase in the incidence of Lyme disease. The nymphs infect host animals, which transmit the infection to uninfected larvae later that same year. A few simple calculations demonstrate that with one-fifth to one-third of the nymphs infected, and numerous tick bites per host animal, nearly all the wild animals in an endemic area will be exposed to B. burgdorferi (Ginsberg 1992). Reservoir competence varies markedly among vertebrates, however. Some important hosts, such as white-tailed deer, are reservoir incompetent (Telford et al. 1988a, b); while other species, such as white-footed mice, are quite efficient as reservoirs (Levine et al. 1985, Donahue et al. 1987). Therefore, the proportion of nymphs infected depends to a large extent on the proportion of larvae that feed on host species that are competent reservoirs. At study sites in Massachusetts, Mather et al. (1989b) found that of three common host species (white-footed mice, Peromyscus leucopus; m e a d o w voles, Microtus pennsylvanicus,

and

chipmunks, Tamias striatus) the vast majority of infected nymphs had fed as larvae on P. leucopus. This species is apparently an important reservoir at many sites, but the roles of various host species as reservoirs remain to be evaluated in most areas. Another tick species that has been implicated as a vector of Lyme disease is the lone star tick, Amblyomma americanum (Schulze et al. 1984a). This is primarily a southern species, with dense populations from Texas to the Atlantic coast, north into Illinois, and east to southern New Jersey (Hair & Bowman 1986). In recent years, A. americanum has apparently expanded in range northward into coastal areas of New York and Rhode Island (Mather & Mather 1990, Ginsberg et al. 1991). Spirochete prevalence in A. americanum was about 3% in nymphs and 5% in adults in an endemic area in New Jersey (Schulze et al. 1986c). Amblyomma americanum rarely acquired spirochetes from infected hosts in the lab, however, and infection did not last through a

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H . S. GINSBERG

molt (Piesman 1988, Mather and Mather 1990). Therefore, the status of A. americanum as a vector of Lyme disease remains unclear.

Transmission in the Western and Southeastern United States The western black-legged tick, I. pacificus, is the primary vector of Lyme disease in western North America (Burgdorfer et al. 1985, Lane & Lavoie 1988). Larvae and nymphs overlap considerably in phenology, with most activity from March through June (Lane & Loye 1989). Adults are most common from November through May. This tick can be found on the West Coast of the United States and Canada, and inland in Nevada, Utah, and Idaho (Lane et al. 1991). Immatures attach to a wide variety of vertebrate species, including reptiles, birds, and mammals, while adults attach mostly to mediumsized and large mammals (Arthur & Snow 1968, Lane et al. 1991). Spirochetes can be passed transovarially in this species (Lane & Burgdorfer 1987), but infection rates in questing ticks are generally in the 1% to 2% range (Lane et al. 1991), far lower than in 1. dammini. One likely reason for the low spirochete prevalence is that large numbers of immatures attach to reptiles (especially to western fence lizards, Sceloporus occidentalis), which are presumed to be inefficient or incompetent reservoirs. A second reason is the overlap of phenologies of immatures with larvae slightly earlier in the season than nymphs (in I. dammini, nymphs are active earlier than larvae). These hypotheses are discussed in greater detail in subsequent chapters. The primary vector in the southeastern United States has not been well established. Ixodes scapularis, a close relative of I. dammini, is a competent vector of Lyme disease (Piesman & Sinsky 1988), but it has not been implicated as an important vector to humans. Spirochete prevalence in I. scapularis is quite low, probably because of frequent attachment of immatures to lizards. Interestingly, when offered mice, lizards, and chickens in laboratory trials, I. dammini, I. pacificus, and I. scapularis showed similar preferences (James & Oliver 1990). Therefore, the differences in host utilization in nature probably result largely from the relative scarcity of lizards in the northeastern United States. Amblyomma americanum is quite common in the southeast (Hair & Bowman 1986), but its status as a vector of Lyme disease has not been established.

