Tick and mammal coevolution, with emphasis on Haemaphysalis


Hoogstraal, H.; Kim, K.C.

Coevolution of parasitic arthropods and mammals: 505-568

1985


The ticks of the superfamily Ixodoidea are postulated to have evolved as obligate parasites of Reptilia in the warm, humid climate of the late Paleozoic or early Mesozoic era. During this period, their basic physiological patterns were established, as was the multihost developmental pattern of the Argasidae and the three-host developmental pattern of the Ixodidae.

Chapter
10
Ornithodoros
(Ornithodoros
savignyi
(Audouin)
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
Harry
Hoogstraal
and
Ke
Chung
Kim
Introduction
506
Premammalian
Evolution
of
Ticks
508
Evolution
of
Mammalian
Ticks
510
Host
Specificity
516
Haemaphysaline
Ticks
519
Structurally
Primitive
(SP)
Haemaphysalines
520
Subgenus
Alloceraea
Schulz
521
Subgenus
Allophysalis
Hoogstraal
527
Subgenus
Aboimisalis
Santos
Dias
532
Subgenus
Shari
fiella
Santos
Dias
538
Haemaphysalis
and
Tenrecs
(Malagasy
Insectivores)
538
Structurally
Intermediate
(SI)
Haemaphysalines
540
Subgenus
Herpetobia
Canestrini
540
Structurally
Advanced
(SA)
Haemaphysalines
546
Subgenus
Ornithophysalis
Hoogstraal
and
Wassef
547
Subgenus
Haemaphysalis
Koch
549
Subgenus
Gonixodes
Duges
551
Subgenus
Kaiseriana
Santos
Dias
552
Subgenus
Garnhamphysalis
Hoogstraal
and
Wassef
555
Subgenus
Aborphysalis
Hoogstraal,
Dhanda,
and
El
Kammah
555
From
Research
Project
3M161102BS10.AD.424,
Naval
Medical
Research
and
Development
Command,
National
Naval
Medical
Center,
Bethesda,
Maryland.
The
opinions
and
assertions
contained
herein
are
the
private
ones
of
the
authors
and
are
not
to
be
construed
as
official
or
as
reflecting
the
views
of
the
Department
of
the
Navy
or
of
the
naval
service
at
large.
(Request
reprints
from
Medical
Zoology
Department,
NAMRU-3,
FPO,
New
York
09527.)
505
506
Acari
Subgenus
Segalia
Santos
Dias
556
Subgenus
Dermaphysalis
Hoogstraal,
Uilenberg,
and
Klein
558
Subgenus
Rhipistoma
Koch
558
Summary
563
References
565
INTRODUCTION
The
generally
large
acarines
constituting
the
tick
superfamily
Ixodoidea
apparently
evolved
as
obligate
parasites
of
Reptilia
in
the
late
Paleozoic
or
early
Mesozoic
era.
During
subsequent
coevolution
with
birds
and
mam-
mals,
adaptations
of
most
tick
species
have
been
conservative.
Structural,
developmental,
physiological,
ethological,
and
reproductive
properties
and
processes
have
changed,
but
chiefly
within
narrow
parameters.
More
radical
adaptations
characterize
a
small
proportion
of
the
world's
mammal-
parasitizing
species.
Most
species
that
have
burst
their
conservative
evolu-
tionary
shackles
are
ixodids
and
parasitize
livestock,
some
also
feed
on
man
and
dogs.
These
species
have
been
more
intensely
investigated
than
others;
however,
they
are
not
entirely
typical
of
their
families.
The
other
species
that
have
adapted
radically,
argasid
parasites
of
New
World
bats,
are
virtually
unknown
biologically.
About
800
tick
species
are
divided
into
three
families,
10
subfamilies,
and
19
genera
(Fig.
10.1).
Most
Argasidae
("soft
ticks")
retain
basic
biolog-
ical
patterns
developed
during
their
early
history
as
reptile
parasites.
How-
ever,
few
argasids
now
parasitize
reptiles
(Hoogstraal
and
Aeschlimann
1982).
Argasid
biological
adaptations
involve
chiefly
resistance
to
dessica-
tion,
host
and
microhabitat
specificity,
diapause,
and
longevity.
Argasid
life
cycle
adaptations
occur
in
a
few
species
of
Ornithodoros
and
in
the
11
species
of
the
specialized
subfamilies
Otobinae,
Antricolinae,
and
Notho-
aspinae
(Hoogstraal
1985).
In
Ixodidae,
the
genus
Ixodes
(Prostriata,
Ixodinae,
about
217
species,
worldwide)
represents
typical
"hard
ticks"
with
secondary
biological
and
structural
specializations,
some
of
which
probably
developed
during
the
Tertiary
period.
All
other
ixodid
genera
are
in
the
Metastriata
line.
The
tropical-subtropical
Aponomma
and
Amblyomma
(Amblyomminae,
about
126
species)
retain
primitive
structural
characters.
All
but
two
of
the
24
Aponomma
species
and
37
of
the
102
Amblyomma
species
are
reptile
para-
sites
(Hoogstraal
and
Aeschlimann
1982).
There
appears
to
be
a
close
affinity
between
the
Amblyomma
faunas
of
Australia
and
South
America.
Only
17
species
of
the
tropical-temperate
Haemaphysalis
(Haemaphysalinae
,
156
species)
retain
"primitive"
structural
characters,
and
a
few
of
these
17
species
are
known
to
be
exceptional
biologically.
During
the
Tertiary
pe-
riod,
numerous
Haemaphysalis
species
coevolved
with
birds
and
mammals
throughout
much
of
the
world
(however,
only
five
species
occur
in
New
Margaropus
(3
spp.)
Hyalornma
I
30
spp.)
Nothoaspis
lisp.)
0
tobi
vs
(
2
spp.I
Boophilus
(
5
spp.1
Hyalomminae
Nothoaspinae
Antricola
18
spP.I
Otobina•
Rhipicontor
(
2spp.)
