Bionomics and ecology of Ornithodoros (P.) turicata americanus (Marx) (Ixodoidea: Argasidae) and other commensal inverte...

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Title:
Bionomics and ecology of Ornithodoros (P.) turicata americanus (Marx) (Ixodoidea: Argasidae) and other commensal invertebrates present in the burrows of the gopher tortoise, Gopherus polyphemus Daudin
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Gopherus polyphemus
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xiii, 278 leaves : ill. ; 28 cm.
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English
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Milstrey, Eric Gordon, 1957-
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Ornithodoros   ( lcsh )
Ticks -- Ecology -- Florida   ( lcsh )
Gopher tortoise   ( lcsh )
Entomology and Nematology thesis Ph. D
Dissertations, Academic -- Entomology and Nematology -- UF
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bibliography   ( marcgt )
non-fiction   ( marcgt )

Notes

Thesis:
Thesis (Ph. D.)--University of Florida, 1987.
Bibliography:
Bibliography: leaves 244-277.
Statement of Responsibility:
by Eric Gordon Milstrey.
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Typescript.
General Note:
Vita.

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University of Florida
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BIONOMICS AND ECOLOGY OF Ornithodoros (P.) turicata
americanus (MARX) (IXODOIDEA: ARGASIDAE)
AND OTHER COMMENSAL INVERTEBRATES PRESENT IN THE
BURROWS OF THE GOPHER TORTOISE, Gopherus polyphemus DAUDIN













BY

ERIC GORDON MILSTREY






















A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE
UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE
REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA

1987


















To Susan, my wife,
and my son, Tristan.












ACKNOWLEDGEMENTS


I want to express my sincerest thanks to Dr. J.F.

Butler for his help, guidance and thoughtful discussion on

my work. I thank him and the USDA for the grant that

funded this research.

Thanks go to Diana Simon, Debbie Boyd, Rick Wilkerson,

Sam Telford, Andy Beck, Ben Beard and the rest of the

wonderful people with whom I have worked with for the past

six years. You have made my stay enjoyable and

professionally profitable.

I am grateful to Mr. Irving Roberts and Mr. G.W.

Schlitzkus of Owens-Illinois for allowing this research to

be done on their lands.

Special thanks go to Ms. Joan Diemer of the Florida

Game and Freshwater Fish Commission, Wildlife Research Unit

in Gainesville. Her insight, good humor and instruction on

the gopher tortoise and its habits proved to be invaluable.

There are very few researchers who are as cooperative.

There were a large number of individual experts that

were consulted during the course of this study, too many to

mention here, and all should be individually acknowledged

but four stand out as being most helpful: Dr. Dale Habeck

for his interest and expertise with rearing immature

insects, Dr. R. Woodruff for his discussions on beetles,












and their interactions and for his paper on the

invertebrates of the gopher burrow, Mr. D. Franz who served

as my major consultant on the vertebrates present in gopher

tortoise burrows and Dr. S.C. Zam for his assistance on the

immunological aspects of this work.

My most profound and deepest thanks go to my wife

Susan for her support through this endeavor. She kept my

morale high and was my primary motivator. I acknowledge

her commitment to my degree as was demonstrated, by her

raising our son, helping me and working full-time so that

we were financially secure. Her typing and editorial

skills were greatly appreciated during manuscript

preparations.












TABLE OF CONTENTS



Page

ACKNOWLEDGEMENTS . iii

LIST OF TABLES ... .. vii

LIST OF FIGURES . .. xi

ABSTRACT . .xii

CHAPTERS

I INTRODUCTION .. ... 1

II ARGASID NICHE SPECIALIZATION IN RELATION
TO SYSTEMATICS AND PATHOGEN TRANSMISSION 11

Historical Perspective: Ticks as Disease Agents 11
Classification of the Ixodoidea .. .13
Morphology ... .... 13
Developmental and Behavioral Characteristics 14
Systematics of Argasidae .. .16
Genus: Argas . 26
Genus: Ornithodoros .. 29
Small Genera: Otobius, Antricola, and
Nothaspis ............... 34
Life Cycles: Laboratory and Field ....... 35
Argas .. ... ... 35
Ornithodoros .... 37
Antricola and Nothaspis ... .42
Ecological Niches Utilized by the Argasidae 42
Troglodytic Niches 42
Niticolous Habitats ... .43
Free Living Hosts 44
Pathogens Associated with Argasid Ticks 44
Burrow Habitats ... .46
Caves and Shelters ... .57
Sheds and Houses ... .58
Shallow Caves and Overhangs ... .63
Deep Caves ... 64
Nests ... 67
Marine nests ............. 67
Ground or cliff nests ......... 71
Arboreal nests .. .75
Free Living Hosts ... .81













Interactions of Argasid Ticks with the
Wider Environment .. .84

III MATERIALS AND METHODS .. .88

Sites . ... 88
Burrows . .. 89
Sampling Technique .............. 90
Sorting . .. 91
Fluorescent Marking .. .93
Temperature and Humidity Measurments ... .94
Age and Sex Structure of Tick Populations 94
Blood Meal Identification .. .94
Invertebrate Identification .. .97
Calculations and Statistics .. .99

IV RESULTS AND DISCUSSION .. 100

Animals Present at the Site .. .100
Blood Meal Identification .. 109
Host Preference .. .124
Host Suitability for Population Growth 131
Seasonality in Feeding and Population Growth 158
Mortality . .. .166
Migration . .. .169
Survivorship .. .178
Population Age Structure. .. .181
Trends in Population Growth .. .184
Population Estimation .. .188
Fisher-Ford estimate .. .188
Removal estimate .. .189
Biological Observations on Other Associated
Invertebrates .. .198
Burrow Commensals .. .198
Invertebrate parasites .. .217
Invertebrate predators .. .227
Dung decomposers .. .231
General decomposers .. .233

V CONCLUSION . .. .238


REFERENCES . ... .244

BIOGRAPHICAL SKETCH . .. .278












LIST OF TABLES


Table Page

2-1. A species list of the family Argasidae and the
hosts they parasitize. 17

4-1. Vertebrates that are known to utilize the
burrows constructed by gopher tortoises at the
two sites. ... 101

4-2. Summary of results of the blood meal analyses
on field collect Ornithodoros t. americanus at
the Lochloosa flatwoods site. .... 110

4-3. Summary of results of the blood meal analyses
on field collect Ornithodoros t. americanus at
the Robert's ranch sandhill site .. 111

4-4. Student's t-test comparisons of percentages of
the Ornithodoros t. americanus populations fed
in burrows in which either tortoise, frog or
tortoise and frog served as host. .. 129

4-5. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus larvae in which one
sample did not have any fed ticks present. 133

4-6. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus first nymphs in which
one sample did not have any fed ticks present. 134

4-7. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus second nymphs in which
one sample did not have any fed ticks present. 135

4-8. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus third nymphs in which
one sample did not have any fed ticks present. 136

4-9. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus late nymphs in which
one sample did not have any fed ticks present. 137












4-10. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus adults in which one
sample did not have any fed ticks present. 139

4-11. Student's t-test comparisons of differences
between larval and first nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which one sample did not have any
fed ticks. ... 142

4-12. Student's t-test comparisons of differences
between first and second nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which one sample did not have any
fed ticks. . ... 143

4-13. Student's t-test comparisons of differences
between second and third nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which one sample did not have any
fed ticks. ... 144

4-14. Student's t-test comparisons of differences
between third and late nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which one sample did not have any
fed ticks. . ... 145

4-15. Student's t-test comparisons of differences
between late nymphal and adult numbers in
sequential population samples of Ornithodoros t.
americanus in which one sample did not have any
fed ticks. . ... 146

4-16. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus larvae in which both
samples had fed ticks. ... 147

4-17. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus first nymphs in which
both samples 'ad fed ticks. ... 148

4-18. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus second nymphs in which
both samples had fed ticks. ... 149


viii












4-19. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus third nymphs in which
both samples had fed ticks. ... 150

4-20. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t.americanus late nymphs in which
both samples had fed ticks. ... 151

4-21. Student's t-test comparisons of differences
between sequential population samples of
Ornithodoros t. americanus adults in which both
samples had fed ticks. .... 152

4-22. Student's t-test comparisons of differences
between larval and first nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which both samples had fed ticks. .153

4-23. Student's t-test comparisons of differences
between first and second nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which both samples had fed ticks. .154

4-24. Student's t-test comparisons of differences
between second and third nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which both samples had fed ticks. .155

4-25. Student's t-test comparisons of differences
between third and late nymphal numbers in
sequential population samples of Ornithodoros t.
americanus in which both samples had fed ticks. .156

4-26. Student's t-test comparisons of differences
between late nymphal and adult numbers in
sequential population samples of Ornithodoros t.
americanus in which both samples had fed ticks. .157

4-27. Seasonal feeding behavior of Ornithodoros t.
americanus on hosts that inhabited gopher
tortoise burrows at the Lochloosa site during
1984 and 1985. ... 159

4-28. Seasonal feeding behavior of Ornithodoros t.
americanus on hosts that inhabited gopher
tortoise burrows at the Robert's ranch site
during 1984 and 1985. ... 160












4-29. Variation in the number of Ornithodoros t.
americanus collected from gopher tortoise
burrows in which a percentage had fed on an
identifiable host. .. .167

4-30. Longevity of Ornithodoros t. americanus under
field conditions (observation period: 472-494
days). . ... ... .179

4-31. Removal sampling population estimates of
Ornithodoros t. americanus in gopher tortoise
burrows sampled at the Robert's ranch sandhill
site. . .191

4-32. Removal sampling population estimates of
Ornithodoros t. americanus in gopher tortoise
burrows sampled at the Lochloosa flatwoods
site. . .193

4-33. Population variation in removal estimates of
Ornithodoros t. americanus in gopher tortoise
burrows at the Robert's ranch sandhill site
and at the Lochloosa flatwoods site between
collection periods. .194

4-34. Invertebrates collected in gopher tortoise
burrows at the Robert's ranch sandhill site and
at the Lochloosa flatwoods site. Month of
collection and its association with the burrow
are also included. .. .199

4-35. Annual changes in the number of invertebrate
species present in gopher tortoise burrows and
the percentage soil water at the Robert's ranch
sandhill location ... .218

4-36. Annual changes in the number of invertebrate
species present in gopher tortoise burrows and
the percentage soil water at the Lochloosa
flatwoods site ... .219












LIST OF FIGURES


Figure Page

4-1. Blood meal analyses of fed Ornithodoros t.
americanus at the Lochloosa pine flatwoods
site. Percentages that each host contributed
to the total number of meals analyzed for each
stage . 113

4-2. Blood meal analyses of fed Ornithodoros t.
americanus at the Robert's ranch sandhill
site. Percentages that each host contributed
to the total number of meals analyzed for each
stage .... 115

4-3. Seasonal feeding behavior of Ornithodoros t.
americanus on hosts that inhabited gopher
tortoise burrows, expressed as percentages of
total burrows that had feeding occurring during
the 1984-1985 sampling periods at the Lochloosa
pine flatwoods site ... 162

4-4. Seasonal feeding behavior of Ornithodoros t.
americanus on hosts that inhabited gopher
tortoise burrows, expressed as percentages of
total burrows that had feeding occurring during
the 1984-1985 sampling periods at the Robert's
ranch sandhill site .... 164

4-5. Age structure of the field population of
Ornithodoros t. americanus in the sandhill
habitat . 183

4-6. Age structure of the field population of
Ornithodoros t. americanus in the pine flatwood
habitat ... .. .183

4-7. Mean estimated population size per gopher
tortoise burrow for Ornithodoros t. americanus
during the 1984-1985 sampling period at both
the Lochloosa flatwoods and the Robert's ranch
sandhill sites. (Correction factors applied to
removal sampling estimates (Carle and Maughan,
1980).) . 197

4-8. Cross sectional diagram of a typical gopher
tortoise burrow with the locations where some
commensal invertebrates are found .. .221














Abstract of Dissertation Presented to the Graduate
School of the University of Florida in Partial Fulfillment
of the Requirements for the Degree of Doctor of Philosophy


BIONOMICS AND ECOLOGY OF Ornithodoros (P.) turicata
americanus (MARX) (IXODOIDEA: ARGASIDAET)
AND OTHER COMMENSAL INVERTEBRATES PRESENT IN THE
BURROWS OF THE GOPHER TORTOISE, Gopherus polyphemus DAUDIN

By

ERIC GORDON MILSTREY

MAY 1987

Chairman: Jerry F. Butler
Major Department: Entomology and Nematology


The principal hosts of Ornithodoros (P.) turicata

americanus (Marx) are the gopher tortoise, Gopherus

polyphemus Daudin and the gopher frog, Rana areolata

aesopus Baird and Girard. Other hosts that were identified

or strongly implicated are the Southern toad, Bufo

terrestis (Bonnaterra), the Florida mouse, Peromyscus

(Podomys) floridanus Chapman, the opossum, Didelphis

virginiana (Kerr) and various snake species. Multiple host

feedings between molts were demonstrated in all life

stages. Implications for improved disease transmission and

reproductive potential were discussed. Although the

tortoise was the most common parasitized, the frog was the

preferred host. Both species could maintain the ticks but

the frog sustained greater population growth rates.












Population growth was maximized when both species

concurrently served as tick hosts.

Larvae were the predominant age class collected

(45.2%), the several stages of nymphs constituted 43.8% of

the total with adults making up the remaining 11.0%. The

male to female sex ratio was 2.3 to 1. Tick populations,

calculated by removal sampling estimation, could be as high

as 3300 but were more commonly below 200. Calculations

using time survived in the field by individuals provides

evidence that the life cycle of O. t. americanus could

approach six years.

The major mortality factors for the soft tick species

were desiccation due to low soil water content in the

burrow or starvation due to the inability to locate a

suitable host. The major mode of dispersion was concluded

to be phoresy on the vertebrate hosts, but active dispersal

could not be discounted.

Significant additions to the number of invertebrate

species known to utilize the tortoise burrow were made. A

number of new undescribed species were recovered. Year

round biological observations provided new information on

many of the commensals.












CHAPTER I
INTRODUCTION



The tick Ornithodoros (Pavlovskyella) turicata

americanus (Marx) is found in peninsular Florida in the

burrows of the gopher tortoise, Gopherus polyphemus

(Daudin) and in some burrows occupied by burrowing owls,

Athene cunicularia (Molina). The species, Ornithodoros

turicata (Duges) is known from Mexico through the

southwestern states of the United States to Kansas, with an

allopatric population in Florida. Beck et al. (1986)

resurrected americanus, the species' name given by Marx

(1895) to this Florida tick population as a subspecific

designation because of its distinctively different biology

and ecology as compared to published records of the western

strain. The taxonomic position of this Florida population

is still uncertain because larval morphological characters

can be used to distinguish the two strains (Milstrey,

unpublished data) but biochemical tests, such as the gel

electrophoresis technique used to separate Ornithodoros

(P.) erraticus Lucas and O. (P.) sonrai Sautet and

Witkowski (Wallis and Miller, 1983), have not yet been

done. Research is in progress on cross breeding the

subspecies (Telford, unpublished data). Further research

in these areas may stabilize the taxonomic position of the

species.