INTRODUCTION

7

Transmission in Europe and Asia The major vector of Lyme disease in Europe is I. ricinus (Stanek et al. 1988); in Asia it is I. persulcatus (Ai et al. 1988). These species overlap in range in eastern Europe (Anderson 1989a). A substantial literature exists on I. ricinus, especially its life cycle and questing behavior (e.g., Lees 1948; Milne 1949, 1950; Gray 1981, 1982, 1984; see Chapter 2). However, these studies mostly concern tick populations in sheep pastures and other human-influenced habitats. The population biology of this tick in natural areas is currently a subject of considerable interest. Variable prevalence of B. burgdorferi and Lyme disease has been reported in different parts of Europe (Stanek et al. 1988), with focal areas of high prevalence (Aeschlimann et al. 1988, Neubert et al. 1988), much like the situation in North America.

Note Added in Proof A recent paper (Oliver, J. H., Jr., M. R. Owsley, H. J. Hutcheson, A. M. James, C. Chen, W. S. Irby, E. M. Dotson, and D. K. McLain. 1993. Conspecificity of the ticks Ixodes scapularis and I. dammini [Acari: Ixodidae], J. Med. Entomol. 30:54-63) presents evidence that Ixodes dammini and I. scapularis are, in fact, the same species. The name I. scapularis is older and has priority, so the species called I. dammini in this book is now known as I. scapularis. This name change could be overturned in the future, but it stands at present. Therefore, readers should be aware that the name I. scapularis now applies to the species that is called both 1. dammini and I. scapularis in this book and in the scientific literature.

Parti

Ecology and Epizootiology

Chapter 1

Natural History of Borrelia burgdorferi in Vectors and Vertebrate Hosts JOHN F. ANDERSON and LOUIS A. MAGNARELLI Lyme disease (Steere et al. 1977a) and related illnesses such as acrodermatitis chronicum atrophicans and lymphadenosis benigna cutis are caused by the spirochete Borrelia burgdorferi (Burgdorfer et al. 1982, Johnson et al. 1984b). This bacterium is transmitted from animals to humans by the bite of a tick. Within the past decade, this spirochete has been found over vast areas in the Northern Hemisphere where ticks abound. The natural history of B. burgdorferi in its tick vectors and animal hosts is the subject of this chapter.

The Spirochete Borreliae are helical cells that measure 0.2 to 0.5 by 3 to 20u with 3 to 10 loose coils (Kelly 1984) (Fig. 1.1). The genus Borrelia is composed of 21 species (Table 1.1), the majority of which are associated with relapsing fever illnesses that are transmitted by soft-bodied ticks (Argasidae) (Johnson et al. 1984a, 1987; Kelly 1984). In contrast to all the other species of tick-associated borreliae except B. thieleri (Kelly 1984), B. burgdorferi is transmitted by hard-bodied ticks (Ixodidae) such as Ixodes dammini, I. ricinus, I. pacificus, I. persulcatus, and I. scapularis (Steere & Malawista 1979; Burgdorfer et al. 1982, 1983, 1985; Burgdorfer & Gage 1986; Ai et al. 1988). This spirochete tends to remain in the midgut of unfed ticks, where it is sequestered in the microvillar brushborder and intercellular spaces of the epithelium (Burgdorfer 1989). Borrelia burgdorferi was initially isolated from I. dammini collected on Shelter Island, New York (Burgdorfer et al. 1982). The strain, designated B31, was shown to have prominent outer-surface proteins with molecular masses of about 31,000 and 34,000 daltons (Barbour et al. 11

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FIGURE 1.1. Unfixed, negatively stained micrograph of Borrelia burgdorferi. Photo by Theodore G. Andreadis.

1985). Isolates with major proteins with similar molecular masses were subsequently isolated from I. pacificus, wild animals, and humans in the United States (Anderson et al. 1983, Benach et al. 1983, Bosler et al. 1983, Steere et al. 1983a, Burgdorfer et al. 1985); from I. ricinus, wild animals, and humans in Europe (Burgdorfer et al. 1982, Asbrink et al. 1984, Hovmark et al. 1988); and from I. persulcatus and humans in Asia (Ai et al. 1988). Variants with different major outer surface proteins from the seminal strain B31 have frequently been isolated from humans and I. ricinus in Europe (Barbour et al. 1985; Stanek et al. 1985; Wilske et al. 1985,1986,1988; Anderson et al. 1986a), but in the United States the isolates from humans, rodents, and most ticks have been remarkably similar to one another and the B31 strain (Barbour et al. 1985). Exceptions have included isolates from a veery songbird (Catharusfuscescens), cottontail rabbits (Sylvilagus floridanus), I. dentatus, I. dammini, I. neotomae, and I. pacificus (Barbour et al. 1985; Bisset & Hill 1987; Ander-