Antricolina•
Anomalohimalaya
I
3
spp.)
Rhipicephalus
(
70
spp.
)
Nosomma
(1
sp.
Cosmiomma
(
lsp.)
Amblyomma
(
102
sals.
,
Dermacentor
(
30
spp.1
Aponomma
(24
spp.)
Ornithodoros
±100
spp.
,
Rhipicephalinae
Amblyomminae
Ornithodorina•
',codes
217
spp.)
I
xodina•
M
ErAsrR
/4
)..4
FAMILY
NUTTALLIELLIDAE
Nuns:1111011a
/
PROSTRIATA
FAMILY
ARGASIDAE
FAMILY
IXODIDA
(
±167
spp.
)
±
643
spp.
)
October
1982
SUPERFAMILY
IXODOIDEA
SUBORDER
METASTIGMATA
ORDER
ACARINA
Figure
10.1
Dendrogram
showing
phylogenetic
relationships
of
Ixodoidea.
The
number
of
species
is
given
in
parenthesis
for
each
genus.
Haemap
hysalis
(155
spp.)
Haemaphysalinae
Argos
156spp.l
Argasinae
508
Acari
World).
The
distinctive
host-related
structural
adaptations
of
Haemaphysalis
ticks
are
discussed
in
detail
hereinafter.
The
Hyalomminae
(genus
Hyalomma,
30
species,
in
the
Palearctic,
Ethio-
pian,
and
Oriental
regions)
retain
the
primitive
long
palpi
of
the
early
reptile
parasites
and
have
a
limited
variety
of
hair-hooking
spurs.
One
species,
H.
(Hyalommasta)
aegyptium
(Linn.),
is
entirely
dependent
on
the
tortoise,
Testudo,
for
population
survival,
but
immatures
also
parasitize
birds
and
small
mammals.
Immatures
of
the
subgenus
Hyalomma
often
parasitize
reptiles
and
birds
but
smaller-sized
mammals
are
the
chief
hosts
of
most
species
in
this
subgenus.
Adults
parasitize
chiefly
Artiodactyla.
The
subgenus
Hyalomma
is
highly
adapted
to
arid
and
semiarid
biotypes
and
to
steppes
and
savannas with
long
dry
seasons.
Immatures
of
the
subgenus
Hyalommina
infest
chiefly
rodents;
adults
parasitize
artiodactyls;
one
is
specific
for
the
Indian
porcupine.
The
Rhipicephalinae
(114
species,
eight
genera,
all
in
the
Palearctic,
Oriental,
and
Ethiopian
regions,
except
a
few
Dermacentor
species
in
the
Nearctic
and
Neotropical)
virtually
never
(in
terms
of
population
survival)
feed
on
reptiles
or
birds.
Rhipicephalinae
have
evolved
the
most
recently
of
all
tick
groups
and
are
parasitic
on
mammals
and
tropical
in
distribution
(except
for
several
Holarctic
Dermacentor
species).
Life
cycle
adaptations
for
parasitizing
wandering,
large
mammals
are
notable
in
two-host
Rhipicephalus
species
and
in
Boophilus
and
Margaropus;
all
species
in
the
two
last-named
genera
have
a
one-host
life
cycle.
In
this
chapter
we
present
data
for
the
host
relationships
of
immatures
and
adults
of
Haemaphysalis
species,
the
tick
group
most
indicative
of
coevolution
between
ticks
and
mammals,
together
with
analyses
of
body
and
appendage
structures,
and
of
life-cycle,
biological,
and
distribution
patterns,
which
furnish
clues
to
the
coevolution
of
these
parasites
and
their
hosts.
PREMAMMALIAN
EVOLUTION
OF
TICKS
Ixodoidea
are
postulated
to
have
evolved
as
obligate
parasites
of
Reptilia
in
the
warm,
humid
climate
of
the
late
Paleozoic
or
early
Mesozoic
era
(Hoogstraal
1978).
Large,
glabrous
reptiles
living
near
each
other
were
easily
available
hosts
for
ancestral
ticks
throughout
the
year.
The
ticks
had
four
developmental
stages,
as
they
still
do:
egg,
larva,
nymph,
and
adult.
Each
postembryonic
instar
imbibed
an
enormous
amount
of
blood
or
tissue
material,
emitted
excess
water
with
coxal
fluids
(Argasidae),
or
salivary
fluids
(Ixodidae),
and
digested
the
remainder
by
relatively
sluggish
physio-
logical
processes.
There
was
no
differentiated
eye
on
the
body
surface.
Questing
for
reptile
hosts
in
early
environments
was
uncomplicated;
movement
toward
a
suitable
feeding
site
on
the
glabrous
host
was
unim-
peded
by
hairs
or
feathers.
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
509
Paleozoic-Mesozoic
Reptilia
radiated
into
numerous
bizarre
forms
filling
a
variety
of
aquatic
and
terrestrial
niches.
Their
more
conservative
tick
parasites
evolved
along
only
two
main
lines
(Fig.
10.1).
The
argasid
line
was
represented
by
the
genera
Argas
and
Ornithodoros,
partially
as
we
know
them
today,
and
undoubtedly
also
by
other
genera
that
are
now
extinct.
Other
contemporary
genera
of
the
argasid
line
probably
did
not
evolve
until
the
Tertiary
period.
(No
truly
fossil
ticks
have
been
discov-
ered.)
The
ixodid
line
was
represented
by
primitive
members
of
the
branches
that
we
now
know
as
the
genera
Ixodes,
Aponomma,
Amblyomma,
and
Haemaphysalis.
Hyalomma
may
have
appeared
later,
close
to
the
Cretaceous
period
of
Mesozoic
environmental
stresses,
when
the
Mesozoic
reptile
diversity
was
reduced
to
the
Rhynchosauria
and
ancestors
of
mod-
ern
birds
and
mammals.