Since 1979 the Florida population of this soft tick or

argasid has been extensively studied by Dr. J. F. Butler

and his colleagues. A number of life history and behavioral

studies have already been done (Beck et al., 1986,

Wilkinson, unpublished data, Telford, unpublished data).

The temperature preference of the subspecies was studied by

Kilbourne (1981). The only field ecology done on the tick

was undertaken by Adeyeye (1982). His studies concentrated

on the interactions between the tick in the burrow and the

outside environment. He found that ticks could be readily

attracted out of the burrows to either a CO2 source or an

animal placed upon the burrow apron. He estimated tick

populations to be between 47 and 1,338 in the burrows

studied. Location within the burrow varied during the year

with higher densities at the entrances in the summer and

fall; the tick retreating deeper into the burrow in winter

and spring.

The reason for the renewed interest in the study of

this tick was due to a combination of two factors. The

first was the introduction of African swine fever (ASF or

ASFV) to the Caribbean and the possibility that this

disease could invade the United States. The second was that

native Ornithodoros ticks could transmit this agent

(Groocock et al., 1980) and that, as in Spain, once












established in the native argasid tick population the virus

might become endemic.

Florida is the gateway to the Caribbean for the United

States. Gibbs and Butler (1984) summarized the risk

factors for Florida being the "port of call" for ASF's

entry into North America. Florida is the major stop off

point for tourists going to, and illegal immigrants coming

from, the islands of the Caribbean. Thousands of tons of

cargo, both legal and illegal, worth millions of dollars,

arrive on Florida's shores annually. Florida has a large

population of both feral and domestic susceptible swine.

Lastly, there are several Ornithodoros species present that

could pick up the pathogen.

African swine fever is an arbovirus which has emerged

as the single most important transmissible swine pathogen

in the world. There are a number of important factors about

this virus and the disease it causes that support this

statement. A partial list of these factors include, the

lack of a vaccine and no expectation for the imminent

development of one, the virulence of the infection, carrier

states in surviving swine, the ease of transmission,

identification of the disease requiring multiple laboratory

procedures utilizing immunofluorescent and cell culture

techniques; and the existence of tolerant wild hosts and












Ornithodorus tick vectors (Hess, 1981; Wardley et

al.,1983).

African swine fever virus is a member of the

Iridovirus family. This family is characterized by having

double stranded DNA with complex capsids formed in the

cytoplasm (Andrewes et al., 1978). Most of these viruses

infect invertebrates; some are found in lizards, fish and

frogs but ASF is the only DNA virus classified as an

arbovirus (Andrewes et al. 1978).

Montgomery, in 1910, first identified the disease in

infected domestic pigs in Kenya (Montgomery, 1921). In

those reported cases mortality rates were over 98%. For 40

years, cases were seen only in sub-Saharan Africa; then, in

1957 and 1960, cases were seen in Spain and Portugal

(Wardley et al., 1983; Wilkinson, 1981). African swine

fever became endemic on the Iberian peninsula and, since

then, the virus has become a worldwide problem, spreading

temporarily into Europe, the Mediterranean, South America

and some Caribbean Islands (Gibbs 1981). Because of the

lack of any other effective control strategy, the present

method of disease control for this virus is total

eradication of all diseased or exposed swine.

African swine fever in Africa is also a sylvatic disease.

There are three normal hosts for the virus: the warthog,

Phacochoerus aethiopicus Pallas; bush pig, Potomocherus











porcus (L.); and the giant forest hog, Hylocherus

meinertzhageni Thomas. The virus appears to be transmitted

normally by the bite of the soft tick that lives in the

burrow, Ornithodoros (Ornithodoros) porcinus porcinus

Walton. Other haematophagous arthropods present were not

implicated in transmission (Plowright, 1975). In the

warthog the infection is inapparent (Thomson et al., 1980).

Plowright found that in the tick Ornithodoros (0.) p.

porcinus, the ingested virus replicates in the midgut of

the tick and then invades the haemocoel and other tissues,

including the reproductive organs. Once established in the

tick it may be transmitted transtadially, venereally and

transovarially (Plowright et al., 1970, 1974; Plowright,

1975, 1977). Thomson (1985) stated that Ornithodoros

ticks remain attached to warthogs outside the burrow but

may fall off later near pig sties, and that these ticks and

not wild swine exposure are the source of virus in primary

outbreaks of ASF in southern and East Africa.

One of the factors that contributed to the virus

becoming endemic in the Iberian peninsula was that it

became established in the local Ornithodoros (P.) marocanus

Velu (0. erraticus "large race") population through feeding

on infected swine (Sanchez Botija, 1963). Four species,

not involved with natural transmission cycles, have been

shown to be able to pick up and transmit the virus under











laboratory conditions: Ornithodoros (0.) coriaceus Koch

(Groocock et al., 1980), O.(P.) turicata americanus and

O.(A.) puertoricensis Fox (Butler et al., 1984a), and

0.(0.) savignyi (Audouin) (Mellor and Wilkinson, 1985).

Several biological-facts about Ornithodoros ticks

confound the potential for ASF disease control. First, is

that they are very long lived, probably at least 10 years

in favorable sites (Pavlovskii and Skrynnik, 1960). They

are often inactive for years at a time and maintain

themselves in locations that are inaccessible to normal

methods of pesticide application such as burrows, under

rocks or bushes and in cliff or cave niches. They do not

stay on the host for long, thus minimizing pesticide

exposure. Some species have larvae that attach to the host

for about a week, providing a method for effective

dispersion. Many Ornithodoros ticks have a diverse host

range feeding on whatever is available--amphibian, reptile,

bird or mammal, rarely dependent upon a single host. Thus,

if the local tick species becomes infected with the ASF

virus, we will be unable to eradicate it from the habitat

or protect the stock by direct pesticide application

(Hoogstraal, 1956), and it may be several years before it

is evident that the ticks are infected because of

aestivation or delay in an infected tick coming into

contact with a pig.












Recently, several methods have been developed that can

be used to identify infections in Ornithodoros ticks.

Geering et al. (1986) developed the immunodot blot test for

detecting ASFV antigens in the hemolymph of Ornithodoros

coriaceus. It has promising field applications for

detecting ASFV and other tick-borne pathogens. Besides the

immunodot blot test, Endris et al. (1986) also used the

hemolymph test for direct immunofluorescence and virus

culture in buffy coat cells to confirm the presence of ASFV

in the tick. The notable advantages of the hemolymph test

are that it can be used on individual ticks, that it does

not kill the ticks and so they can therefore be used for

further study.

Although ASF is an arbovirus, vector transmission is

not the primary method of swine transmission outside

Africa. Internationally, it appears that the major mode of

transmission is from the ingestion of uncooked or cured

pork products (Gibbs and Butler, 1984). Within a herd, the

virus spreads swiftly by contact (Scott, 1965) or air

(Wilkinson, 1981). It can also be transmitted by germ

plasm (Gibbs, 1981) or mechanically from contaminated farms

or veterinary tools. In the endemic areas of Spain and

Africa, domestic and wild swine encounters must be guarded

against. The ease of transmission is the primary

difficulty encountered when attempting to control the











disease. Since the virus is relatively resistant and can

survive on contaminated surfaces for at least 60 days

(Endris and Hess, personal communication), personnel,

equipment and vehicles moving between farms can readily

transfer the virus between herds (Wardley et al., 1983).

The original African swine fever isolates of

Montgomery (1921) were highly virulent. The high virulence

of the African isolates has not been maintained with the

disease's expansion outside Africa (Hess, 1981). These

lower virulent strains have complicated the control of the

disease for three reasons: (1) the development of higher

numbers of inapparent swine carriers, (2) the less distinct

symptoms that characterize the disease and (3) the

development of nonhemadsorptive virus strains. Pigs may

survive initial infection with little or no symptomology

from these lower virulent strains but these chronic

carriers can infect the whole herd before the disease is

recognized (DeTray, 1957).

Disease recognition and confirmation is a difficult

problem. African swine fever has the same symptoms as hog

cholera and other hemorrhagic diseases (Wardley et al.,

1983). Only in those herds that have had hog cholera

vaccination and still come down with the symptoms is ASF

likely to be suspected. Confirmation of the disease must

be done in a laboratory using a combination of












immunofluorescent and cell culture techniques, but 1% still

remain undetectable (Hess, 1981). Therefore, negative

results do not always confirm the herd is disease free.

In order to protect Florida and the rest of the United

States, this study was undertaken to better understand the

argasid ticks that could serve as potential vectors before

the introduction of ASF. The objectives of my study on

O.(P.) t. americanus were to (1) identify the natural hosts

of the tick, (2) identify the principal factors controlling

the population dynamics in the burrow systems of the host

gopher tortoise, and (3) to collect other invertebrate

species which cohabit the burrow system and expand the

information known about these species. Throughout the

range of the gopher tortoise, tortoise populations are

being threatened. Some states now consider them endangered

and so the burrow's endemic fauna is threatened.

Collection of these endemic invertebrates, therefore,

provides (1) recognition of unknown species before they

become extinct, (2) a data base to gauge the impact of

decreased tortoise populations, and (3) an annual

perspective of invertebrate populations since the three

previous studies were short term (Hubbard, 1894, 1896;

Young and Goff, 1939; Woodruff, 1982). Since this burrow

habitat has been present since the early Pleistocene period

(Auffenburg, 1969), an investigation of the fauna could










10

provide an unparalleled view of the past evolutionary

history and stability of the commensal invertebrate

community.











CHAPTER II
ARGASID NICHE SPECIALIZATION IN RELATION TO SYSTEMATICS
AND PATHOGEN TRANSMISSION



Historical Perspective: Ticks as Disease Agents

In order to evaluate the epidemiology of potential New

World soft tick vectors of ASFV and other diseases, the

interactions of known soft tick vectors, the diseases they

transmit and their ecological habitats are reviewed. This

review provides a worldwide perspective of both

Ornithodoros and Argas tick problems. This broad view is

required since modern transportation methods and ecological

manipulation have enhanced the possibility that regional

disease/vector problems can become international ones

(Gibbs, 1981; Hoogstraal, 1985). Hard tick (Ixodidae)

diseases and their transmission were not included with the

exception of those diseases that have also been

demonstrated in soft ticks.

The family Argasidae was largely ignored during the

early years of tick research, other than the taxonomic work

by Nuttall and Warburton (1908). In the 1930s, relapsing

fevers were recognized as important soft tick transmitted

diseases. Interest in the diseases was so strong that in

1941 an American Association for the Advancement of Science

(AAAS) symposium was held on the subject because relapsing

fever was "spreading in the United States, particularly in











the southern and western parts and is widely

prevalent in Latin America" (Moulton, 1942, P4). The study

of this disease by Drs. G. E. Davis and E. Brumpt provided

significant increases in the knowledge of the biology of

the burrow and house inhabiting Ornithodoros vectors, as

well as providing the research momentum to greatly increase

the number of collected soft tick species. This served as

the initiation point for the extensive study of argasid

taxonomy by Cooley and Kohls in 1944. Since this time many

more species have been described and the genera and

subgenera have stabilized.

In the last 25 years, with the widening interest and

improvements in the isolation and identification of

arthropod transmitted viruses (arboviruses), interest in

the Argasidae as disease vectors has renewed. In the same

period, the "ecology movement", increased the awareness of

wildlife and their diseases. These two factors undoubtedly

provided the research interest necessary for the increased

number of examinations of zoonoses involving wild animals

and their parasites, including argasids. These studies

increased the number of viruses and tick species known.












Classificiation of the Ixodoidea

Morphology

An important part of any study comparing the host and

habitat specificity of an arthropod is the ability to

identify the arthropod in question. Not only must an

arthropod species be identifiable, but separable from other

similar species. Additionally, the taxonomic study of

those other related species provides (1) a point of

reference for the study of those other related species, (2)

a view of the evolutionary variety in the group and the

phylogeny of the species and (3) host and habitat

specificity of the group. Comparison of the phylogeny,

physiology and specificity of the related species may

provide data in aiding inference on the ecology and

possibly the evolutionary history of the species under

study.

Ticks are classified in the order Metastigmata or

Parasitiformes depending on the systematist consulted

(Kranz, 1978). The superfamily Ixodoidea Banks contains

all three tick families: Argasidae, Ixodidae and

Nuttalliellidae. Argasidae are leathery with no scutum,

and the fourth palpal segment is apical. In the other two

families a scutum is present on all stages. In the

Nuttalliellidae the scutum and integumental texture is

similar and the fourth palpal digit is apical. The












Ixodidae, or hard ticks, have a scutum which is strongly

sclerotized and distinct from the integument, and the

fourth palpal digit is reduced and arises from a

subterminal ventral pit on the third segment (Hoogstraal,

1973a).



Developmental and Behavioral Characteristics

Argasids have specialized in feeding for short periods

of time on hosts that intermittently visit the site where

the ticks are present. These ticks are normally found in

arid locations or in areas where there are long dry

seasons. In areas with heavy rainfall they are restricted

to caves, treeholes or dry crevices, rarely burrows

(Hoogstraal, 1973a). The short host exposure time, limited

habitats, long survival time away from the host and strong

thigmotropic response of these ticks have contributed to

their being so poorly known.

The biologically more diverse family Ixodidae is much

better known due to its parasitic behavior. It is active

on the soil and vegetation questing for hosts, where it

feeds for long periods and on which it mates. The family

also has many species that parasitize man's livestock and

other animals he utilizes.

Besides the behavioral differences between argasids

and ixodids there are some important physiological











differences. Ixodids have only one nymphal stage whereas

argasids have two to eight (Hoogstraal, 1973a). In the

Argasidae some species have non-feeding stages, either as

larvae or first nymphal stage. Argasids mate off the host.

In the ixodids, females lay one large egg batch, numbering

up to 20,000, and then die. Argasid females lay many egg

batches before they die, usually with a blood meal

preceding each. Argasid egg batches are much smaller,

numbering in the hundreds.

The family Nuttalliellidae is represented by one

African species: Nuttalliella namaqua Bedford. It is known

only from 21 specimens collected from host animal skins,

from under rocks and in swallow nests (Keirans et al.,

1976; Hoogstraal, 1985). Hoogstraal (1985) stated that the

major host is probably the rock hyrax.

Besides Bedford's (1931) description and the

redescription of Keirans et al. (1976) using scanning

electron microscropy, two other investigations have been

done. Roshdy et al. (1983) studied spiracle structure and

El Shoura et al. (1984) studied female internal morphology.

They found certain characters similar to either argasids or

ixodids and some unique structures. The internal and

external distinctiveness of Nuttalliella led El Shoura et

al. (1984) to conclude that it represents a

phylogenetically distinct branch derived from the prototype












Ixodoidea base and is not the missing link between argasids

and ixodids.