NATURAL HISTORY OF THE BORSELIA

BURGDORFERI

13

TABLE 1.1. Species of Borrelia, Their Vectors, and Their Associated Disease Species

Vector

Disease

B. anserina

Argas species

Avian borreliosis

B. brasiliensis

Ornithodoros

brasiliensis

B. caucasica

Ornithodoros

verrucosus

Tick-borne relapsing fever

erraticus

Tick-borne relapsing fe"er

B. crocidurae

Ornithodoros

B. dugesii

Ornithodoros dugesi

B. duttonii

Ornithodoros moubata

Tick-borne relapsing fever

B. graingeri

Ornithodoros

Tick-borne relapsing fever

B. harveyi

Unknown

B. hermsii

Ornithodoros hermsi

Tick-borne relapsing fever

B. hispanica

Ornithodoros

erraticus

Tick-borne relapsing fever

B. latyschewii

Ornithodoros

tartakovskyi

Tick-borne relapsing fever

B. mazzottii

Ornithodoros talaje

Tick-borne relapsing fever

B. parkeri

Ornithodoros parkeri

Tick-borne relapsing fever

B. persica

Ornithodoros

Tick-borne relapsing fever

B. recurrentis

Pediculus humanus

Louse-borne relapsing fever

B. theileri

Rhipicephalus species Boophilus microplus

Cattle and horse borreliosis

B. tillae

Ornithodoros zumpti

B. turicatae

Ornithodoros

graingeri

tholozani

turicatae

Tick-borne relapsing fever

B. venezuelensis

Ornithodoros rudis

Tick-borne relapsing fever

B. burgdorferi

Ixodes species

Lyme borreliosis

B. coriaceae

Ornithodoros coriaceus

Bovine abortion

SOURCES: Data taken from Johnson et al. 1984b, 1987; Kelly 1984.

son et al. 1988, 1989; Lane & Pascocello 1989). While major proteins vary considerably among European borreliae isolated from humans, specific illnesses linked to particular variants have not been documented. The variants isolated from ticks and rabbits in the United States have not yet been isolated from humans and therefore are not known to cause human disease.

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J. F. ANDERSON AND L . A . MAGNARELLI

Tick Vectors At least five species of morphologically similar ticks that feed relatively frequently on humans are competent vectors of B. burgdorferi. North American species include I. dammini, I. pacificus, and I. scapularis. Old World species are identified as I. ricinus and I. persulcatus. All have similar life histories and feed on a wide variety of host animals. The three species in North America tend to occur in different geographical areas. Ixodes pacificus extends along the West Coast of the United States from the California-Mexico border northward into southwestern Canada (Bishopp & Trembley 1945, Cooley & Kohls 1945, Gregson 1956, Arthur & Snow 1968, Easton et al. 1977, Keirans & Clifford 1978, Furman & Loomis 1984, Anderson et al. 1989, Burgdorfer 1989). A disjunct inland population exists in Nevada and Utah. Ixodes scapularis, found in the southeastern United States, extends from Florida westward to central Texas and northward into southern Indiana and northern Virginia (Bishopp & Trembley 1945, Cooley & Kohls 1945, Keirans & Clifford 1978, Anderson 1989a, Burgdorfer 1989). Ixodes dammini extends northward from Virginia into New Hampshire, Vermont, and Maine and westward through southern Ontario to its westernmost border in Minnesota and Iowa, including southern Illinois (Spielman et al. 1979, 1985; Coan & Stiller 1986; Anderson et al. 1987c, 1990a; Ginsberg & Ewing 1988; Wilson et al. 1988a; Anderson 1989a; Burgdorfer 1989; Pinger & Glancy 1989; Smith et al. 1990; Bouseman et al. 1990; Levine et al. 1991). One or both Eurasian species occur from the British Isles eastward to the islands of Japan. Ixodes ricinus extends from England to about 50° to 55° east longitude (Arthur 1966, Snow & Arthur 1970, Doss et al. 1978, Anderson 1989a, Burgdorfer 1989). It has been collected in North Africa and as far north as 65° north latitude. Ixodes persulcatus overlaps with I. ricinus in eastern Europe and is found in a relatively broad band across Asia (Arthur 1966, Doss et al. 1978, Anderson 1989a, Burgdorfer 1989). Each tick feeds three times in its life, initially as a larva, then as a nymph, and finally as an adult. The duration of the life cycle is a year or more. Ixodes scapularis and I. pacificus may take one to two years to complete their lives (Rogers 1953, Arthur & Snow 1968, Furman & Loomis 1984). Ixodes dammini usually completes its life cycle in two years (Spielman et al. 1985). Ixodes ricinus and I. persulcatus often complete their life cycles in two years, though in the far northern regions