The
Rhipicephalinae
(Dermacentor,
Rhipicephalus,
Boophilus,
and
related
genera)
(Fig.
10.1)
did
not
appear
until
the
Tertiary
period,
when
mammals
and
birds
replaced
reptiles
as
the
dominant
verte-
brates.
The
few
ixodid
species
(all
in
the
subfamilies
Hyalomminae
or
Rhipicephalinae)
utilizing
only
one
or
two
hosts
in
their
life
cycles
did
not
evolve
until
after
mammals
appeared.
Early
ixodid
ticks
were
probably
as
large
as
the
largest
extant
Ambly-
omma
(females
10-12
mm
long,
males
about
a
millimeter
shorter,
larvae
about
1
mm
long).
A
single
bloodmeal
for
each
postembryonic
stage
fur-
nished
food
for
ixodid
larvae
to
change
into
nymphs,
for
nymphs
to
be-
come
adults,
and
for
adults
to
mature
and
reproduce.
Excessive
quantities
of
host
blood
or
tissue
were
required
to
meet
these
energy
demands.
Females
took
especially
large
meals
in
producing
a
single
egg
batch
before
dying
and
for
eggs
to
develop
and
hatch
into
larvae
capable
of
seeking
their
own
food.
Male
ixodids
needed
less
food
to
support
reproductive
processes
and
maintain
life
even
while
mating
with
one
or
more
females.
The
early
ixodid
egg
batch
may
have
contained
few
eggs,
each
relatively
large.
The
clue
for
this
conjecture
is
furnished
by
the
structurally
primitive
relict
Haemaphysalis
(Alloceraea)
inermis
Birula,
which
produces
a
batch
of
only
200
large
eggs.
Argasids
associated
with
Paleozoic-Mesozoic
reptiles
were
probably
30-
50%
longer
and
broader
than
ixodids;
their
body
volume
distinctly
ex-
ceeded
that
of
ixodids.
Three
bloodmeals
were
insufficient
to
meet
the
energy
requirements
of
these
large
ticks.
Thus
argasid
nymphs
underwent
two
or
more
instars,
each
with
a
separate
bloodmeal
on
a
separate
host,
rather
than
only
one
instar
and
one
meal
as
in
smaller
ixodid
nymphs.
The
large
adult
argasids
took
several
bloodmeals,
and
the
females
oviposited
after
each
full
meal,
thus
differing
distinctly
from
adult
ixodids.
Primitive
argasid
and
ixodid
larvae
could
indulge
in
a
leisurely
feeding
period.
Their
small
size
and
concealed
feeding
sites
in
reptile
skin
folds
sheltered
them
from
being
scraped
off
the
active
host.
Early
nymphs
and
adults
probably
also
fed
slowly
for
several
days,
but
they
fared
badly.
Few
large
nymphs
and
even
fewer
larger
females
could
escape
dislodgement
510
Acari
while
hanging
from
the
host
for
several
days
like
gradually
enlarging
beans.
Accordingly,
natural
selection
at
an
early
stage
of
the
tick
evolution..
ary
history
resulted
in
unique
adjustments
in
the
length
of
their
feeding
periods.
Small
argasid
larvae
mostly
continued
to
feed
for
several
days,
but
larger
nymphs
and
adults
survived
by
feeding
rapidly,
in
30-60
minutes.
Ixodid
larvae,
nymphs,
and
adults
(females),
on
the
other
hand,
fed
slowly
and
gradually
for
several
days.
They
reached
their
final
large
balloon
shape
only
during
the
last
6-12
hours
before
disengaging
from
the
host.
Male
ixodids
also
fed
slowly
(if
at
all)
but
took
a
smaller
meal.
EVOLUTION
OF
MAMMALIAN
TICKS
In
the
early
Tertiary
or
the
late
Cretaceous
period,
some
70
million
years
ago,
primitive
bird
and
mammal
lines
exploded
into
numerous
specialized
orders
replacing
reptiles
as
the
dominant
terrestrial
vertebrates.
The
new
vertebrates
filled
more
ecological
niches
and
developed
a
greater
variety
of
life-styles
than
did
early
reptiles.
Most
mammals
and
birds
were
much
smaller
than
the
majority
of
the
early
reptiles
they
replaced.
Many
Mesozoic
ticks
were
probably
unable
to
adapt
to
the
new
hosts
and
per-
ished.
Adaptive
radiation
in
surviving
tick
lines
paralleled
that
of
the
new
vertebrates,
but
at
a
slower
and
more
conservative
tempo
and
rate.
Distinct
preferences
for
certain
types
of
hosts
among
the
biologically
and
ecologi-
cally
disparate
vertebrates
developed
in
existing
tick
lines
(genera
and
species
groups).
Existing
lines
diversified
and
new
generic
groups
(Rhipicephalinae)
evolved.
As
tick
body
size
decreased,
certain
structures,
biological
properties,
and
behavior
patterns
were
modified.
There
were
few
modifications
in
rates
of
physiological
processes;
some
were
more
speedy,
but
most
were
even
more
sluggish
than
before.
Different
feeding
patterns
evolved
in
the
various
groups
of
Argasidae
and
Ixodidae.
After
the
Pleistocene
epoch,
when
man
introduced
domestic
animal
herds
into
the
environment,
these
few
species
and
species
groups,
in
both
families,
were
to
achieve
great
veterinary
and
medical
importance.
Most
argasid
species
have
remained
sheltered
in
burrows
or
niches
close
to
colonies,
nests,
roosts,
dens,
or
caves
frequently
or
seasonally
revisited
by
birds
or
mammals.
Thus,
protected
by
microhabitats
as
well
as
by
lim-
ited
exposure
time
during
feeding,
and
assured
periodically
of
ample
food
from
resting
immature
or
adult
birds
or
mammals,
some
large
argasids
have
survived
in
association
with
large
hosts
such
as
porcupines,
wart-
hogs,
wild
pigs,
and
hyenas.