Systematics of Argasidae

The family Argasidae is split into five genera: Argas,

Ornithodoros, Otobius, Antricola and Nothoaspis. Each

genus also is in its own subfamily but, except for Argas,

the rest of the genera are thought to be derived from

Ornithidorine stock (Hoogstraal, 1985). However most

authors consider the last four genera to be in the

subfamily Ornithodorinae. A list of the species present in

the family and their hosts is presented in Table 2-1. The

list is presented in alphabetic order within each group or

subgenus as the phylogenetic relationships for most of the

species are unclear. This classification is not the only

one--the Russian, Pospelova-Shtrom in 1946 and 1969

proposed another scheme. Notable points in it are the

generic resurrection of Carios (Argas subgenus), Alveonasus

(Ornithodoros subgenus) and Alectrobius (Ornithodoros

subgenus) and the development of three tribes. In the

tribe Otobiini, Otobius and Alveonasus are separated from

the other Ornithidorinae based primarily upon the

similarities in feeding and development of some of the

species present in both genera. Although both systems have

their strengths and weaknesses (Pospelova-Shtrom, 1969),









Table 2-1. A species list of the family Argasidae and the hosts they parasitize.a


Family Argasidae Canestrini 1890

Subfamily Argasidinae

Genus Argas Latreille 1796

Subgenus Argas Latreille 1796

"reflexus group"
africolumbae Hoogstraal, Kaiser, Walker,
Ledger and Converse 1975
beijingensis Teng 1983
brevipes Banks 1905
dalei Clifford, Keirans, Hoogstraal and Corwin 1976
hermanni Audouin 1827
himalayensis Hoogstraal and Kaiser 1972
latus Filippova 1961
macrostigmatus Filippova 1961
polonicus Siuda, Hoogstraal, Clifford and Wassef 1964
reflexus (Fabricius 1794)
tridentatus Filippova 1961
vulgarus Filippova 1961
(A.) sp. Egypt origin (Clifford et al. 1983 *)

japonicuss group"
assimilis Teng and Song 1983
cooleyi Kohls and Hoogstraal 1960
sp. near cooleyi Hoogstraal 1985*
falco Kaiser and Hoogstraal 1973
japonicus Yamaguti, Clifford and Tipton 1968
lagenoplastis Froggatt 1906
lowryae Kaiser and Hoogstraal 1975


pigeon

pigeon
owl, falcon, wren, woodpecker
burrowing owl
pigeon
snow partridge
pigeon, swallow
cormorant
pigeon
pigeon
sparrow, pigeon
pigeon, sparrow, owl, crow, falcon



swallow
swallow
gull
falcon
swallow
fairy martin
falcon









Table 2-1. (cont.)


monachuss group"
dulus Keirans, Hoogstraal and Capriles 1971
monachus Keirans, Radovski and Clifford 1973

"neghmei group"
neghmei Kohls and Hoogstraal 1961
moreli Keirans, Hoogstraal and Clifford 1978

"cucumerinus group"
cucumerinus Neumann 1901
magnus Neumann 1896

Subgenus Persicargas Kaiser, Hoogstraal and Kohls 1964

"persicargas group"
persicus (Oken 1818)
steptopelia Hoogstraal, Kaiser and Kohls 1968

"arboreus group"
arboreus Kaiser, Hoogstraal and Kohls 1964
miniatus Koch 1844
nullarborensis Hoogstraal and Kaiser 1973
robertsi Hoogstraal, Kaiser and Kohls 1968
sanchezi Duges 1891
walkerse Kaiser and Hoogstraal 1969
(P.) sp. Madagascar origin (Hoogstraal et al. 1983 *)

giganteuss group"
giganteus Kohls and Clifford 1968

"beklemischevi group"
abdussalami Hoogstraal and McCarthy 1965
beklemischevi Pospelova-Shtrom, Vasilyeva and Semashko 1961
radiatus Railliet 1893
ricei Hoogstraal, Kaiser, Clifford and Keirans 1975
theilerae Hoogstraal and Kaiser 1970


palm chat
monk parakeet


pigeon, chicken, man
chicken, wild birds, man


vulture, pelican
pigeon, chicken


chicken, arboreal nesting birds
dove


heron
chicken, small birds
crow
heron, stork, cormorant
chicken, dove, quail, turkey
chicken



ground nesting birds


vulture
vulture
vulture, turkey, chicken
vulture
vulture









Table 2-1. (cont.)

zumpti Hoogstraal, Kaiser and Kohls 1968

"ungrouped Persicargas species"
(P.) sp. South African origin (Hoogstraal 1985 *)

Subgenus Microargas Hoogstraal and Kohls 1966

transversus Banks 1902

Subgenus Carios Latreille 1966

australiensis Kohls and Hoogstraal 1974
daviesi Kaiser and Hoogstraal 1973
dewae Kaiser and Hoogstraal 1974
macrodermae Hoogstraal, Moorhouse, Wolf and Wassef 1977
pusillus Kohls 1950
sinensis Jeu and Zhu 1982
vespertilionis (Latreille 1802)

Subgenus Chiropterargas Hoogstraal 1955

boueti Roubaud and Colas-Belcour 1933
confusus Hoogstraal 1955
cordiformis Hoogstraal and Kohls 1967
ceylonensis Hoogstraal and Kaiser 1968

Subgenus Secretargas Hoogstraal 1957

echinops Hoogstraal, Uilenberg and Blanc 1967
hoogstraali Morel and Vassiliades 1965
transgariepinus (White 1846)

Subgenus Ogadenus Pospelova-Shtrom 1946

brumpti Neumann 1907


vulture






Galapagos tortoise



insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats



insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats



hedgehog
lizards
insectivorous bats


rock hyrax, lizards, birds









Table 2-1. (cont.)

Ungrouped Argas species

brueschi Dryenski 1957
sp. Afganistan origin (Hoogstraal et al., 1979 *)


Subfamily Ornithodorinae

Genus Ornithodoros Koch 1844

Subgenus Ornithodoros Koch 1844

apertus Walton 1962
compacts Walton 1962
eremicus Cooley and Kohls 1941
indica Rau and Rao 1971
moubata (Murray 1877)
porcinus Walton 1962
procaviae Theodor and Costa 1960
savignyi (Audouin 1827)

Subgenus Pavlovskyella Pospelova-Shtrom 1950

alactagalis Issaakjan 1936
arenicolous Hoogstraal 1953
asperus Warburton 1918 (= verrucosus)
braziliensis Aragao 1923
cholodkovski Pavlovsky 1930
erraticus (Lucas 1849)
foleyi Parrot 1928 (=francheri)
furcosus Neumann 1908
graingeri Heish and Guggisberg 1953
grenieri Klein 1964
gurneyi Warburton 1926
hermsi Wheeler, Herms and Meyer 1935
macmillani Hoogstraal and Kohls 1966


Citellus sp.
lizards


porcupine, warthog
tortoises
deer mice
barking deer
warthog, porcupine, man
warthog, porcupine, man
rock hyrax
camel, man


rat, hamster, badger, lizards
rodents, hedgehog, lizards
rodents, hedgehog, lizards
goat, tortoise, lizards, snake
mammals, man, birds
bats
hedgehog, rodents, lizards, toad
domestic livestock, man
porcupine, bat, man
rodent (Hypogeomys)
kangeroo
chipmunk, mice, bat, bird, squirrel
cockatoo, owl









Table 2-1. (cont.)

marocanus Velu 1919
nereensis Pavlovsky 1941
nicollei Mooser 1932
normandi Larrousse 1923
parkeri Cooley 1936
rostratus Aragao 1911
sonrai Sautet and Witkowski 1944
sparnus Kohls and Clifford 1963
tartakovski Olenev 1931
tholozani Laboulbene and Megnin 1882
turicata (Duges 1876)

verrucosus Olenev, Zasukhin and Fenyuk 1934
zumpti Heisch and Guggisberg 1953

Subgenus Ornamentum Clifford, Kohls and Sonenshine 1964

coriaceus Koch 1844

Subgenus Alectrobius Pocock 1907

"bat feeding group"
azteci Matheson 1935
base (Schulze 1935)
boliviensis Kohls and Clifford 1964
brodyi Matheson 1935
clarki Jones and Clifford 1972
dusbabeki Cerny 1967
dyeri Cooley and Kohls 1940
eptesicus Kohls, Clifford and Jones 1969
hasei Schulze 1940 (= dunni)
jul Schulze 1940
kelleyi Cooley and Kohls 1940
knoxjonesi Jones and Clifford 1972
mimon Kohls, Clifford and Jones 1969
peropteryx Kohls, Clifford and Jones 1969


swine, rodents, rabbit
burrowing mammals
Neotoma, dog, squirrel, man
rodents
prairie dogs, Citellus, burrowing owls
burrowing rodents, dog, man, peccary
Mastomys, grass rat (Arsicanthis)
Peromyscus, Neotoma
rodents, carnivores, tortoise
man, sheep, hedgehog, rodent
tortoise, snake, burrowing owls, pig,
Citellus, Neotoma, man
burrowing rodents
rat, mouse


deer, cattle, man




insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats








Table 2-1. (cont.)


peruvianus Kohls, Clifford and Jones 1969
rossi Kohls, Sonenshine and Clifford 1965
setosus Kohls, Clifford and Jones 1969
stageri Cooley and Kohls 1941
tadaridae Cerny and Dusbabek 1967
tiptoni Jones and Clifford 1972
yumatensis Cooley and Kohls 1940

capensiss group bird parasites"
amblus Chamberlin 1920
capensis Newmann 1901
collocaliae Hoogatraal, Kadarsan, Kaiser and VanPeenen 1974
coniceps Canistrini 1890
denmarki Kohls, Sonenshine and Clifford 1965
sp. near denmarki California origin (Clifford, 1979 *)
maritimus Vermeil and Marguet 1967
muesebecki Hoogstraal 1969
sawaii Kitaoka and Suzuki 1973
spheniscus Hoogstraal, Wassef, Hays and Keirans 1985
yunkeri Keirans, Clifford and Hoogstraal 1984

"Galapagos iguana group"
darwini Kohls, Clifford and Hoogstraal 1980
galapagensis Kohls, Clifford and Hoogstraal 1980

"miscellaneous host group"
casebeeri Jones and Clifford 1972
chironectes Jones and Clifford 1972
concanensis Cooley and Kohls 1941
cyclurae de la Cruz 1984
echimys Kohls, Clifford and Jones 1969
marmosae Jones and Clifford 1972
puertoricensis Fox 1947
talaje (Guerin-Meneville 1849)
tuttlei Jones and Clifford 1972


insectivorous
insectivorous
insectivorous
insectivorous
insectivorous
insectivorous
insectivorous


cormorant, pelican, booby, tern
penguin, gull, tern
cave swiftlets
pigeon
tern, gull, booby
various marine birds
gull, tern
booby
shearwaters
penguin
tern, booby, albatross, penguin


iguana
iguana


rodent (Othtylomys)
marsupial (Chironectes), cotton rat
bat, swallow, raptor
iguana
rodent (Echimys), marsupial (Marmosa)
marsupial (Marmosa)
rat, rabbit
Neotoma, man, dog, cat, chicken
tapir, Agouti









Table 2-1. (cont.)

Subgenus Proknekalia Keirans, Hoogstraal and Clifford 1977

peringueyi Bedford and Hewitt 1925
peusi (Schulze 1943)
vansomerini Keirans, Hoogstraal and Clifford 1977

Subgenus Subparmatus Clifford Kohls and Sonenshine 1964

marinkellei Kohls, Clifford and Jones 1969
mormoops Kohls, Clifford and Jones 1969
viguerasi Cooley and Kohls 1941

Subgenus Alevonasus Schulze 1944

acinus Whittick 1938
canestrinii (Birula 1895)
delanoei Roubaud and Colas-Belcour 1931
eboris Theiler 1959
foleyi Parrot 1928
lahorensis Newmann 1908

Subgenus Reticulinasus Schulze 1941

batuensis Hirst 1929
chiropterphila Dhanda and Rajagopalan 1971
faini Hoogstraal 1960
madagascariensis Hoogstraal 1962
rennellensis Clifford and Sonenshine 1962
salahi Hoogstraal 1953
solomonis Dumbleton 1958
steini (Schulze 1935)
sp. New Guinea origin (Hoogstraal, 1985 *)
sp. New Guinea origin (Hoogstraal, 1985 *)
sp. Thailand origin (Hoogstraal, 1985 *)


swallow
swallow
swallow


insectivorous bats
insectivorous bats
insectivorous bats


large mammals
sheep, cattle
hedgehog
porcupine
sheep, antelope, gerbil, man
domestic livestock, mouflon


fruit
fruit
fruit
fruit
fruit
fruit
fruit
fruit
fruit
fruit
fruit









Table 2-1. (cont.)

Ungrouped Ornithodoros species

aragasi Fonseca 1960
cooleyi Mclvor 1941
davisi Fonseca 1960
elongatus Kohls, Clifford and Sonenshine 1965
natalinus Cerny and Dusbabek 1967
nattereri Warburton 1927
rudis Karsch 1880 (=venezuelensis)


Genus Otobius Banks 1912

lagophilus Cooley and Kohls 1940
megnini (Duges 1884)


Genus Antricola Cooley and Kohls 1942

Subgenus Antricola Cooley and Kohls 1942

cernyi de la Cruz 1978
coprophilus McIntosh 1935
habenensis de la Cruz 1976
martelorum de la Cruz 1978
mexicanus Hoffman 1959
naomiae de la Cruz 1978
occidentalis de la Cruz 1978
silvai Cerny 1967


Oryzomys "rat"
carnivores
Oryzomys "rat"
iguana
insectivorous bats
host unknown
man, rodents, chicken




rabbit, hare
deer, antelope, cattle


insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats
insectivorous bats









Table 2-1. (cont.)

Subgenus Parantricola Cerny 1966

marginatus (Banks 1910)


Genus Nothoaspis Keirans and Clifford 1975

reddelli Keirans and Clifford 1975


insectivorous bats




insectivorous bats


a : Compiled from de la Cruz, 1978a; Hoogstraal, 1985; Hoogatraal et al., 1979b; Jones and
Clifford, 1972; Kohls et al., 1965 and Sonenshine et al., 1966.

* : The reference in which the existence of the undescribed species is mentioned.











the American system used in this paper is utilized by most

of the world's acarologists.



Genus: Argas

The genus Argas has 56 species recognized at this

time. They are grouped into seven subgenera and numerous

subgroups (Hoogstraal et al., 1979b). Definitions of the

subgenera are found in several publications: A.(Argas),

(Hoogstraal, 1957); A.(Persicargas), (Kaiser et al., 1964);

A.(Ogadenus), (Pospelova-Shtrom, 1946); A.(Chiropterargas),

(Hoogstraal, 1955); A.(Carios), (Hoogstraal, 1958);

A.(Secretargas), (Hoogstraal, 1957); and A.(Microargas),

(Hoogstraal and Kohls, 1966b). Other references that

should be consulted for systematic separation are

Sonenshine et al. (1962) for larval characters and four

papers on differences in the structure of the Haller's

organ in the genus Argas; Clifford et al. (1983),

Hoogstraal et al. (1983), Hoogstraal et al. (1984) and

Roshdy et al. (1984). Ecologically all Argas species are

restricted to dry niches in desert, semi-desert, steppe or

savanna environments with long dry seasons or dry caves and

shelters. The one exception is A.(A.) macrostigmatus

Filippova which parasitizes crested cormorants,

Phalacrocorax aristotelis L., on islands in the Black Sea

(Hoogstraal et al., 1979b).












"he subgenus Argas has 25 species, distributed

worldwide (Hoogstraal et al., 1979b; Hoogstraal, 1985).