NATURAL H I S T O R Y OF THE BORRELIA

BURGDORFERI

15

of their range, ticks may live five or six years (Arthur 1966, Balashov 1972). The seasonal distribution of the four life stages of I. dammini is as follows (Spielman et al. 1985): larvae hatch from eggs predominately in midsummer (July and early August), and after feeding fully from a host they detach and drop to the ground. Larvae either molt into nymphs or remain in an engorged state in the duff layer of the soil throughout the winter (Yuval & Spielman 1990a). Blood-fed larvae molt into nymphs the following spring. Host-seeking nymphs become abundant in late spring and early summer (late May, June, and early July). After ingesting blood from animals, they fall to the ground and molt into adults. Males and females seek large animals, such as dogs and deer, in mid October through mid November primarily, and on warm days during winter and again in early spring of the following year. Seasonal abundance of the three feeding stages of the other species differs from I. dammini. For example, larvae, nymphs, and adults of I. pacificus may be collected throughout the year in California. Adults are most abundant during fall and winter; subadult stages are abundant in spring and early summer, with peak activity of nymphs occurring in May and preceding peak larval feeding by several weeks (Arthur & Snow 1968, Furman & Loomis 1984, Westrom et al. 1985, Lane & Loye 1989). All five species feed on a wide variety of host animals, including reptiles, birds, and mammals. Numbers of host species parasitized by specific tick species total at least 80 for I. dammini and I. pacificus, 53 for I. scapularis, 241 for I. persulcatus, and 317 for I. ricinus (Anderson 1991). Larval and nymphal ticks feed on a much larger variety of hosts than do adult ticks (Anderson 1988, 1989a; Burgdorfer 1989). Immature ticks feed on small, medium-sized, and large mammals; birds; and, with the exception of I. dammini, also reptiles. Laboratory studies have revealed that even I. dammini will feed on reptiles (James & Oliver 1990), but it has little opportunity to do so, as lizards, the most typical reptile to act as host, are uncommon in its geographical range. Adult ticks tend to feed on large mammals and to a lesser extent on medium-sized mammals (Balashov 1972, Piesman et al. 1979, Anderson et al. 1987c). Certain host species are parasitized more heavily than are others (Spielman et al. 1979, 1985; Carey et al. 1980; Main et al. 1982; Anderson 1988; Telford et al. 1988a; Fish & Dowler 1989; Fish & Daniels

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J . F. A N D E R S O N AND L . A . MAGNARELLI

1990). Rodents, particularly the white-footed mouse, are primary hosts for larvae and nymphs of I. dammini, though these immature ticks feed on larger mammals as well. Reptiles are preferred hosts for larvae and nymphs of I. pacificus and possibly I. scapularis (Rogers 1953, Arthur & Snow 1968, Furman & Loomis 1984, Lane & Loye 1989, Lane & Stubbs 1990), though mammals also are parasitized by both species. Apodemus appears to be a primary host for at least larval I. ricinus (Matuschka et al. 1990). Ground-inhabiting birds also are parasitized, particularly by I. dammini and I. ricinus (Anderson 1988, 1989a, 1991). Larvae and nymphs feed on nesting birds and juvenile birds that have recently learned to fly, as well as on birds migrating northward in the spring and southward in the fall (Anderson & Magnarelli 1984; Mehl et al. 1984; Anderson et al. 1986b, 1990b; Schulze et al. 1986b; Battaly et al. 1987; Anderson 1988; Weisbrod & Johnson 1989). Birds are a natural means of dispersing ticks over short and long distances and can distribute ticks intercontinentally (Hoogstraal et al. 1963). Adult ticks are more discriminatory in their feeding habits than are subadult forms. Adults do not feed on birds and tend not to attach to rodents or other small animals, although larger rodents such as woodchucks (Marmota monax) and gray squirrels (Sciurus carolinensis) are occasionally parasitized (Anderson 1988). They feed primarily on deer, carnivores, cattle, and hogs (Balashov 1972; Piesman et al. 1979; Anderson & Magnarelli 1980; Main et al. 1981; Spielman et al. 1981, 1984, 1985; Wilson et al. 1985, 1988b, 1990b; Lane & Burgdorfer 1986). Ixodes ricinus and I. persulcatus also attach to lagomorphs (Balashov 1972).