Smaller
argasids
evolved
together
with
small
vertebrates
such
as
martins,
pigeons,
tenrecs,
rodents,
and
bats.
Notably,
the
larvae,
nymphs,
and
adults
of
each
argasid
species
inhabiting
a
shel-
tered
microhabitat
feed
on
the
same
kind
of
host—the
only
one
generally
available
in
these
situations.
Hungry
argasids
may
feed
on
exceptional
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
511
hosts
venturing
into
their
habitat;
some
argasids
survive
on
the
atypical
meal,
but
afterward
most
develop
poorly
if
at
all.
The
Ixodidae
have
better
adapted
biologically
and
ecologically
than
the
Argasidae
to
hazards
associated
with
complete
dependence
on
highly
mobile
birds
and
mammals
in
diverse
habitats.
For
many
reasons,
size
reduction
was
paramount
to
success.
This
reduction,
in
some
cases,
ap-
pears
to
be
clearly
related
to
the
small
size
of
the
preferred
host
group.
In
other
cases,
the
size
reduction
apparently
results
from
a
dominating
evolu-
tionary
trend
regardless
of
host
size,
as
exemplified
by
the
small
Haemaphy-
salis,
Boophilus,
and
Margaropus
on
characteristic
hosts
such
as
deer,
an-
telopes,
wild
cattle,
giraffes,
and
zebras.
The
early
Aponomma
or
Aponomma-like
reptile-parasitizing
ixodid
was
about
10
mm
long
with
narrowly
elongate,
four-segmented
palpi
(Figs.
10.2,
10.3).
The
palpal
segment
4
was
separated
from
3
by
a
suture
and
was
situated
apically,
as
in
argasids.
In
contemporary
Aponomma,
the
segment
4
(with
its
cluster
of
apical
sensory
setae)
remains
distinct
and
apical.
How-
ever,
the
Aponomma
species
parasitizing
modern
reptiles,
which
are
much
smaller
and
less
diverse
than
Mesozoic
reptiles,
have
become
small-
or
medium-sized
ticks.
An
early
step
in
ixodid
body
size
reduction
associated
with
birds
and
mammals
occurred
when
the
palpal
segment
4
became
a
diminutive,
ventrally
directed
appendage
relocated
in
a
protective
pit
of
segment
3
(but
retaining
a
cluster
of
sensory
setae).
This
pit
is
apical
in
H.
(Alloceraea)
vietnamensis
Hoogstraal
and
Wilson,
the
largest,
most
primitive
species
of
the
155-member
genus
Haemaphysalis
(Hoogstraal
and
Wilson
1966)
(Fig.
10.4),
but
in
more
than
600
other
ixodid
species,
this
pit
is
ventral
and
subapical.
Today,
adults
of
only
Aponomma,
Amblyomma,
Hyalomma,
some
Ixodes,
and
a
very
few
primitive
Haemaphysalis
have
narrowly
elongate
palpi
(Fig.
10.5).
Elongate
palpi
persist
in
certain
immature
Ixodes
and
Haemaphysalis
whose
adult
palpi
have
become
short
and
compact.
Evolutionary
changes
in
structure
have
been
slower
and
more
conservative
in
immature
than
in
adult
ticks.
Elongate
palpi
of
immatures
furnish
clues
to
the
early
history
of
Ixodidae
and
to
relationships
between
Ixodidae
and
Argasidae.
As
new
generic
taxa,
such
as
Dermacentor,
Rhipicephalus,
Anomalo-
himalaya,
Boophilus,
and
other
genera
of
Rhipicephalinae
evolved
together
with
mammals,
adult
palpi
became
short
and
compact
(Fig.
10.4).
Imma-
ture-stage
palpi
of
Dermacentor
and
of
some
other
rhipicephaline
species
remained
elongate.
The
typical
ixodid
three-host
cycle
(Fig.
10.6)
became
modified
to
a
two-
host
or
a
one-host
cycle
in
certain
species
of
Hyalomma
and
Rhipicephalinae
that
inhabited
environments
where
wandering
mammal
numbers
were
few,
home
ranges
were
extensive,
or
dry
seasons
were
long
and
hot.
The
one-host
cycle
developed
in
response
to
the
movements
of
widely
wander-
ing
medium-
or
large-sized,
forest-
or
steppe-inhabiting
mammals
or
to
2
I
0
r
I.
I
r
••
1
1f
,
A
r
c,
r
C
D
Figure
10.2
Adult
Aponomma
varanensis
(Taiwan),
a
"Mesozoic-type"
reptile
parasite.
(A,
B)
male;
(C,
D)
female;
dorsal
and
ventral
views.
Figure
10.3
Adult
Aponomma
varenensis.
(A-H)
Male:
(A,
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome,
ventral
view;
(D)
genital
area;
(E)
spiracular
plate
(A,
anterior;
D,
dorsal);
(F)
coxae
and
trochanters
Ito
IV;
(G)
femur
IV,
internal
view;
(H)
tarsi
I
to
IV,
external
view.
(I-P)
Female:
(I,
I)
capitulum,
dorsal
and
ventral
views;
(K)
hypostome;
(L)
genital
area;
(M)
spiracular
plates;
(N)
coxae
and
trochanters
I
to
IV;
(0)
femur
IV;
(P)
tarsi
I
to
IV.
512
\it
I
I
K
2
0
1
r
A
-
NO
III
IV
H
G
F
/
li
1'
IV
J
0
M
513
r
.
•,
."
Ai
,
°
. .
A
B
a
il
•••••.)
J
jJ
p
ti
//i
0
III
0
LT
,
Figure
10.4
Female
Haemaphysalis
(Alloceraea)
vietnamensis,
structurally
probably
the
most
primitive
member
of
the
genus.