All members of the subgenus Argas parasitize birds. Most

parasitize birds on rocky nest sites such as cliffs, rocky

islands or stone masonry; the exceptions are the arboreal

nest parasites: A. dulus Keirans, Hoogstraal and Capriles

on the palm chat, Dulus dominicus (L.), in the Dominican

Republic (Keirans et al., 1971), A. monachus Keirans,

Radovski and Clifford on monk parakeets, Myiopsitta

monachus (Boddaert) in Argentina (Keirans et al., 1973),

and A. brevipes Banks which is found in tree holes and

parasitizes the birds that nest in these shelters (Kohls et

al., 1961). The Neotropical A. dalei Clifford, Keirans,

Hoogstraal and Corwin parasitizes the burrows of the South

American variety of the burrowing owl Athene cunicularia

(Clifford et al., 1976). There are two species of the

subgenus; A.(A.) cucumerinus Neumann and A.(A.)

macrostigmatus that specialize in parasitizing marine birds

(Hoogstraal, 1985).

The subgenus Persicargas consists of 15 species

distributed worldwide (Hoogstraal et al., 1979b). All

species in this subgenus parasitize birds that return

annually to the same nesting or resting site, or that

remain at the same site year round. All but one species

inhabits trees (Hoogstraal et al., 1983). The exception,












A.(P.) zumpti Hoogstraal, Kaiser and Kohls is found in

vulture nests in rocky situations but Hoogstraal (1985)

suspects it also inhabits trees.

The subgenus Microargas has only a single

representative species, Argas (M.) transversus Banks, a

parasite of the several subspecies of the Galapagos

tortoise, Geochelone elephantopus (Harlan) (Hoogstraal et

al., 1973). This very small tick (1.5 x 2.3 mm) undergoes

its entire life cycle, including the egg stage, under the

carapace of the tortoise against the leathery skin.

The subgenus Carios is composed of six bat

parasitizing species, one in the Paleartic, Ethiopian and

Oriental regions, two in the Oriental region and the rest

in the Australian region (Hoogstraal et al., 1979b;

Hoogstraal, 1985).

The subgenus Chiropterargas consists of four Old World

species. The hosts for these ticks are a wide variety of

genera of insectivorous bats (Hoogstraal, 1985).

The subgenera Carios and Chiropterargas have branched

from a single stem which apparently evolved from an Argas

parasite of birds nesting among rocks and adapted to cave-

dwelling bats (Roshdy et al., 1984). Roshdy et al. (1984)

summarized the external morphological similarities of the

two subgenera and focused on the Haller's organ structure.

In both subgenera the Haller's organ roof is solid,












differing from Argas, Microargas and Secretargas. The

Chiropterargas, in the evolutionary process, have diverged

more than Carios from the typical Argas (Hoogstraal, 1985).

The subgenus Secretargas consists of three species, a

single African species and two from Madagascar. Roshdy

(1963) examined the internal morphology of A.(S.)

transgariepinus and agreed with Hoogstraal's (1957)

conclusion that the subgenera Argas and Secretargas are

closely related.

The subgenus Ogadenus has only one species, Argas O.

brumpti Neumann, found in the eastern and southern portion

of the Ethiopian region.

In the Haller's organ study of Hoogstraal et al.

(1984) on Secretargas and Ogadenus a number of evolutionary

conclusions and hypotheses were presented. The Malagasy

Secretargas species and A.(O.) brumpti parallel some

Ornithodoros evolutionary trends such as sheltering in

soil, lizard host specificity and the phylogenetically

primitive unroofed Haller's organ capsule, but retain the

lateral suture that characterizes the Argas-Persicargas

stem of the genus Argas from which they evolved.



Genus: Ornithodoros

The genus Ornithodoros consists of about 110 species

in eight subgenera. However several species are unplaced












in any subgenera. Presently accepted subgeneric

classification was developed by Clifford et al. (1964) and

expanded by Keirans et al. (1977a). Taxonomic position

within subgenera, however, is not as well developed as for

Argas. Classification in the genus is heavily dependent

upon larval characteristics and is seen in the series of

papers describing most of the world's known larvae: Western

Hemisphere larvae (Kohls et al., 1965), Eastern Hemisphere

larvae (Sonenshine et al., 1966) and two revisions to

include fifteen new Western Hemisphere species (Kohls et

al., 1969; Jones and Clifford, 1972). Filippova (1966)

gives a comprehensive review of the Soviets' argasid fauna.

Hoogstraal (1985) has summarized most subsequent

information.

The subgenus Ornithodoros has eight representative

species. Most species are present in the Ethiopian region

with the O.(0.) moubata complex and 0.(O.) savignyi, but

the Neartic has O.(O.) eremicus Cooley and Kohls, the

Oriental region has O.(0.) indica Rau and Rao, and the

Paleartic 0.(O.) procaviae Theodor and Costa (Hoogstraal,

1985).

The sub-Saharan 0.(O.) moubata superspecies was split

by Walton (1962). His classification includes O.(O.)

apertus Walton, associated with African porcupines,

Hystrix; O.(O.) compactus Walton, associated with several












tortoise species, Testudo, south of the Zambezi river;

domestic and wild races of 0.(0.) moubata (Murray) and two

subspecies of 0.(0.) porcinus Walton: porcinus a wild

strain associated with warthogs, Phacochoerus, and

domesticus found in East African dwellings. Because of the

recent species split, much of the published literature on

O.(0.) moubata is difficult to interpret as to which

species or subspecies is being discussed. Several papers

by Walton (1953, 1957, 1958, 1960, 1964, 1979) could aid in

this interpretation.

The subgenus Pavlovskyella has 32 species that occur

in all regions of the world (Hoogstraal, 1985). All

species are primarily restricted to caves, burrows or dens.

All but one species parasitize mammals. However many are

known to utilize birds (4 species) and reptiles (5 species)

as blood sources also (Hoogstraal, 1985).

The subgenus Ornamentum is represented only by the

pajaroello, 0.(0.) coriaceus Koch, a Neartic species found

on the Pacific slope from California to Mexico. The

species parasitizes large herbivores, including deer and

cattle, and occasionally man. It is found in the soil under

trees that serve as "deer beds" in scrub oak forests

(Cooley and Kohls, 1944). This species is unique in that

it possesses two pairs of two eyes.












The subgenus Alectorobius is the largest in the genus

and the most diverse in habitat and host preference. It is

primarily a New World subgenus with a few Old World species

related to the marine bird parasite, O.(A.) capensis

Neumann. Hosts of the subgenus are bats (20 species),

birds (11 species), Galapagos iguanid lizards (2 species)

or miscellaneous hosts (9 species) (Hoogstraal, 1985).

The subgenus Proknekalia consists of three rare

swallow (Hirundo spp.) parasitizing species from the

Paleactic and Ethiopian regions. The subgenus is closely

related to Alveonasus and is remarkable for its

nonmammillate cuticle and for the fringed body setae of the

larvae. Little biological information is available for any

of the species.

The subgenus Subparmatus consists of three bat

parasites present in Central and South America. Notable

features of the species are unique ventral sclerotized

plates, a pointed hypostome and pulvilli on all adults and

nymphs (Cooley and Kohls, 1944). Hoogstraal (1985)

hypothesized that Subparmatus and the genera Antricola and

Nochoaspis represent two separate branches from a common

base in the subgenus Alectorobius, with the latter two

genera differing more distinctively than Subparmatus from

the typical Ornithodoros.












The subgenus Alveonasus consists of six species

present in the Old World which feed on a wide variety of

animals. This subgenus is quite distinct morphologically

and its subgeneric classification represents the most

notable dichotomy between the Western and Russian

systematic systems with the Russians recognizing it as a

genus (Pospelova-Shtrom,1946, 1969).

The subgenus Reticulinasus is an Old World group with

representation in all three geographic regions. There are

nine described and three undescribed species, all of which

are parasites of cave-dwelling fruit bats, usually

Rousettus spp. (Hoogstraal, 1985). Only for O.(R.) salahi

Hoogstraal have any biological data been published

(Hoogstraal, 1953a).

There are seven species in which subgeneric

affilations have not been defined (Kohls et al., 1965).

These are 0. cooleyi McIvor, a parasite of western U.S.

carnivores; 0. elongatus Kohls, Clifford and Sonenshine, a

larva from Dominican Republic with an unknown host; 0.

natalinus Cerny and Dusbabek, a Cuban bat parasite; O.

nattereri Warburton from Brazil; O. aragasi Fonseca and O.

davisi Fonseca from nests of rats (Oryzomys spp.) in Peru.

The last is O. rudis Karschan imported parasite in Central

and South America of rodent nests, chicken coops and humans

(Dunn, 1927).












Small Genera: Otobius, Antricola and Nothaspis

The genus Otobius has only two species 0. megnini

(Duges) and 0. lagophilus Cooley and Kohls. These species

from western North America adapted to parasitize roaming

mammals in the arid and semi-arid biomes (Hoogstraal,

1985). Otobius megnini parasitizes the ears of deer,

Odocoileus; pronghorn antelope, Antilocapra; domestic

cattle; horses; sheep; goats; dogs and occasionally man

(Cooley and Kohls, 1944). Otobius lagophilus parasitizes

the ears of rabbits (Silvilagus) and jackrabbits (Lepus).

The genus Antricola contains nine species in two

subgenera. They are specialized parasites of insectivorous

bats in the New World. Antricola (A.) coprophilus McIntosh

is found in the western states bordering Mexico, A.(A.)

mexicanus Hoffman in Central America and A.(Parantricola)

marginatus (Banks) in Cuba and Puerto Rico (Cooley and

Kohls, 1944). All other species are known only from Cuba

(de la Cruz, 1976, 1978a,b).

The genus Nothaspis is represented by a single

species, N. reddelli Keirans and Clifford. The species was

found in guano with Antricola mexicanus parasitizing

Mormoops bats in Mexico (Keirans et al., 1977b).












Life Cycles: Laboratory and Field

The life cycle of the Argasidae, as previously

mentioned, consists of eggs, larvae, several nymphal stages

and an adult stage that can have multiple reproductive

cycles. Between each genus, subgenus or even species there

are variations in the life cycle. Such variations are

either manifested as variable numbers of nymphal stages or

in the duration of a stages' feeding on the host: short

(minutes), long (days) or none. During the course of time,

coevolution of the ticks with their hosts has favored this

diversity of the life cycle (Hoogstraal and Kim, 1985). So

the comparison of various life cycles of ticks in relation

to the hosts they parasitize shows the optimum strategies

for survival and allows inferences to be drawn on the

mechanisms that contribute to this optimum developmental

pattern.



Argas

The life cycles of most members of Argas are

characterized by slow feeding larvae (days) and fast

feeding nymphs and adults (30-120 min.). There are usually

two to four nymphal stages (Kettle, 1984). The development

and reproductive pattern of nondiapausing Argas (A.)

africolumbae Hoogstraal, Kaiser, Walker, Ledger and

Converse indicate that two to three generations could












develop annually on chickens (Kraiss and Gothe, 1982).

Khalil (1979) found that the life cycle of A.(P.) persicus

(Oken) with low host availability could extend to more than

two years, but that 10 generations per year could occur

under optimal conditions.

Developmental diapause is not uncommon in Argas

species. In the Moscow area, Frolov (1971) found that

female A.(P.) persicus underwent diapause. Kaiser (1966a)

found that female A.(P.) arboreus Kaiser, Hoogstraal and

Kohls collected in the winter would hold off egg laying

for several weeks. Confirmation of naturally diapausing

females was found in a field study of A.(P.) arboreus in an

Egyptian rookery (Guiris, 1971). This diapausing condition

serves to synchronize host availability with the emergence

of the larva, the tick's most susceptible stage.

The life cycles of the bat-parasitizing species of

Argas show some unique developmental alterations that

probably evolved in response to the rarity of feeding

opportunities in the caves and shelters where they are

found. The field biology of these species has not been

reported.

The life cycle of the widely distributed A.(Carios)

vespertilionis (Latreille) was described by Hoogstraal

(1956, 1958). The females lay 3 to 4 batches of between 35

and 50 eggs over a 12 month period. The larval feeding












period on the bat is usually 17 to 19 days. There are two

nymphal stages which feed for short periods. Most adults

emerge from the second molt. The developmental time varies

from 56 to 80 days. The emerged female commences egg

laying no earlier than 13 weeks post emergence, after at

least two blood meals.

The life cycle of two of the Chiropterargas species,

A.(C.) boueti Roubaud and Colas-Belcour and confusus

Hoogstraal was described by Hoogstraal (1956). Argas (C.)

boueti females lay their eggs on vertical surfaces. The

larvae feed on the bats from 8-42 days but usually 16-25

days. The first and second nymphal stages do not feed.

Adults emerge after the second molt. Occasionally a third

nymphal stage occurs and it will feed prior to molting to

an adult. The life cycle can be completed in less than 100

days. The life cycle of A.(C.) confusus is longer: 120-300

days. The larvae feed from 5-50 days but usually 21-27

days. The first nymphal stage does not feed. The second,

third and fourth nymphal stages each feed. Adults emerge

from the fourth nymphal instar.



Ornithodoros

In the genus Ornithodoros a variety of developmental

modes exist. In the subgenus Ornithodoros, life cycles for

0.(0.) savignyi (Patton and Craig, 1913; Cunliffe, 1922)












and O.(0.) moubata (Hoogstraal, 1956) have been studied.

The females, considering their relatively large size, lay

few eggs per egg batch, averaging 219 (100-417) for O.(0.)

savignyi. Over the 5 to 7 feeding/egg laying period in the

females' life she can lay 900 in O.(0.) savignyi and 500-

1200 in O.(0.) moubata. The larvae hatch from the large

egg and molt to nymphs without feeding. As many as eight

nymphal instars can occur but four or five is usual, with

males emerging at earlier molts than females.

Life cycle studies of several Pavlovskyella species

has shown that the larvae, nymphs and adults are rapid

feeders. An exception is Ornithodoros (P.) tartakovski

Olenev whose nymphs and adults in winter are known to

remain attached to the hosts for several days (Hoogstraal,

1985). The life cycles have from two to five nymphal

stages, males frequently emerging at earlier molts,

usually third or fourth instar, than females, normally

fourth or fifth instars. Balashov (1968) states that there

is only one gonotropic cycle per year, occurring in the

warm season for O.(P.) tholozani Laboulbene and Megin and

O.(P.) verrucosus Olenev, Zesukhin and Fenyuk, but two in

O.(P.) tartakovski under favorable conditions. Life spans

can exceed 23 years (Pavlovskii and Skrynnik, 1960).

Autogeny, the production of viable eggs without a meal,

as an adult is known from four species of Ornithodoros.












All four are Pavlovskyella species. Feldman-Muhsam (1973)

reported autogeny in 0. tholozani, 0. tartakovskyi and 0.

parkeri Cooley with a more detailed comparison of

anautogenous and autogenous females productivity in 0.

tholozani (Feldman-Muhsam and Havivi, 1973). Although not

reported to occur in laboratory colonies of 0. arenicolous

Hoogstraal by Feldman-Muhsam, Hoogstraal (1953b) reports

that autogeny occurs with field collected individuals.