Animal Reservoirs of the Spirochete Borrelia burgdorferi was initially isolated from wild mammals in 1982, when it was cultured from the blood of white-footed mice (Peromyscus leucopus) and a raccoon (Procyon lotor) (Anderson et al. 1983, Bosler et al. 1983). Since the tick vectors parasitize such a large number of host animals (Anderson 1991), it is not surprising to now have a relatively long list of species that have been recorded to have active or past exposure to this bacterium. Animals become infected cutaneously via the bite of an infected tick and sometimes show subsequent multisystemic infection. Spirochetemia in hamsters is transitory, lasting for about 6 days after in-

NATURAL H I S T O R Y OF THE BORRELIA

BURGDORFERI

17

traperitoneal inoculation (Johnson et al. 1984a). Spirochetes invade tissues, such as those of the spleen and kidney, within 14 days postinfection and persist, probably for the life of the animal (Johnson et al. 1984a). Skin tissues also contain B. burgdorferi (Nakayama & Spielman 1989), and it is for this reason in part that white-footed mice remain reservoir competent. Burgdorfer and Gage (1986) reported spirochetemias in rabbits, with alternating high and low levels of spirochetes that affected the percentage of feeding ticks that became infected. Further study is needed on this "relapse phenomenon" and its effect on prevalence of infected ticks. Borrelia burgdorferi has been isolated from or detected in tissues of 17 wild and 3 domestic mammals and 8 birds in the United States (Table 1.2). In Europe, B. burgdorferi has been recorded from 3 rodents (Table 1.2). One rodent reservoir has been identified in Asia (Table 1.2). The white-footed mouse is a particularly important host for the spirochete in the northeastern and midwestern United States (Anderson et al. 1983,1985,1986c, 1987b; Bosler et al. 1983,1984; Levine et al. 1985; Bosler & Schulze 1986; Donahue et al. 1987; Callister et al. 1989). These mice apparently harbor the spirochete throughout their lives (Bosler & Schulze 1986, Donahue et al. 1987), and where Lyme disease is prevalent, 70% to 80% or more of the mice in areas may be infected. Prevalence of infection is highest in summer, following peak feeding by nymphs, and lowest in winter, when immature ticks are inactive (Anderson et al. 1987a). Other species of rodents, such as eastern chipmunks, may also be important reservoirs, but these animals have not been extensively studied (Anderson et al. 1985, Mather et al. 1989b). Apodemus may be an important reservoir in Europe and Asia (Hovmark et al. 1988, Miyamoto et al. 1991). Borrelia burgdorferi strains, cultured from rodents in the eastern and midwestern United States, are indistinguishable from the Shelter Island strain (B31) and other isolates from humans (Anderson et al. 1985, Barbour et al. 1985). Clearly, rodents are a major source of infection for spirochetes that are transmitted to humans. Cottontail rabbits, however, have antigenically different forms of B. burgdorferi (Anderson et al. 1989). These variants and those isolated from ticks feeding on rabbits in the United States have not yet been associated with human disease, but it is important to emphasize that there is variation among isolates of B. burgdorferi in Europe as well. Ixodes ricinus is the primary vector there and is known to feed more extensively on lagomorphs (Oryctolagus cuniculus) (Milne 1949) than 1. dammini feeds on rabbits in the United States (Spielman et al. 1979,

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