(A,
B)
Dorsal
and
ventral
views;
(C,
D)
capitulum,
dorsal,
and
ventral
views;
(E)
hypostome,
ventral
view;
(F)
genital
area;
(G)
spiracular
plate
(A,
anterior;
D,
dorsal);
(H)
coxae
and
trochanters
I
to
IV;
(I)
femur
IV,
internal
view;
(J)
tarsi
I
to
IV,
external
view.
514
Larva
Nymph
Adult
AMEILYOMMA
I
l
HYALOMMA
HAEMAPHYSALIS
Nymph
Male
Female
H.
INERMIS
H
PUNC
TA TA
4
44
"
EMIIMACENTOR
H
AT
HERURUS
1
H
.
ERINACEI
RHIPICEPHAL
US
I
SOOPHILUS
H.LEACHII
Figure
10.5
The
capitulum
(dorsal
view)
of
immature
and
adult
Amblyomma,
Hyalomma,
Dermacentor,
Rhipicephalus,
and
Boophilus
ticks
(there
is
little
sexual
dimorphism
of
the
capitulum
in
these
genera),
and
of
immature
and
adult
Haemaphysalis
of
structurally
primitive
(SP)
groups
[H.
(Alloceraea)
inermis,
H.
(Aboimisalis)
punctata]
and
structurally
advanced
(SA)
groups
[H.
(Aborphysalis)
atherurus,
H.
(Rhipistoma)
erinacei,
H.
(R.)
leachi].
516
Acari
STAGE
Multihost
3-host
2-
hos
t
I
1-
hos
t
EGG
Several
batches
on
ground
Single
batch
on
ground
LARVA
r
host
1
I
t_
molt/ground
vs../WV
r
host
2
/
'
L.
molt/ground
r
host
3
,<'
L
.".^..".".^.
molt/ground
\/
r
host
4
<
1
L
W.
,
\/\
molt/ground
\"/\./\"/
r
host
5
<'
t
t_
r
host
6
<'
1
k.
r
host
7
+
<
1
L
host
1
‹'
molt
/
s.."/"..W/
host
2
<
I
WW
,"
molt
/ground
host
3
<
I
r
i_
ground
r
I
k.
r
..
s....e..v.."././
host
1
<
I
".."...".."."."
molt
/
host
2
<
I
I
r
molt
'host
1_
ground
r
L
host
1
i
r
molt/host
molt/host
I
I
L
NYMPH
ADULT
FAMILIES
Argasids
I
xod
ids
+
160
spp.
-
+
630
spp.
10
spp.
10
spp.
Figure
10.6
Tick
life-cycle
patterns.
feeding
during
winter,
when
small
mammals
moving
under
snow
are
un-
available
to
immature
ticks
of
species
that
do
not
inhabit
burrows
(Hoog-
straal
1978).
In
effect,
winter
activity
is
a
substitute
for
diapause,
which
is
an
exceptionally
common
phenomenon
in
ticks.
HOST
SPECIFICITY
The
Ixodoidea
show
a
high
degree
of
strict
host
specificity,
which
is
one
of
the
important
biological
factors
determining
the
ecological
and
geographi-
cal
distribution
and
population
densities
of
most
ticks.
However,
the
pat-
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
517
tern
of
limited
host
specificity
may
be
altered
when
physiologically
accept-
able
domestic
or
feral
mammals
intrude
into
the
primary
host—parasite
associations.
This
secondary
host—parasite
relationship
often
becomes
so
prevalent
that
it
frequently
obscures
the
pattern
of
host
specificity
and
leads
to
incorrect
conclusions.
Hoogstraal
and
Aeschlimann
(1982)
re-
viewed
the
patterns
of
tick—host
associations
and
presented
an
analysis
of
host
specificity
among
ticks
of
vertebrates.
This
analysis
is
the
basis
for
the
following
discussion.
The
host
specificity
of
ticks
is
expressed
by
the
degree
of
limited
or
strict
association
with
the
host:
(1)
strict-total
specificity
(ST);
(2)
moderate-total
(MT);
(3)
strict-stage-stage
(SSS);
(4)
strict/moderate-stage-stage
(SMSS);
(5)
moderate-stage-stage
(MSS);
and
(6)
nonparticular
(NP).
Any
particular
type
of
host
specificity
is
limited
to
a
specific
tick
taxon.
The
ST
host
specificity
refers
to
the
ticks
whose
adults
and
immatures
both
are
strictly
specific
for
the
same
limited
host
group,
as
in
all
genera
of
Argasidae
and
Aponomma,
Boophilus,
Margarapus,
and
a
few
species
in
other
major
genera
of
Ixodidae.
The
MT
specificity
indicates
that
both
adults
and
immatures
are
strictly
host
specific
but
the
host
group
is
somewhat
less
limited
as
in
Ornithodoros,
Ixodes,
Amblyomma,
and
Rhipicephalus.
The
SSS
specificity
represents
the
ticks
whose
adults
and
immatures
are
each
strictly
specific
for
different
limited
host
groups;
this
occurs
chiefly
in
Ixodidae
(Ixodes,
Amblyomma,
Hyalomma,
Dermacentor,
Nosomma,
and
Rhipicephalus).
In
the
SMSS,
when
adults
are
strictly
specific
to
a
host
group,
immatures
are
moderately
specific
to
a
different
group,
and
con-
versely,
when
immatures
are
strictly
host
specific,
adults
are
moderately
specific
to
a
different
host
group,
as
in
Ixodidae.
The
MSS
ticks
are
those
whose
host
specificity
is
moderately
limited
for
both
adults
and
imma-
tures,
again
as
in
Ixodidae.
The
NP
ticks
readily
accept
nonspecific
hosts
as
found
in
some
hard
ticks.
Monotremata.
Four
species
are
ST
specific
to
monotremes:
Ixodes
or-
nithorhynchi
Lucas
on
platypus;
three
species
on
echidna—Ornithodoros
(Pavlovslcyella)
sp.,
Amblyomma
(Adenopleura)
echidnae
Roberts,
and
Apo-
nomma
concolor
Neumann
(most
of
Aponomma
parasitic
only
on
reptiles).