Loomis (1961) described the life cycle of

0.(Ornamentum) coriaceus from data obtained in his

laboratory and from several earlier researchers. It was

found that as many as seven molts occur, but that most

individuals molt to adults after the fifth nymphal stage.

The life cycle in the laboratory takes 15 months but

probably needs no less than two years in the field. The

larvae feed on the host for 7 to 10 days with the first two

nymphal stages being non-feeding (Clifford et al., 1964).

The life cycle of Alectorobius is known for several

species. In bats, the life cycles of O.(A.) kelleyi Cooley

and Kohls and O.(A.) tadaridae Cerny and Dusbabek have been

followed in the laboratory. Sonenshine and Anastos (1960)

reared O.(A.) kelleyi. The life cycle consists of eggs,

larvae, 2 to 4 nymphal instars and adults. They found the

time span for the cycle varied from 54-258 days. The

larvae fed on wild bats stayed attached longer, 9 to 20












days (15.4 mean), versus 8 to 18 days (12.2 mean) on white

rats. The first nymphal stage was non-feeding. Males

emerged from the second or third nymphal molts, whereas

females emerged from the third or fourth nymphal molts.

Nymphal and adult feeding time rarely exceeded 1.5 hours.

The Cuban O.(A.) tadaridae feeds mostly on bats that roost

in palm trees and its life cycle was examined by Honzakova

et al. (1983). In this case, larval feeding was shorter

(6-13 days) and adult feeding longer (10 hours). This

species fed in the first nymphal instar. Hoogstraal (1985)

states that in those O. (Alectrobius) species that feed on

bats a feeding first nymphal instar is normal.

In all other Alectorobius species for which life cycle

information is known, the first nymphal instar is non-

feeding. This is known from the rodent feeding species:

O.(A.) talaje (Guerin-Meneville) (Davis, 1942c), 0.(A.)

puertoricensis Fox and O.(A.) dugesi Mazzotti (Davis, 1955)

and the bird parasitizing species: 0.(A.) concanensis

Cooley and Kohls (Davis, 1942c) and O.(A.) coniceps

Canistrini (Davis and Mavras, 1956). In O.(A.)

puertoricensis the span from larvae to adult varied from

one month to six weeks with males emerging from the third

nymphal instar and females from the fourth and fifth (Fox,

1947; Davis, 1955).











In the marine bird parasitizing Ornithodoros capensis

group, life cycles have been reported for four species:

O.(A.) muesebecki Hoogstraal (Hoogstraal et al., 1970),

O.(A.) coniceps (Hoogstraal et al., 1979a), O.(A.) amblus

Chamberlin (Khalil and Hoogstraal, 1981) and O.(A.)

spheniscus Hoogstraal, Wassef, Hays and Keirans (Hoogstraal

et al., 1985). In those examined, there was a long feeding

period (4 to 23 days) for larvae and a non-feeding first

nymphal instar. As many as six or seven nymphal instars

were found, with adults emerging after the fourth. Minimum

life cycle length was under six months in optimum

laboratory conditions. Pavlovskii and Skrynnik (1960)

reported a maximum lifespan of 4 years for O.(A.) coniceps.

The life cycle of Otobius species is different from

most soft ticks. Otobius megnini larvae hatch from eggs

after 11 days in summer and 3-8 weeks in cooler weather.

The larvae attach in the ear and remain attached 5-11 days.

The two nymphal stages can remain attached for as long as

seven months, but two to three months is normal. The

engorged second instar nymphs drop off and crawl up to some

dry crevice or crack and molt. Adults possess non-

functional mouthparts. Males live for up to 160 days

(average 100 days) with females living as long as 638 days

producing from 358 to 1546 eggs (averaging 814 eggs)(Hooker

et al., 1912). Otobius lagophilus has a similar life cycle












with females averaging 175 eggs (100-250) (Hopla, 1955).

Nymphs appear not to be restricted to the ears, having been

collected while attached to the throat and jaw.



Antricola and Nothaspis

Antricola adults do not feed and have a nonfunctional

short hypostome. Only the larvae have been collected on

bats, but engorged nymphs have been collected (Hoogstraal,

1985; de la Cruz, 1976; Cooley and Kohls, 1944). In

Nothaspis the males have a nonfunctional hypostome and the

female is unknown. Nymphs are physically capable of

feeding (Keirans and Clifford, 1975). Larval identity is

unclear, so no conclusions can be drawn on the its feeding

ability.



Ecological Niches Utilized by the Argasidae

Troglodytic Niches

The life styles of species in the family Argasidae can

be grouped under three headings: Troglodytic (hole

dwellers), niticolous (nest dwellers) and free living.

This classification provides for easier comprehension of

the host-parasite ecological interrelationships.

Classification of soft ticks on this basis does not reflect

taxonomic classification.












There are three subgroups of troglodytic niches:

burrows, caves and xeric shelters. There are a number of

varieties of burrows utilized by one or more species of

soft tick: large burrows (warthogs, foxes and other

canines), small burrows (burrowing owls, shearwaters,

penguins and other marine birds) and reptile burrows

(tortoises and lizards). Caves are used by bats, birds

(falcons, swallows, sparrows, etc.), and small mammals, all

of which are parasitized in these habitats by argasids.

Xeric shelters are a variety of cave habitat in which the

external environmental conditions, except rainfall, are

relatively unmodified. Examples of this type are shallow

caves, cliff overhangs, primitive livestock sheds and human

dwellings. Members of the genus Ornithodoros are the

predominant species that have specialized in parasitizing

troglodytic niches. However cave bat specialization is

found in some Argas subgenera and two Ornithodoros derived

genera: Antricola and Nothaspis (Hoogstraal, 1985).



Niticolous Habitats

Most niticolous habitats are provided by birds but

some by mammals also living in nests. Nest habitats

include not only the familiar vegetation or mud constructed

nests, but also substrate nests used by many marine birds,

raptors, doves and pigeons. Mammalian nest constructors












parasitized by argasids include squirrels, rock hyrax,

mice, woodrats and other rodents. Only those niticolous

habitats that are utilized for several seasons or years

have argasids present. Members of the genus Argas are the

predominant species involved in parasitizing niticolous

habitats (Hoogstraal et al., 1979b).



Free Living Hosts

There are very few argasid species that can be

classified as parasites of free living or motile host

species such as antelope and deer. Argasids parasitizing

this type of host have had to evolve physiological or

parasitic behavioral mechanisms to circumvent the

sensitivity to environmental variations, both climatic and

nutritional (host availability), that appear to have

restricted most other argasid species to specific habitats.

The only argasid species that are classified as using this

type of host are Ornithodoros 0. savignyi, O. O. coriaceus,

O. P. gurneyi Warburton, and the two Otobius species, 0.

megnini and 0. lagophilus.



Pathogens Associated with Argasid Ticks

Argasid ticks transmit a wide variety of infectious

disease agents. With the exception of African tick-borne

relapsing fever caused by Borrelia duttoni (Novy and Knapp)












vectored by 0.(0.) moubata (Felsenfeld, 1971), all are

zoonoses, intertransmissible between animals or man. The

ability of soft ticks to serve not only as vectors, but

also as reservoirs significantly affects the focality and

epidemiology of the diseases. The range of disease agents

vectored by Argas and Ornithodoros include RNA and DNA

viruses, rickettsia, spirochetes, protozoa and nematodes.

Pavlovski (1960) classified foci of vectored illnesses by

their biological, abiotic and geographic features. Since

argasid ticks generally are confined to very specific

habitats, e.g., caves, burrows, cliff faces, bird nests,

etc., and their probability of individual survival out of

these habitats is low (Aviva et al., 1973), the natural

focus of most Argas and Ornithodoros vectored diseases is

limited to small areas of the biotype. So, in most cases,

these agents present little threat to man or his livestock.

Exceptions to this statement apparently are confined to

those zoonoses (1) in which a polyvectoral foci exists with

the second vector being more environmentally motile, such

as mosquitoes and hard ticks or (2) where human activity

either comes into contact with or generates an ecologically

similar foci to the autochthonous foci thus allowing

disease and/or vector crossover to the domestic habitat.

The following is a discussion on the focality of argasid

transmitted diseases based upon the commonality of niche












specialization in the various species of the family

Argasidae.



Burrow Habitats

Most burrows are constructed by small animals but a

few larger animals also construct them. Examples are

warthogs in the family Suidae and many canids such as

foxes, coyotes and jackals. In the burrows of warthogs are

found Ornithodoros porcinus, the reservoir vector of

African swine fever virus, and several other species in the

O.(0.) moubata complex including 0.(0.) moubata and 0.(0.)

apertus (Walton, 1979).

In Africa Ornithodoros (0.) porcinus is infected and

the African swine fever virus is transmitted transtadially,

sexually and transovarially (Plowright et al., 1970, 1974),

with the tick serving as vector, amplifier and reservoir

for the disease. In Africa, the virus circulates between

the tick and the warthog and bushpig in the burrows the

swine excavate (Thomson et al., 1980; Plowright et al.,

1969). In these wild swine, infection does not lead to

death, but in domestic swine death is common. Primary

outbreaks of ASF in domestic swine was believed to be due

to contact with "carrier" wild pigs but this can be

discounted (Thomson, 1985). Thomson provided evidence

showing that Ornithodoros species can be found in high












numbers on warthogs away from the burrow generating support

for the theory of Plowright et al. (1969) that ASF infected

ticks could be transported to the vicinity of domestic pigs

either by warthogs or on the carcasses of warthogs. Ticks

dislodged there could remain a potential source of

infection for many months. This phoretic dispersal of soft

ticks also explains how a giant forest hog, a solitary

forest dweller, might encounter an infected tick.

The Ornithodoros moubata complex has served as a

laboratory vector of several important pathogens.

Ornithodoros moubata strains of unknown origin have been

shown to vector Coxiella burneti (Derrick) (Q fever)

(Davis, 1943c), Francisella tularensis (McCoy and Chapin)

(Tularemia) (Burgdorfer and Owens, 1956) and Leptospira

interrogans (Stimson) (Burgdorfer, 1956; Strickland, 1984).

Similar ability to vector these diseases was shown, also by

the authors, in the small burrow inhabiting, rodent-

parasitizing, species: O.(P.) parkeri, O.(P.) turicata and

O.(P.) hermsi Wheeler, Herms and Meyer. Rocky Mountain

spotted fever (RMSF) caused by Rickettsia rickettsi

(Wolbach) can be vectored experimentally by O.(P.) parkeri

(Davis, 1942a,b) and O.(P.) rostratus Aragao (Davis,

1943b). Several other argasids are able to be infected by

RMSF, but not able to vector it: O.(P.) turicata (Davis,

1942a,b, 1943a), 0. rudis (Davis, 1943b; Hoogstraal, 1967)











and O.(P.) nicollei and Otobius lagophilus (Hoogstraal,

1967). The European ixodid vectored pathogen Rickettsia

sibirica Zdrodovskii (=R. slovaca) was found in A.(P.)

persicus infecting poultry in Armenian SSR (Rehacek et al.,

1977). No published field data implicate any of these

ticks as significant factors in the epidemiology of these

diseases. However, all of these agents are significant

diseases of burrow-dwelling rodents and livestock, and the

possibility that argasids may serve as secondary vectors

and reservoirs of these diseases might aid in the stability

of these diseases in the biocenosis.

Natural transmission of Q fever by burrow-inhabitating

Ornithodoros has been demonstrated, but the epidemiological

significance of this transmission is questionable

(Hoogstraal, 1985). Balashov (1968) reviewed data that

O.(P.) tholozani is involved in the natural transmission of

Coxiella burneti (Derrick) in the warm deserts of the USSR.

Ornithodoros (P.) marocanus Velu (0. erraticus "large

form") outside Casablanca, Morocco, parasitizes rabbits,

Oryctolagus cuniculus (L.) that were naturally infected

with C. burneti and the ticks transmitted the agent in the

laboratory to guinea pigs during feeding (Blanc and

Bruneau, 1955).

In North America the two small burrow-inhabiting tick

species are O.(P.) turicata and O.(P.) parkeri.












Ornithodoros (P.) turicata is also found in numerous small,

usually shallow caves and, occasionally, livestock pens.

Cooley and Kohls (1944) report the hosts of O.(P.) turicata

to be rattlesnakes, turtles, tortoises, burrowing owls,

ground squirrels, prairie dogs, woodrats, rabbits, pigs,

cattle, horses and man. Beck et al. (1986) recognized two

subspecies of this tick, with the disjunct peninsular

Florida population having the name O. t. americanus.

Besides the physical separation they discuss life cycle and

biological differences.

Ornithodoros (P.) parkeri is a close relative of

0.(P.) turicata (Cooley and Kohls, 1944). It is a parasite

in the burrows of ground squirrels, prairie dogs and

burrowing owls in the western United States. Its range is

more northern than O.(P.) turicata (Cooley and Kohls,

1944). Its life cycle is shorter with up to five nymphal

stages, but adults begin emerging from second nymphal

stages (Davis, 1941b). This shorter life cycle may be

evolutionary favored in the cooler climate it inhabits

because of the imposed shortened seasonal activity period.

The only diseases transmitted normally by these two

Ornithodoros species are Borrelia. Borrelia classification

difficulties antigenicc drift, serological variations and

mutations) led to the belief in tick specificity of the

respective species, which were often named after the












species of Ornithodoros from which they were isolated

(Felsenfeld, 1979). However, laboratory experiments

transmitting one Borrelia species to another tick that does

not carry it naturally or from a louse to a tick are often

successful. Hence, there was a trend toward the

recognition of one Borrelia species with the tick adapted

strains being recognized as variants or subspecies

(Felsenfeld, 1979). For practical and epidemiological

reasons the multispecies concept is adhered to in this

discussion.

In the two species O.(P.) turicata and O.(P.) parkeri

the Borrelia species are turicatae and parkerii. The ticks

serve not only as the vectors of these diseases, but also

as amplifiers and reservoirs through transtadial survival

and transovarial transmission (Davis, 1941a, 1942a,b,c,

1943b). Felsenfeld (1979) proposed the hypothesis that

borreliae are primarily symbionts and parasites of ticks,

that have specialized in Ornithodoros species by genetic

evolution and adaptation and that vertebrate invasion is an

evolutionary accident. However, the fact that uninfected

ticks can pick up the infection from a host with a

spirochetemia (Davis, 1941a), and that highly virulent

strains that produce high spirochetemia in the host are

maintained in nature (Felsenfeld, 1971), suggests that the

ability of Borrelia to infect vertebrates is evolutionary












favored as a mechanism of increasing the percentage of tick

infections since transtadial and transovarial mechanisms

are not completely effective (Gaber et al., 1984).

Borreliosis due to infection from O.(P.) turicata and

O.(P.) parkeri bites or contact with coxal fluid is rare in

man. Burgdorfer (1980) stated that of 280 cases of

relapsing fever in the U.S. (1954-1978), only 30 cases

could be attributed to B. turicatae (Brumpt) and none to B.

parkerii Davis. The greater number of cases of B.

turicatae is probably due to its vector being adapted for

survival in a wider variety of habitats (Cooley and Kohls,

1944) that come in contact with man and his activities.

Primarily these species are zoonoses of ticks and burrowing

rodents (Davis, 1942a, 1943b).

In the Neotropics, three species (O.(P.) furcosus

Neumann, O.(P.) braziliensis Aragao and O.(P.) rostratus)

exist that are primarily parasites of burrowing rodents,

but commonly attack man, dogs, livestock and peccary

(Hoogstraal, 1985). Only O.(P.) braziliensis is known to

carry a disease: B. braziliensis. Ornithodoros (A.)

puertoricensis, a Carribean species, parasitizes Rattus and

iguanids in burrows and is a potential vector of ASF in

this region (Butler et al., 1985).

In the African region there are twelve species that

are parasites of burrowing animals, eight of them are not











present elsewhere. All of these eight species are known

from several geographic areas and are presently

epidemiologically insignificant. These eight are

represented by Ornithodoros (0.) compactus which

parasitizes tortoises, Testudo spp. in scrapes south of the

Zambezi River (Walton, 1962); O.(A.) delanoei Roubaud and

Colas-Belcour from burrows and caves and parasitizing

hedgehogs, porcupines and small rodents across North Africa

(Hoogstraal, 1956, 1985); O.(A.) eboris Theiler from a few

specimens collected in a porcupine burrow in South Africa

(Hoogstraal, 1985); 0.(P.) normandi Larrousse a parasite in

rodent burrows in Tunisia (Hoogstraal, 1956); O.(P.) sonrai

a parasite of the grass rat (Arvicanthis) in Senegal

(Wallis and Miller, 1983); O.(P.) zumpti inhabits burrows

of the striped mouse, Rhabdomys pumilio (Sparrman) and

other rodents in Cape Province, South Africa (Hoogstraal,

1956); O.(P.) arenicolous in North African mammal burrows

(Hoogstraal, 1953b) and O.(P.) greinieri from lowland

forest burrows of the endangered rodent Hypogeomys antimena

Grandidier in Madagascar (Hoogstraal, 1985).

There is little disease transmission in these African

endemics. From these species in the Ornithodoros and

Alveonasus subgenera no diseases have been reported. In

the Pavlovskyella species both viruses and borreliae are

known. Borrelia tillae Zumpt and Organ is known from












O.(P.) zumpti (Zumpt and Organ, 1961) and a Borrelia strain

was found in O.(P.) normandi (Hoogstraal, 1956). Because

of confusion in the literature in separating O.(P.) sonrai

from O.(P.) erraticus, the reports of a Borrelia in o.(P.)

sonrai need to be re-examined. Wallis and Miller (1983)

point out that the two species are separable, not only

biochemically, but by the respective Nairovirus they each

vector; Qalyub virus in O.(P.) erraticus and Bandia in

O.(P.) sonrai. These two members of the Qalyub serogroup

(Bunyaviridae) are not only vectored by ticks, but the

ticks are also the reservoirs for these viruses

(Hoogstraal, 1985).

The Paleartic region shares with Africa several rodent

burrow parasitizing argasids. Some are the most prominent

in epidemiological importance in the whole family. They

are O.(P.) erraticus, O.(P.) tholozani, O.(P.) morocanus

and O.(A.) foleyi Parrot. Ornithodoros (A.) foleyi is the

exception, since this desert species has had no virus or

spirochetes isolated from it (Hoogstraal, 1985). Although

O.(P.) tholozani is known from burrows, its importance as a

vector is related to its activities in caves and animal

shelters and will be discussed in the next section.

The most recently prominent member of this group is

O.(P.) morocanus, a species previously synonomous with

O.(P.) erraticus that is found in Spain, Portugal and












northwestern Africa (Hoogstraal, 1985). This tick is the

vector and reservoir of B. hispanica (de Buen), the

causative agent of Hispano-African tick-borne relapsing

fever (Felsenfeld, 1979). Following the introduction of

ASF virus into Portugal and Spain (between 1957 and 1960)

this tick became infected with the virus and the disease

became endemic (Wilkinson, 1981). Like O.(P.) tholozani,

but not like O.(P.) erraticus, this tick species infests

not only burrows, but also stables and pens of domestic

livestock, especially in cooler or mountain regions

(Pospelova-Strom, 1953; Hoogstraal, 1985). Avivi et al.

(1973) correlated O.(P.) tholozani migration out of the

protected cave and burrow habitat with atmospheric relative

humidity.

Ornithodoros (P.) erraticus is distributed from

northern Africa, across northern Arabia, to Turkey,

southwestern USSR and into Iran. Hoogstraal (1985)

considers O.(P.) alactagalis and O.(P.) neerensis to be

junior synonyms. Hoogstraal et al. (1954) studied this

species in Egypt discovering in the rodent burrows it

parasitizes a wide variety of rodents, lizards, burrowing

owls and even a toad (Bufo spp.). There may be two

generations annually.

A wide variety of diseases are transmitted by this

species. Qalyub virus (Nairovirus) in Egypt (Wallis and











Miller, 1983) and Artashat virus (Bunyaviridae,

unclassified serogroup) in Armenian SSR (L'vov et al.,

1975b) were isolated from this species. Qalyub virus

replication and transmission in the tick was examined by

Miller et al. (1985). The only piroplasm vectored by a

soft tick, Babesia (Nuttallia) meri Gunders is transmitted

by O.(P.) erraticus (Gunders and Hadani, 1974). The

piroplasm infects the fat sand rat, Psammoys obesus

Cretzschmar. Several hard ticks and O.(P.) tholozani that

parasitize the rat, were incapable of transmitting the

agent.

Borrelia crocidurae (Leger), the causitive agent of

North African relapsing fever, is vectored by O.(P.)

erraticus. Gaber et al. (1984) provided distribution, host

information, ecology, seasonal dynamics and transmission

information. The other local Ornithodoros tick in Egypt,

O.(O.) savignyi that has never been found to be infected in

nature, was also examined for spirochete transmission. The

sand tampan O.(0.) savignyi could harbor it transtadially

but not transovarially.

Hyperparasitism is very common in O.(P.) erraticus and

this could serve to increase the overall incidence rate of

infection in the tick population (Helmy et al., 1983). The

report also summarizes evidence on six other argasid

species, including O.(P.) tholozani and O.(P.)











tartakovskyi, that have been observed to hyperparasitize,

and all are associated with Borrelia transmission.

Human lice, Pediculus humanus, biting B. crocidurae-

infected animals easily acquire and maintain the infection

(Haberkorn, 1963a,b). Thus, louse-infested persons who are

bitten by infected O.(P.) erraticus may experience tick-

borne relapsing fever and serve as a source of louse-borne

B. crocidurae (Gaber et al., 1984). Hoogstraal (1985)

expressed the hypothesis that the epidemic of louse-borne

relapsing fever in Egypt and North Africa after World War

II may have been due to this spirochete, and not to

Borrelia recurrentis (Lebert).

In the Paleartic region, excluding North Africa, the

remaining burrow inhabiting species are O.(P.)

tartakovskyi, O.(P.) cholodkovski Pavlovsky and O.(P.)

asperus Warburton. Ornithodoros (P.) tartakovskyi, the

most significant epidemiologically, is distributed in

southern Russia, Iran, Afghanistan and China (Fillippova,

1966). It inhabits the burrows of rodents and small

carnivores, as well as the resting places of hedgehogs,

tortoises, other reptiles and, infrequently, shelters of

livestock. Its life cycle may be completed in three to

four months or may extend to two years. Unlike other

Pavlovskyella species, it is known for remaining attached

to the host for long periods of time especially in the











winter (Hoogstraal, 1985). It can survive 12 years under

laboratory conditions (Pavlovskii and Skrynnik, 1960).

Ornithodoros (P.) tartakovskyi is the natural vector

of the filarial worm Dipetalonema viteae Krepkogorskaja

that infects central Asian gerbils (Hoogstraal, 1985).

Borrelia latyschevii (Sofiev), the causative agent of

Central Asian relapsing fever, is transmitted by O.(P.)

tartakovskyi and causes a mild disease. Another severe

disease causing agent is Borrelia caucasia Kandelaki

transmitted by O.(P.) asperus (O.(P.) verracosus ?)

(Felsenfeld, 1971). Plague has been associated with O.(P.)

tartakovskyi (Hoogstraal, 1985).

Chim virus is found in both argasids, (O.(P.)

tartakovskyi and O.(P.) tholozani) and ixodids

(Rhipicephalus (R.) turanicus) Pomerantsev, that inhabit

the burrows of the great gerbil in Uzbek SSR (L'vov et al.,

1979).



Caves and Shelters

This category is an ecological catch-all in that its

premise, a natural geological shelter, or an artificial

shelter that architecturally simulates a natural one, with

xeric conditions but with ambient or high relative

humidity, is ecologically quite wide. The subcategories,

sheds and houses, overhangs and shallow caves, and deep












caves were defined on ecological and epidemiological

parameters.



Sheds and Houses

Several species have adapted to become synanthropic.

The two most important are Ornithodoros (0.) moubata

"domestic race" and O.(0.) porcinus domesticus. These are

associated not only with some homes in most of Africa, but

also with domestic animal enclosures and pigsties, where

ASFV might circulate (Haresnape and Mamu, 1986).

African relapsing fever, Borrelia duttoni, circulates

only between these ticks and man in domestic situations.

The disease is distributed through most of sub-Saharan,

East and South Africa. The development of an infection in

the tick is typical of all known Ornithodoros spirochete

infections (Geigy, 1968). The Borrelia are passed both

transtadially and transovarially. The highest spirochete

densities develop in young nymphs and adults in the

salivary glands, but in older females in the ovaries.

Transmission of the agent to the mammalian host is usually

by bite, but coxal gland fluid is often infective if it can

reach an open wound.

In central and northern South America, Ornithodoros

rudis apparently has developed a similar relationship where

it parasitizes both man and livestock (Cooley and Kohls,











1944) in addition to its normal rodent hosts. This tick

transmits Borrelia venezuelensis Brumpt (=neotropicalis)

(Felsenfeld, 1971, 1979). Transovarial transmission of the

spirochete has not been observed in this tick (Felsenfeld,

1979). There are only two soft tick species outside the

subgenus Pavlovskyella that transmit a mammalian infecting

Borrelia zoonoses, 0. rudis is one and the other is, 0.(0.)

coriaceus (Hoogstraal, 1985). Ornithodoros rudis has also

been associated with domestic situations in which Rocky

Mountain spotted fever (RMSF) circulated (Hoogstraal,

1967).

The remainder of the species that infect houses and

sheds are primarily livestock pests. These include O.(P.)

tholozani, O.(P.) morocanus (previously discussed), O.(P.)

turicata (previously discussed), O.(A.) canestrinii

(Birula) and O.(A.) lahorensis Neumann. These are all

species that have undergone niche crossover, the

Pavlovskyella species from burrows and the Alveonasus

species from shallow caves and overhangs.

Ornithodoros (P.) tholozani is a widely distributed

Old World species found from Libya through the Near East

and Greece through southern Russia, northern India into

southwestern China. It is referred to as O.(P.) papillipes

and O.(P.) cross in the Soviet and Indian literature

respectively. Aviva et al. (1973) studied the ecological












parameters of its survival in caves in Israel. Pospelova-

Shtrom (1953) found that in Russia it was present only in

those caves, houses or animal shelters with temperatures of

24-250C and a relative humidity of 70-75%. In

Turkmenistan, the tick can be found in cool mountain

elevations in more exposed natural shelters, such as under

rocks, but in the dry foothills only in caves and burrows.

In Israeli caves that house animals continuously, tick

populations can be high. In those caves that are used

infrequently, tick population numbers differ greatly, but

usually numbers decrease with only late nymphs and females

present. These ticks are deeply buried in the soil and do

not emerge to attack casual cave inhabitants (Avivi et al.,

1973).

The known hosts are reviewed by Hoogstraal (1985).

They include man, sheep, goats, porcupines (Hystrix),

hedgehogs (Hemiechinus, Paraechinus), foxes, badgers,

jackals (Canis) and numerous rodents. Camels, cattle and

birds, including chickens, also serve as hosts.

Ornithodoros (P.) tholozani is known to be involved in

two Flavivirus species zoonoses. West Nile virus was

isolated from the tick (L'vov et al., 1975a). This virus

normally circulates between culicine mosquitoes and birds,

occasionally affecting man (Berge, 1975). Karshi virus was

found in 0.(O.) tholozani and Hyalomma asiaticum, two












parasites of the great gerbil, Rhombomys opimus

(Lichtenstein), in Russia (L'vov et al., 1976; Hoogstraal,

1985). Chim virus, previously mentioned, also circulates

between argasids and ixodids in the burrows of this gerbil

(L'vov et al., 1979).

Associated with O.(P.) tholozani is the pernicious

Persian relapsing fever, Borrelia persica (Dschunkowsky)

(Felsenfeld, 1971, 1979). This tick's adaptability and

ready acceptance of man, his domestic animals and domestic

rodents as sources for blood meals (Balashov, 1968;

Hoogstraal, 1981) provides opportunity for human

infections. Additionally, lice are known to pick up B.

persica (Felsenfeld, 1971) thus increasing the

epidemiological importance of this tick.

The most important species in the subgenus Alveonasus

is O.(A.) lahorensis. It was originally a parasite of the

Asiatic mouflon, Ovis aries Linnaeus and other wandering

ungulates that rested on cliff faces, but is now a

notorious parasite of domestic sheep, goats, camels and

cattle in western China, Pakistan and from southern Russia

to Saudi Arabia (Fillippova, 1966). In Russia this tick

has become a serious parasite especially in primitive

stables.

Its life cycle is unusual in that it resembles a two-

host tick. The larvae, which can survive for a year unfed,












attach to the host for 3 to 6 weeks and drop off as third

instar nymphs. After molting, the tick becomes an adult

and will feed for 2-3 hours. Females can produce two egg

hatches (300-500 eggs). Unfed adults can survive for 18

years (Fillippova, 1966). This life cycle and the

longevity of the stages has allowed the parasite to readily

adapt to parasitizing domestic animals. The developmental

adaptability and high survivability of this tick places it

also in the free living category. However, because of its

dependence upon some form of shelter, it is included here.

The unique life cycle of this tick, with long host

attachment periods, is epidemiologically relevant because

of the increased probability of a disease-infected tick

being introduced to an area where it may serve as the

source of a new disease foci. Its long lifespan means a

reservoir exists with a lifespan equal to or greater than

its hosts, so it may encounter and infect one to three

naive host generations during the course of its life.

Two disease agents are involved with this species.

Crimean-Congo hemorrhagic fever virus was isolated from a

larva collected from a horse (Sureau et al., 1980).

Hoogstraal (1985) suspected the isolate came from active

virus in the undigested blood meal rather than a true

infection. There is a single report of Anaplasma

transmission by argasids. Immature O.(A.) lahorensis












became infected with Anaplasma ovis Lestoguard when feeding

on sheep and could transmit it to other sheep (Bityukov,

1953). There is also an early report by Kamil and Bilal

(1938) that the tick was capable of transmitting tularemia.

Kusov et al. (1962) stated that all stages are capable of

transmitting Q fever and the association between this tick

and domestic animals implicates it in the epidemiology of

the disease.

Ornithodoros (A.) canestrinii is found in Iran and

Turkmen SSR. It parasitizes wild sheep, goats and gazelles

in caves or overhangs. Domestic animals are also

parasitized in stables (Hoogstraal, 1985). Kusov (1973)

reported its biology. He reported the life cycle may

require 10-16 years. Presently no diseases are known to be

vectored by this species.