Four
species
are
MT:
Amblyomma
(three
species),
Haemaphysalis
(one
species);
and
three
are
NP.
Marsupialia.
Twelve
species
are
ST
ticks
representing
Ornithodoros
(Pay-
lovskyella),
Ixodes
(Entoplpiger),
I.
(Exopalpiger),
I.
(Sternalixodes),
Haemaphy-
salis
(Ornithophysalis),
Amblyomma,
and
Aponomma,
on
wallabies,
kan-
garoos,
dasyurids,
bandicoots,
and
wombats.
Eight
species
are
MT
(Haemaphysalis
and
Ixodes),
and
three
are
NT.
Insectivora.
Madagascar
tenrecs
have
eight
ST
species:
Argas
(one
518
Acari
species),
Ixodes
(one
species),
Haemaphysalis
(six
species).
About
an
equal
number
of
Ixodes
and
Haemaphysalis
are
ST
parasites
of
other
insectivores.
Chiroptera.
The
24
ST
species
parasitize
the
Old
World
bats,
and
31
ST
ticks
are
parasitic
on
the
New
World
bats.
They
include
Argas
(Carlos)
(all
six
species),
A.
(Chiropterargas)
(all
four
species),
Ornithodoros
(Reticulinasus)
(all
11
species),
0.
(Alectorobius)
(20
species),
0.
(Subparmatus)
(all
three
species),
Antricola
(all
seven
species),
and
Nothaspis
(monotypic)
(Ar-
gasidae);
Ixodes
(Eschatocephalus)
(two
species),
I.
(Lepidixodes)
(one
species).
Primates.
Two
Ixodes
species
are
ST
parasites
of
Ethiopian
Colobus
and
Cercopithecus
monkeys.
Malagasy
lemurs
have
one
Ixodes
and
one
Haemaphysalis
ST
species.
Edentata
and
Pholidota.
The
Neotropical
Edentata
have
two
ST
species
and
three
SS
(adult)
species
of
Amblyomma
(Amblyomma).
In
the
same
sub-
genus
there
are
two
other
species
that
are
MT
parasites.
Two
Amblyomma
(Adenopleura)
species
are
ST
parasites
of
pangolines
or
scaly
anteaters.
Other
adenopleuran
Amblyomma
are
specific
for
reptiles.
Lagomorpha.
The
Ochotonidae
are
host
to
two
ST
species
of
Ixodes
and
one
MT
species
of
Ixodes
(Pholeoixodes).
They
also
are
parasitized
by
imma-
tures
of
other
Ixodes
and
Dermacentor
and
both
adults
and
immatures
of
several
Haemaphysalis
and
Rhipicephalus
species.
Rabbits
and
hares
(Leporidae)
are
hosts
of
numerous
immatures
and
some
adults
of
ST,
SMS,
and
NP
species;
ST—Haemaphysalis
(two
species),
Otobius
(one
species),
Dermacentor
(one
species),
Ixodes
(two
species);
SMS—Haemaphysalis
(one
species),
Amblyomma
(one
species),
Ixodes
(two
species),
Rhipicephalus
(five
species).
Rodentia.
Only
limited
data
are
available
for
host
specificity
in
rodent
ticks.
There
are
23
ST
species
of
rodents
in
the
Neotropical
and
18
in
the
Nearctic
regions.
They
represent
Ornithodoros,
Ixodes,
and
Amblyomma.
In
the
Palearctic,
12
ST
species
comprise
eight
Ixodes,
one
Argas,
one
Rhipicephalus,
and
three
Anomalohimalaya.
The
Malagasy
Nesomyidae
have
five
ST
Ornithodoros,
Ixodes,
and
Haemaphysalis
species.
Rodents
are
impor-
tant
hosts
of
many
MT
Ornithodoros
and
some
ixodid
species
and
for
ft
-
ma-
tures
of
some
300
of
the
approximately
600
ixodid
species
with
a
three-host
life-cycle
pattern.
Carnivora.
Adults
of
certain
Haemaphysalis
and
Rhipicephalus
species
are
primary
parasites
of
Carnivora.
R.
(R.)
sanguineus
is
an
universal
ST
species
for
domestic
dogs
and
Ixodes
(two
species)
and
Haemaphysalis
(three
species)
are
ST
species.
SS
and
MS
(adult)
species
of
Carnivora
are
Ixodes
(seven
species),
Amblyomma
(one
species),
Dermacentor
(one
species),
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
519
Haemaphysalis
(17
species),
Rhipicephalus
(about
15
species),
and
Rhipicentor
(two
species).
Tubulidentata,
Proboscidea,
and
Hyracoidea.
Little
host
specificity
is
found
in
ticks
of
Tubulidentata
and
Proboscidea.
No
host-specific
tick
is
known
for
the
aardvark,
and
adults
of
one
Amblyomma
and
one
Dermacentor
species
are
SS
parasites
of
the
Ethiopian
elephants.
Six
ST
parasites
are
found
on
rock
hyraxes
(Procavia
and
Heterohyrax),
which
include
four
species
of
the
Haemaphysalis
(Rhipistoma)
orientalis
group,
one
Ixodes,
and
one
Rhipicephalus.
A
single
argasid
ST
species
[Ornithodoros
(0.)
procaviae
Theodor]
is
found
on
Procavia
in
the
Negev
Desert
(Palearctic).
Perissodactyla.
Numerous
SS
or
MS
(adult)
species
of
Amblyomma,
Hya-
lomma,
Rhipicephalus,
Dermacentor,
and
Boophilus
are
parasitic
on
Equidae
and
Rhinocerotidae,
with
one
ST
species,
Margaropus
winthemi
Karsch,
on
the
zebra
and
the
domestic
horse.