Shallow Caves and Overhangs

A variety of species in several subgenera of

Ornithodoros and Argas have adapted to parasitizing hosts

in shallow caves and overhangs. Two 0. (Alveonasus)

species: foleyi and acinus Whittick parasitize large

animals sheltering in these habitats (Hoogstraal, 1985).

Numerous 0. (Pavlovskyella) species utilize this habitat in

addition to burrows but O.(P.) graingeri Heish and

Guggisberg, the spirochete host for B. graingeri Heish











(Heisch, 1953), is specifically known from cave habitats

(Hoogstraal, 1956; Condry et al., 1980). The three Argas

(Secretargas) species live in this habitat type but, unlike

the bat-parasitizing African species, the species from

Madagascar utilize a "micro" version provided by small to

medium size rocks (Hoogstraal et al., 1984). The most

unusual among all of these is A.(A.) cucumerinus. This

species has developed a quick feeding larva (all other

subgenus Argas species use a longer feeding period) and

parasitizes marine birds that rest but do not nest on the

Peruvian sea cliffs where these ticks reside (Clifford et

al., 1978).



Deep Caves

All cavernicolous species included in this section are

parasites of bats, except for the Australian falcon

parasite, A.(A.) lowryae Kaiser and Hoogstraal, in which

the single collection came from birds which were nesting in

a cave (Kaiser and Hoogstraal, 1975). In the Old World,

insectivorous bats are parasitized by species in the

subgenera A. (Carios) and A. (Chiropterargas) (Hoogstraal,

1956, 1985) and cave dwelling fruit bats by the subgenus O.

(Reticulinasus) (Hoogstraal, 1953). In the New World only

Ornithodorinae species parasitize bats. Bats are the sole

hosts of the subgenus Subparmatus, and the genera Antricola












and Nothaspis. About half of the species in the 0.

(Allectorobius) subgenus have bats as their sole known

host.

Kyasanur Forest disease (KFD) virus was isolated from

0.(R.) chiopterphila Dhanda and Rajagopalan, a fruit bat

parasite in India (Dhanda and Rajagopalan, 1971). Normally

KFD is a disease transmitted by hard ticks, especially

Haemaphysalis, in which transtadial but not transovarial

transmission occurs (Hoogstraal, 1966, 1981).

Experimentally, transtadial, transovarial and Fl

transmission of KFD to susceptible hosts have been

demonstrated for A.(P.) persicus (Sengh et al., 1971) and

O.(P.) tholozani (Bhat and Goverdhan, 1973). The

importance of any of these ticks in the transmission cycle

of this disease is unclear (Hoogstraal, 1985). Two

serologically ungrouped viruses were isolated from O.

Reticulinasus species: one from Muroor, India, in the tick

O.(R.) piriformis Warburton (Sreeivasan et al., 1983) and

one from an undescribed species in Chobar Gorge, Nepal

(Berge, 1975).

Another bat associated Flavivirus species is Sokuluk,

isolated from the insectivorous bat-feeding A.(C.)

vespertilionis in southern Russia (L'vov et al., 1973).

Hoogstraal (1980) suspects that Keterah virus from A.(C.)

pusillus Kohls and Issyk virus from A.(C.) vespertilionis












and Ixodes (E.) vespertilionis Koch may be geographic names

for the same virus. Hoogstraal (1985) reviewed data from

several Russian authorities which indicate that this virus

or virus complex, regarded as being associated chiefly with

bats and bat-parasitizing Argas (Carios) and Ixodes ticks,

should be appreciated as being more serious

epidemiologically in light of demonstrated circulation

between birds, mosquitoes and man.

In the New World, Estero Real virus was isolated from

O.(A.) tadaridae, a bat parasite in Cuba where its

circulation probably does not affect birds, humans or

domestic animals (Malkova et al., 1985). Matucare virus

from Bolivia was isolated from the bat parasite O.(A.)

boliviensis Kohls and Clifford (Justines and Kuns, 1970).

Both of these viruses were collected from atypical subgenus

representatives. Both ticks feed on bats that do not

utilize caves, but instead live in palm trees or, in the

case of the O.(A.) boliviensis specimens mentioned, live in

the palm leaf thatch of huts. Considering the ease in

collecting specimens in palm trees versus caves, it is not

surprising that Neotropical bat-circulating viruses were

first isolated from these tick species.












Nests

Nests are defined as those habitats that have animals

which either periodically utilize the site to rear young or

use the nest for longer periods as a domicile, but in both

cases the site must be at the substrate surface or

arboreal. Some mammal domiciles meet this criteria, but

birds dominate this habitat type. There are four

subcategories: marine nests, ground or cliff nests,

arboreal nests and rodent nests.



Marine nests

Soft ticks that parasitize marine ground nesting birds

are usually in the Ornithodoros (A.) capensis group but one

Argas, A.(A.) macrostigmatus also parasitizes birds in this

habitat (Fillippova, 1966). Only the O.(A.) capensis group

species are virus infected (Hoogstraal, 1973b). However on

an inland saline lake in California where California gulls,

Larus californicus Lawrence, nest is an undescribed species

of tick near Argas (A.) cooleyi Kohls and Hoogstraal from

which Mono Lake virus was isolated (Berge, 1975;

Hoogstraal, 1985). Ornithodoros (A.) capensis, the

postulated progenitor of the group has a worldwide

distribution and parasitizes a variety of marine nesting

birds: gulls (Larus), cormorants (Phalacrocorax), penguins,

terns (Sterna), etc. (Kohls et al., 1965). It is known to












vector several viruses. Soldado virus in the "Hughes"

serogroup is a complex of strains found worldwide,

infecting three capensiss group" species: O.(A.) capensis,

O.(A.) maritimus Hoogstraal and O.(A.) denmarki Kohls,

Sonenshine and Clifford, Amblyomma loculosum Neumann and

numerous birds: terns, gulls and cormorants (Chastel et

al., 1983). Hughes virus, is restricted to the Caribbean

and was isolated in Trinidad from O.(A.) capensis and in

Florida from O.(A.) denmarki (Hughes et al., 1964) and

several other Caribbean locations. The Hughes group is

considered important to human health because of the risk of

contact between human and infected sea birds, especially in

the Mediterranean where Soldado virus caused a serious

resistant rhinitis in an ornithologist (Chastel et al.,

1981).

In the Pacific and off the Australian coast several

viruses have been isolated in O.(A.) capensis. Midway

virus infects O.(A.) capensis and O.(A.) denmarki in the

Pacific where antibodies are prevalent among black tailed

gulls, Larus crassirostris Vieillot (Takahashi et al.,

1982). Saumarez Reef virus was isolated from O.(A.)

capensis and Ixodes eudyptis Maskell parasitizing sooty

terns in Australia (St. George et al., 1977). In the

Quaranfil serogroup, Johnson Atoll virus is present from

Hawaii, Australia, New Zealand to the coast of Namibia












(Hoogstraal, 1985). The virus has been found in O.(A.)

capensis and O.(A.) denmarki and is known to affect terns,

gannets and cormorants (Austin, 1978; Hoogstraal, 1985).

In the Upolu serogroup, Upolu and Aransas Bay virus were

isolated from O.(A.) capensis upon the Great Barrier Reef

in Australia and the coast of Texas, respectively (Yunker

et al., 1979).

Besides Hughes virus, three other related viruses are

present in the New World (Clifford, 1979). Raza and

Farallon infest O.(A.) denmarki and O.(A.) sp. near

denmarki, respectively, in islands off California and

Mexico. Punta Salinas virus may cause human disease in

guano workers parasitized by O.(A.) amblus in Peru

(Clifford et al., 1980). Huacho (HUA) virus (Orbivirus)

also infects Ornithodoros (A.) amblus in Peru (Hoogstraal,

1985). In the Paleartic only two O.(A.) capensis group

species are found, O.(A.) maritimus and O.(A.) muesebecki.

Russian researchers have isolated West Nile virus in

several bird parasitizing argasids including O.(A.)

maritimus (Mirzueva et al., 1974). These ticks are

probably not involved in primary transmission. Another

Flavivirus species, Meaban virus was collected from O.(A.)

maritimus parasitizing gulls on offshore islands in France

(Chastel et al., 1985). Baku, an Orbivirus and Caspiy, a

Bunyavirus, from the USSR, were isolated from O.(A.)











coniceps and O.(A.) maritimus, parasitizing pigeon nests

and herring gulls, respectively (Berge, 1975; L'vov et al.,

1980).

Puffin Island virus was found in O.(A.) maritimus on

an island off the coast of Wales (Gould et al., 1983).

Zirga virus in O.(A.) muesebecki, a parasite of boobies,

cormorants, osprey and other marine birds in the Arabian

Gulf may be the causative agent of blisters, pruritus and

fever in people bitten by the tick (Hoogstraal and

Gallagher, 1982).

In reviewing the transmission of these viruses,

several similarities become evident. First the hosts of

these viruses and ticks are pelagic or range over wide

areas of seacoast so that the reported wide distribution of

these viruses and their vector ticks is easily explained.

The long feeding larvae may be transported long distances

(Hoogstraal, 1973a) thus serving as the ticks migration

mechanism.

Duffy (1983) studied the effects on seabirds of 0.(A.)

amblus and reviewed similar data of other researchers. He

stated that high tick population levels are reached after

four to ten years of continuous use of the site. Birds

deserting the area, perhaps with attached larvae, are more

likely to have encountered a virus infected tick and so the











rate of virus dissemination to other colonies is increased

(Hoogstraal, 1973b, 1985).

Spread of these viruses out of the marine bird and

tick colony niches is shown by Russian viral isolates found

in O.(A.) coniceps, a pigeon nest parasite. This spread

into the wider biocenosis of the virus can be explained

perhaps by the tendency of some seabird species to nest on

cliffs. Such coexistence can afford the ticks of each host

the opportunity to feed on the others' host. Infected

pigeons could then infect urban populations of pigeons and,

subsequently, their soft tick parasites which are known to

feed on man (Hoogstraal et al., 1979a; Siuda et al., 1979;

Hoogstraal, 1985).



Ground or cliff nests

Pigeons, swallows, martins, raptors and house sparrows

are the predominant hosts that utilize these cliff

habitats. Soft ticks that parasitize birds in these

habitats are predominantly in the subgenera: Argas (Argas)

and Ornithodoros (Proknekalia) but the species O.(A.)

coniceps, O.(A.) collocaliae Hoogstraal, Kadarsan, Kaiser

and Van Peenen and O.(A.) concanensis are also included.

Ticks in these habitats are found in cracks in the walls,

under debris or nests, or inside the mud nests of swallows.












Pigeons (Colomba livia Gmelin), a domesticated

species, are parasitized in both wild and domestic

situations with several Argas species but A.(A.) reflexus

(Fabricius) (Hoogstraal and Kohls, 1960a) and A.(A.)

hermanni Audouin (Hoogstraal and Kohls, 1960b) are the most

predominant.

In domestic pigeon houses two Uukuvirus species were

isolated (Berge, 1975). Isolates of these two have come

only from these domestic sources. Grand Arbaud (GA) virus

infects pigeons and their parasites, Argas (A.) reflexus,

in Camarque, France. Ponteves virus was also isolated from

Argas (A.) reflexus near the same location in France.

Grand Arbaud virus, has also been identified in A.(A.)

hermanni in Egypt (Hoogstraal, 1985).

There are a number of viruses that have been isolated

from tick parasites in this subcategory that are not

restricted to this habitat. These include the Flavivirus,

Royal Farm and West Nile isolated from A.(A.) hermanni and

O.(A.) coniceps (WN only) which also affects various

mammals including man and may be vectored by ixodids

(Hoogstraal, 1985; Darwish et al., 1983; Sidorova et al.,

1975; Schmidt and Said, 1964).

Baku virus and Caspiy virus isolates in O.(A.)

coniceps were discussed in the marine nest section.

Quaranfil virus was isolated in A.(A.) hermanni and A.(A.)












vulgaris Filippova and this virus will be discussed in the

section on heron rookery argasids.

In humans and other animals most argasid bites cause

local irritation, minor tissue damage and sometimes

pruritus (Lavoipierre and Rick, 1955). However a case was

reported of induced anaphylactic shock due to the allergic

response of a 59 year old Italian to the salivary toxins of

A.(A.) reflexus (Miadonna et al., 1982). The ticks

parasitized the pigeons that lived in the roof of her

house.

Several viruses or virus groups are known that seem to

be associated with either the habitat or the host type.

Chenuda virus infects Argas (A.) hermanni from Egyptian

pigeon houses and Ornithodoros (P.) peringueyi Bedford and

Hewitt from nests of the cliff swallow Petrochelidon

spilodera (Sundevall) in South Africa (Berge, 1975).

Serological evidence of Chenuda virus infection has been

shown for several mammals and the virus has been isolated

in Culex mosquitoes that probably fed on infected migrating

turtle doves (Hoogstraal, 1985). The role of these vectors

in the cyclic transmission is not understood. The Abu

Hammad subgroup (Nairovirus) consists of three viruses; Abu

Hammad (A.(A.) hermanni), Abu Mina (A.(P.) streptopelia

Hoogstraal, Kaiser and Kohls) and Pretoria (A.(A.)

africolumbae), all infecting doves and pigeons and their











argasid parasites from the Ethiopian region to Iran

(Darwish and Hoogstraal, 1981; Hoogstraal et al., 1975).

The host and tick vectors of Abu Mina virus are found in

arboreal nest habitats. The presence of seropositive

mammals to Abu Hammad and Abu Mina virus indicates a wider

range of virus reservoirs and vectors than is presently

known (Hoogstraal, 1985).

In the western United States there are two swallow

parasites: Argas (A.) cooleyi and O.(A.) concanensis.

Ornithodoros (A.) concanensis has a wider host range

including other birds, bats, mice and woodrats (Hopla and

Loya, 1983; Cook, 1972).

Rickettsia bellii is an agent found in Ixodidae

(Haemaphysalis and Dermacentor) and also in argasid bird

parasites, A.(A.) cooleyi and O.(A.) concanesis described

by Philip et al.(1983). There is no evidence that this

agent causes human illness.

All three viruses from this habitat were isolated from

Argas (A.) cooleyi: Sapphire II (Texas, Montana, New Mexico

and South Dakota) (Hoogstraal, 1973b, 1985), Sunday Canyon

(Texas) (Yunker et al., 1977) and Sixgun City (Texas,

Colorado, New Mexico and South Dakota) (Yunker et al.,

1972; Hoogstraal, 1985).











Arboreal nests

Arboreal nests are primarily the habitat of Argas

(Persicargas) species. Exceptions in the New World are

Argas (A.) dulus (Keirans et al., 1971), A.(A.) monachus

(Keirans et al., 1973), A.(A.) brevipes (Kohls et al.,

1961) and Ornithodoros (P.) macmillami Hoogstraal and Kohls

in Australia (Hoogstraal and Kohls, 1966a). None of these

exceptions is known to be involved in disease transmission.

Epidemiologically significant tick-infested arboreal nest

habitats can be divided into heron rookeries and vulture

nests. Domestic poultry houses and rearing situations are

also included in this category since most of the soft tick

parasites involved are A. Persicargas species.