The
Tapiridae
have
four
Amblyomma,
one
Ixodes,
and
one
Dermacentor
SS
species.
Artiodactyla.
At
least
190
ixodid
species
(none
are
Aponomma,
Anomalo-
himalaya,
or
Rhipicentor,
and
relatively
few
are
Ixodes)
and
only
six
argasid
ticks
(five
Ornithodoros
and
one
Otobius)
are
parasitic
on
Artiodactyla.
Most
of
these
ticks
are
SS
(adult)
species.
The
ST
species
are
Ornithodoros
(0.)
porcinus
Walton
on
the
Ethiopian
suids;
Haemaphysalis
traguli
Oudemans
on
the
Oriental
Tragulidae;
Dermacentor
(Anocenter)
nitens
Neumann
on
the
Neotropical
cervids;
Ornithodoros
(Ornamentum)
coriaceus
Koch
on
the
Nearctic
cervids;
0.
(0.)
indica
Rau
and
Haemaphysalis
(H.)
birmaniae
Supino
on
the
Oriental
cervids;
two
Margaropus
on
the
Ethiopian
giraffids,
M.
reidi
Hoogstraal
and
M.
wileyi
Walker;
Otobius
megnini
Duge's
on
the
Nearctic
Antilocapridae;
and
0.
(Alveonasus)
lahorensis
Neumann,
0.
(Pavlovskyella)
tholozani
(Laboulbene
and
Megnin),
Boophilus
annulatus
(Say),
and
B.
kohlsi
Hoogstraal
and
Kaiser,
on
the
Palearctic
Bovidae,
and
Boophilus
decoloratus
(Koch)
and
B.
geigyi
Aeschlimann
on
the
Ethiopian
bovids.
HAEMAPHYSALINE
TICKS
The
155
species
of
the
genus
Haemaphysalis
(Fig.
10.1),
parasitic
on
birds
and
mammals,
constitute
the
most
useful
assemblage
in
the
superfamily
Ixodoidea
for
displaying
numerous
interrelated
structural-biological
clues
to
affinities
between
tick
species
and
groups
and
to
historical
and
contem-
porary
host
associations.
Only
the
genus
Ixodes
is
larger
(
±
217
species)
than
Haemaphysalis,
but
we
know
much
less
about
Ixodes
biology
and
immature
stages.
A
number
of
structurally
primitive
species,
each
with
specialized
biological
proper-
ties,
provide
indicators
of
the
early
history
and
contemporary
survival
and
520
Acari
adaptation
of
Haemaphysalis
species.
No
other
tick
genus
shows
this
range
of
lucid
clues
or
this
variety
of
data
for
species
of
biological
and
evolution-
ary
significance.
An
unusual
proportion
of
this
data
derives
from
studies
of
species
restricted
to
"remote"
areas
of
the
world.
Haemaphysalis
sexual
dimorphism
is
expressed
by
the
usual
ixodid
characters:
presence
of
porose
areas
on
the
female
basis
capituli,
differ-
ences
in
the
male
and
female
scutums
and
external genital
areas,
and
larger
female
body
size
(Figs.
10.11,
10.12,
10.15, 10.16,
10.20).
However,
Haemaphysalis
ticks
differ
from
those
of
other
genera
in
that
male
capitular
spurs
and
spurlike
angles,
and
also
coxal
spurs,
are
almost
invariably
more
luxurient
than
those
of
females.
Comparing
these
special
haemaphysaline
characters
in
the
same
sex
of
different
species,
and
between
males
and
females
of
a
single
species,
provides
numerous
valuable
indicators
of
haemaphysaline
and
host
associations
and
to
the
evolutionary
dynamics
of
these
relationships.
Structural
differences
between
larval,
nymphal,
and
adult
stages
are
equally
valuable
indicators
of
phylogenetic
consociations
and
contribute
basic
criteria
for
differentiating
haemaphysaline
subgenera.
All
Haemaphysalis
species,
so
far
as
known,
have
a
three-host
type
of
life
cycle.
Hosts
of
immatures
and
adults
of
many
species
differ
significantly:
as
do
the
hedgehog
and
fox,
shrew
and
yak,
mouse
and
lion,
rat
and
boar,
lizard
and
ibex,
or
bird
and
bison.
Male
and
female
Haemaphysalis
each
furnish
a
minimum
of
20
clearly
definable,
diverse
structural
characters
for
comparison.
Each
nymph
pro-
vides
at
least
15
characters
and
each
larva
at
least
six.
Different
males
and
females
in
about
150
taxa
(very
few
species
are
known
by
only
one
sex)
provide
about
6000
character
states
(units)
for
comparison.
We
also
know
of
125
different
nymphs
(1875
units)
and
115
different
larvae
(690
units).
With
this
total
of
8565
units
for
morphological
analysis,
it
has
been
possible
to
develop
a
subgeneric
classification
that
is
meaningful
morphologically
as
well
as
biologically
and
reflects
Haemaphysalis—host
coevolution.
Of
the
155
known
Haemaphysalis
species,
150
easily
fall
into
16
subgenera
(a
few
of
which
remain
to
be
described).
Other
ixodid
genera
(except
Ixodes)
contain
fewer
species
with
fewer
structural
indicators.
After
more
than
200
Ixodes
species
have
been
better
studied,
a
comparative
phylogenetic
and
host
analysis
of
Ixodes
and
Haemaphysalis
should
considerably
enhance
the
understanding
of
tick
and
host
coevolution.
STRUCTURALLY
PRIMITIVE
(SP)
HAEMAPHYSALINES
The
17
structurally
primitive
(SP)
haemaphysaline
species
in
four
subgen-
era
(Alloceraea,
Allophysalis,
Aboimisalis,
Sharifiella)
link
Haemaphysalis
and
other
nonrhipicephaline
ixodids
and
differ
distinctly
from
138
other
haemaphysaline
species
in
12
other
subgenera
(Hoogstraal
1965,
1978).