In heron rookeries, the main species involved are

A.(P.) arboreus in Africa (Hoogstraal, 1985) and A.(P.)

robertsi Hoogstraal, Kaiser and Kohls in the Oriental and

Australian regions (Hoogstraal et al., 1975). In Florida,

A.(P.) radiatus Railliet was collected from mangrove trees

frequented by herons (Kohls et al., 1970).

Quaranfil virus is widely distributed in Africa and

the Middle East and is reviewed by Hoogstraal (1985). This

disease causes human infections but is largely a disease

infecting Argas ticks and the birds they parasitize. The

viral epidemiology in the tick A.(P.) arboreus has been

examined together with tick species specificity for virus












infectiveness (Kaiser, 1966b,c). The fact that most

mammals in affected areas carry positive antibody titers

(Darwish and Hoogstraal, 1981) implicates ixodid

involvement in the cycle. However, the exact interactions

are unclear.

Tyamanini (NYM) virus was isolated from a cattle egret

and it also infects the heron parasites; A.(P.) arboreus,

A.(A.) hermanni and A.(A.) robertsi and is distributed

across both Africa and the southern Paleartic region to

Thailand (Hoogstraal et al., 1975; Darwish and Hoogstraal,

1981). Nyamanini virus seasonal dynamics in A.(P.)

arboreus is known, with high infection rates in winter,

spring and summer, and lower rates in the fall (Kaiser,

1966b). The virus is known by antibody response to also

infect mammals (Berge, 1975).

The Kas Shuan (Nauovirus "Dera Ghazi Khan serogroup")

subgroup consists of Kao Shuan (KS) and Pathum Thani (PT)

infecting A.(P.) robertsi in Southeast Asia, Taiwan and

Australia (Khalil et al., 1980). The widely distributed

locations of virus illustrate how little is known about the

role of bird migration in virus dispersal as the infected

herons migrate back and forth between these areas.

Recently, Lake Clarendon virus (unclassified and

serologically ungrouped) was found in the cattle egret












parasite A.(P.) robertsi in Australia. Its maintenance in

the tick is not transovarial (St. George et al., 1984).

In West Pakistan, two viruses were isolated from the

vulture parasite Argas (P.) abussalami Hoogstraal and

McCarty: Manawa (Urkuvirus) and Bakau (Bunyaviridae ?)

(Berge, 1975; Hoogstraal, 1985). Manawa is from West

Pakistan where it was isolated from Argas abussalami a

vulture nest inhabitant. Subsequently, Manawa virus was

isolated from two Rhipicephalus species and high antibody

titers were detected in cattle, goats, humans, sheep,

quail, pigeons and sparrows, indicating a need to

reevaluate the natural history and importance of this agent

(Darwish et al., 1983; Hoogstraal, 1985). Bakau virus also

has a wide host range with isolates from Culex mosquitoes

and seropositive reactions in rodents and man (Darwish et

al., 1983). Argasid parasites of vultures exist worldwide

but no other viral isolates have been reported.

Many Argas (Persicargas) species were collected from

parasitized domestic chickens and other poultry. These

tick species can become significant problems. Although

virus transmission is not an apparent problem, these ticks

do vector diseases and can cause avian paralysis.

Aegyptianella pullorum Carpano is the monotypic member

of this piroplasm genus. It is the agent of aegyptianosis,

a non-contagious disease of birds, including domestic











chickens, ducks, geese and quail. The disease and its

epidemiology was reviewed by Gothe and Kreier (1977). The

disease appears to be restricted to a bird-Argas cycle in

temperate and tropical areas. Aegyptianella is found to

develop in the gut and salivary gland of all mobile tick

life stages, but transovarial transmission is rare.

Overlapping generations of Argas appear to be necessary for

the maintenance of the disease. Maintenance is also aided

by the fact that infected chicks are infective 18 months

later. The following are known to be involved in field

transmission to chickens and other fowl: A.(P.) persicus,

A.(P.) walkerae Kaiser and Hoogstraal, A.(P.) africolumbae,

and the American A.(P.) radiatus and A.(P.) sanchezi Duges.

In Argas species, Borrelia anserina (Sakharoff), the

causative agent of avian borreliosis, is found. The

disease is pathenogenic to all domestic fowl. The Old

World vectors are A.(P.) arboreus and A.(P.) persicus. The

spread of the latter worldwide has also spread this disease

(Hoogstraal et al., 1979b). In the Western Hemisphere, the

Persicargas subgenus members A.(P.) sanchezi and A.(P.)

miniatus Koch are implicated in transmission (Da Massa and

Adler, 1979; Santos, 1982).

Using four species of Argas present in Egypt; A.(P.)

persicus, A.(P.) arboreus, A.(P.) streptopelia and A.(A.)

hermanni, two experimental studies were undertaken to












examine spirochete localization (Diab and Soliman, 1977)

and transtadial and transovarial transmission (Zaher et

al., 1977). These are model studies in Borrelia/tick

transmission and specificity. They outline the variable

suitability of closely allied Ornithodoros species for this

Borrelia pathogen.

Avian paralysis induced by Argas infestation is not

uncommon and Gothe has reviewed the subject (Gothe, 1984;

Gothe et al., 1979). Avian paralysis is known to be caused

by A.(A.) reflexus, A.(A.) africolumbae, A.(P.) persicus,

A.(P.) walkerae, A.(P.) arboreus, A.(P.) radiatus, A.(P.)

miniatus and A.(P.) sanchezi. Pharmacological response of

the Argas toxins in relation to this problem was examined

in Gothe et al. (1979). The higher the parasite load, the

greater the extent and intensity of the paralysis. Older,

healthy and heavier birds are less likely to succumb

(Rosenstein, 1976) but no immunity is produced (Gothe,

1984).

Host immunity to argasid ticks is at best partial.

Trager (1940) showed that chickens repeatedly fed upon by

Argas persicus nymphs and adults developed no protective

immunity. However, when the chickens were exposed to the

longer feeding process of the larvae, they developed a

partial immunity. In feeding A.(P.) arboreus larvae on

wild (presumably pre-exposed) cattle egrets, the












engorgement period was longer when compared to naive birds

(Hafez et al., 1971). Additionally, the age dependent

immunity (susceptable naive chick versus older egrets) of

the host is important in the transmission of Quaranfil

virus by affecting the ability of the previously tick

infested bird to minimize or prevent the agent to cause

disease upon reexposure (Kaiser, 1966c; Hoogstraal, 1985).

Argasid ticks in mammal nests constructed above

ground are primarily restricted to the Neartic. Some have

become health hazards to man because of this host

association. In Mexico, O.(P.) nicollei Mooser normally

parasitizes woodrats, Neotoma, and ground squirrels,

Citellus, but it also infests caves and rural homes

(Hoffman, 1962; Kohls et al., 1965). Ornithodoros sparnus

Kohls and Clifford in the western United States parasitizes

Peromyscus and Neotoma (Kohls and Clifford, 1963). The

biology of these two species is virtually unknown.

Ornithodoros (P.) hermsi is another western United

States species, but it is found normally at high altitudes.

It parasitizes small rodents such as chipmunks (Eutamias),

woodrats (Neotoma) and pine squirrels (Tamiasciurus) that

nest in hollow logs, stumps or cabins (Davis, 1939; Cooley

and Kohls, 1944). Ornithodoros (A.) talaje (= 0. dugesi ?)

parasitizes a wide variety of mammals, birds and man, and












is found in houses, woodrat nests, and burrows (Cooley and

Kohls, 1944; Kohls et al., 1965).

Ornithodoros (P.) hermsi, not being a burrow parasite

but a nest parasite of small mammals, has ample opportunity

to encounter man because it parasitizes rodents that den in

cabins and "lean-to's" (Cooley and Kohls, 1944; Harwood and

James, 1979). Burgdorfer (1980) demonstrated how human

activity near infected nidi provides an opportunity for

transmission. The statistics showed that of 280 cases of

relapsing fever (1954-1978), 250 were attributed to B.

hermsi Davis and 30 were B.turicatae. In Mexico and

Guatemala O.(A.) talaje transmits a Borrelia, known by the

name Borrelia mazzottii Davis, to man. However,

distinctiveness of the strain is questionable (Felsenfeld,

1971).



Free Living Hosts

Only five species can be considered free living:

Ornithodoros (0.) savignyi, O.(0.) coriaceus, O.(P.)

gurneyi, Otobius lagenophilus and 0. megnini. These

species although restricted to dry, desert-like habitats,

have evolved behavioral and physiological mechanisms that

make them independent of the need for physical shelters.

Three additional species could also be included but,

because of their frequent collection in sheltered












situations, they are not. They are Argas (A.) cucumerinus,

A.(O.) brumpti and Ornithodoros (A.) lahorensis.

The sand tampan, 0.(0.) savignyi, posesses eyes, a
trait shared only with one other Ornithodoros species: 0.

(Ornamentum) coriaceus. Hoogstraal (1956) reviewed the

biology of the species. It is found throughout Africa, the

Middle East and India. Its distribution is strongly

correlated with those areas that use dromedary camels. It

is found in shaded areas where animals are tethered or at

rest. It is not usually found indoors. It normally rests

under the sand surface from which it emerges to feed at

night. It is not normally associated with any disease but

can maintain Borrelia crocidurae (Leger) (Gaber et al.,

1984) and transmit ASFV experimentally (Mellor and

Wilkinson, 1985). Ornithodoros (0.) savignyi, with its

wide host range, including pigs, and its presence in ASFV

endemic areas, suggests it may be a natural field vector of

this disease (Mellor and Wilkinson, 1985).

Ornithodoros (0.) coriaceus, originally a deer

parasite in California, has long been associated with the

cattle disease, epizootic bovine abortion. A number of

viral agents and a clamydial agent have been isolated from

the tick but were not responsible for the disease (Storz et

al., 1960; McKercher et al., 1969, 1973, 1980; Wada et al.,

1976; Schmidtmann et al., 1976).












Finally, a spirochete was isolated that is transmitted

by bite or via coxal fluid but does not cause infections in

mice or rabbits and can only be detected in the tick or

cultures of tick tissues (Lane et al., 1985). Osebold et

al. (1986) demonstrated that the spirochete discovered by

Lane and his colleagues is the cause of the disorder.

Additionally, in northern California, O.(0.) coriaceus

transmitted a mild strain of C. burneti (Enright et al.,

1971).

In Australia, the kangaroo tick, Ornithodoros (P.)

gurney, is a parasite of crepuscular macropods, especially

the red kangaroo, Macropus rufus (Desmarest). The ticks

are found in loose soil in kangaroo wallows in open

savannahs. Doube (1975a,b) examined its biology in the

laboratory. The larvae, unlike other Pavlovskyella, remain

attached for four to six days and nymphal instars one, two

and three also remain attached for several days. The

species also undergoes a reproductive diapause when exposed

to low (10-150C) or high (400C) temperatures or short

photoperiods. No diseases are known to be associated with

this tick and it is not a livestock pest.

The genus Otobius, with its specialized life cycle, is

the most highly evolved Argasid genus toward a free living

life style. There exist few diseases associated with these

ticks beside the fact 0. megnini has become a problem in












cattle worldwide where it may occlude the ear canal and

cause severe irritation and discomfort. Cases of human

parasitism have also been reported and even a case of human

paralysis due to the presence of a nymphal Otobius megnini

in the ear of a South African child (Peacock, 1958).

Colorado tick fever virus was isolated from Otobius

lagophilus parasitizing infected rabbits in Nevada and Utah

(Berge, 1975; Hoogstraal, 1985). This disease is primarily

associated with Dermacentor andersoni Stiles and the impact

of this argasid/virus cycle on the epidemiology of this

disease is unclear. Also unclear is the importance of this

tick in the transmission cycle of Rocky Mountain spotted

fever.



Interactions of Argasid Ticks with the Wider Enviromnent

As can be seen in the previous section, argasid ticks

are found in a wide variety of habitats, parasitizing a

variety of animals and can transmit many disease causing

agents. The conventional wisdom is that argasid ticks

cause problems only in small localized areas and their

impact to man is only minimal. This belittling attitude is

true in most cases, but not all. The potential problems

that these ticks could cause has been demonstrated in a few

cases only, but they show the fallacy of classifing the

Argasidae as esoteric, unimportant pests.












In some cases, man's activities have generated the

opportunity for argasid tick transmission or the expansion

of a minor zoonotic argasid into the sphere of man's

activities where it has become a pest. Examples of

zoonotic disease transmission impacting on man include

epizootic bovine abortion in cattle exposed to the deer

parasite, 0.(0.) coriaceus, or relapsing fever transmission

by O.(P.) hermsi in mountain cabins (Schmidtmann et al.,

1976; Harwood and James, 1979). Man's activities are no

doubt responsible for the spread of the pests: Otobius

megnini, Argas (P.) persicus and Ornithodoros (A.)

lahorensis. Man's activities have also provided habitats

for some of the more adaptable parasites which then became

pests. Examples include Ornithodoros (P.) marocanus and

O.(0.) moubata in pigsties (Hoogstraal, 1985), the chicken

coop parasitizing Argas (Persicargas) spp. and O.(P.) rudis

and O.(A.) boliviensis into Latin American houses (Cooley

and Kohls, 1944).

Global transport of diseases is a significant problem

and is accomplished both by man and by ticks themselves.

Three argasid vectored diseases transported internationally

by man are African swine fever, aegyptianosis and avian

borreliosis (Hoogstraal, 1985). The international

transport of argasid tick diseases by ticks themselves was

recognized by Hoogstraal (1961) with migrating birds that












carried ticks. Pelagic bird migration is no doubt

responsible for the distribution of the Ornithodoros

capensis species group and the viruses in the Hughes

serogroup. Bird migrations and colonization, such as that

of the cattle egret, Bulbucus ibis (L.), from Africa to the

Americas, if involving infected birds could expose local

argasids to a foreign virus like Qaranfil.

Man's recent broad scale exportation of exotic fauna

to other continents, whether legally or illegally, could

introduce foreign argasid ticks. The potential for this

problem is well demonstrated by the international movement

of domestic animals and its subsequent effect.

As has been shown, soft ticks provide a suitable

environment for the culture and vectorship of a wide

variety of pathogens. Therefore, new pathogens introduced

into its nidus have the possibility of survival and future

transmission. Additionally, the long life of argasids

could provide a maintenance reservoir for a pathogen. When

the tick vectors the pathogen it may then spread widely via

more mobile vectors such as mosquitoes. Examples of this

system are the Qaranfil virus and West Nile virus in Egypt

(Hoogstraal, 1985). Another opportunity for disease

interaction between argasid species and nidi can occur

where they are adjacent geographically. This allows an

animal, infected by the bite of one tick, to be fed upon by









87

another species of tick for which it is an abnormal host--

thus infecting both tick species. An example of this is

Caspiy virus found in both O.(A.) coniceps and O.(A.)

maritimus (L'vov et al., 1980).

Any or all of these epidemiological factors could

interact to generate a new epidemiological problem that

would showcase soft ticks as significant vectors--just as

African swine fever has done recently in Spain and

Portugal. That experience should serve as a warning for

disease epidemiologists and entomologists to not forget the

vector potential of members of the family Argasidae.




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