The
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
521
most
basic
criterion
of
the
17
SP
species
is
the
presence,
in
each
stage,
or
only
in
larvae
and
nymphs,
of
a
lateral
convexity
of
the
basis
capituli
or
of
a
projection
from
each
side
of
the
basis
capituli.
The
next
most
basic
criterion
is
the
palpal
structure.
SP
palpi
are
elongate
and
compact,
but
not
baso-
laterally
salient.
SP
capitular
and
leg
spur
development
is,
with
few
nota-
ble
exceptions,
exceedingly
slight.
In
all
of
the
other
138
haemaphysaline
species,
the
basis
capituli
is
rectangular,
usually
with
posterior
cornua;
lateral
projections
are
absent.
In
the
17
species
constituting
SP
subgenera,
a
stepwise
progression
from
atypical
to
typical
haemaphysaline
characters
is
exhibited
from
species
to
species
and
from
larva
to
nymph
to
adult,
as
well
as
between
males
and
females
of
individual
species
(Fig.
10.7).
This
progression
provides
a
clear
picture
of
the
structural
evolution
through
history.
Comparative
criteria
of
SP
and
structurally
advanced
(SA)
subgenera,
closely
associated
with
host
and
geographical
relationships
and
biological
properties,
are
the
basic
indi-
cators
of
evolutionary
processes
within
this
large
group
of
ixodid
ticks.
Together
with
SP
haemaphysalines,
the
single
structurally
intermediate
(SI)
subgenus
Herpetobia
(seven
species)
and
the
11
SA
subgenera
exhibit
a
gradual
but
strong
phylogenetic
trend
away
from
Amblyomminae-like
characters
of
SP
subgenera
and
set
the
genus
Haemaphysalis
apart
structur-
ally
(but
not
biologically)
from
all
other
ixodid
genera.
The
dominating
phylogenetic
trend
throughout
the
genus
Haemaphysalis
is
away
from
laterally
salient
basis
capituli
and
Aponomma-Amblyomma
type
elongate
palpi
toward
(1)
a
rectangular
basis
capituli
with
posterior
cornua,
(2)
compact
to
broadly
basosalient
palpi,
and
(3)
various
combinations
of
coxal
and
trochantal
spurs
and
capitular
spurs,
angles,
or
emarginations.
These
hair-hooking
devices
(Figs.
10.8-10.10)
assist
the
small
tick
in
pene-
trating
a
maze
of
stiff
hairs
and
spines
to
reach
a
feeding
site
on
the
host
integument.
A
trend
toward
smaller
bodies
and
capitula
is
also
strong.
In
small-sized
ticks,
posterior
cornua
on
a
rectangular
basis
capituli
and
com-
pact
or
short,
broad
palpi
function
more
effectively
to
force
a
passage
though
feathers
or
fur
than
do
a
broad
basis
capituli
and
elongate
palpi.
Large
primitive
ticks
parasitizing
glabrous
reptiles
were
not
faced
with
this
problem.
Subgenus
Alloceraea
Schultz
The
Alloceraea
species
are
H.
(A.)
vietnamensis
Hoogstraal
and
Wilson
of
the
Vietnam
highlands;
H.
(A.)
kitaokai
Hoogstraal
of
Japan,
Taiwan,
and
Hu-
nan
(China);
H.
(A.)
aponommoides
Warburton
(Hoogstraal
and
Mitchell
1971)
of
highlands
in
the
central
and
eastern
Himalayan
range
and
south-
ern
China;
and
H.
(A.)
inermis
Birula
of
the
southwestern
USSR,
northern
Iran,
Turkey,
and
eastern
and
southern
Europe
(in
France
probably
in-
troduced
with
East
European
deer
for
parks
and
hunting
reserves).
H.
(A.)
vietnamensis
SP
characters
are
the
most
pronounced
(Fig.
10.4).
In
a
.
z
z
to"
fti
<ra
0
H.
INERMIS
H
THEILERAE
H.PUNGTATA
H.GHORDEILIS
Figure
10.7
The
capitulum
(dorsal
and
ventral
views)
of
the
larva,
nymph,
male
and
female
of
selected
species
in
structurally
primitive
Haemaphysalis
subgenera.
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
523
H.
MEGALAIMAE
H.
BREMNER!
H.
CONCINNA
H.
JAPONICA
H.
LAGRANGEI
H.
SHIMOGA
oar
H.MONTGOMERYI
H.CUSPIDATA
H.
YENI
H.
CALVA.
r11
H.
ASIATICA
H.
FOSSAE
H.
LEACHI
Figure
10.8
The
male
capitulum
(dorsal
and
ventral
views)
of
selected
structurally
advanced
(SA)
Haemaphysalis
species,
showing
the
broad
palpi
with
hair-hooking
spurs
obsolete
or
minute
in
the
Ornithophysalis
species
parasitizing
birds
(H.
megalaima)
or
birds
and
marsupials
(H.
inemneri),
and
a
unique
palpal
modification
for
grasping
artiodactyl
hairs
(H.
concinna),
or
a
variety
of
hair-hooking
spurs
or
slits
for
hooking
around
hairs
of
Artiodactyla
(H.
japonica,
lagrangei,
shimoga,
montgomeryi,
cuspidata,
yeni,
calva),
or
Carnivora
(H.
asiatica,
fossae,
leachi).
this
large
haemaphysaline
(3.6
mm
long),
the
basis
capituli
is
short,
later-
ally
convex,
and
lacks
cornua;
the
palpi
are
narrowly
elongate
(clavate),
segment
3
lacks
a
ventral
spur,
and
segment
4
is
in
an
apical
pit;
the
dental
formula
is
3/3;
coxal
spurs
are
small
or
obsolete;
tarsi
are
narrowly
elon-
gate,
and
tarsus
I
has
a
huge
claw;
the
body
integument
is
leathery
and
the
genital
aperture
is
slitlike
(Hoogstraal
and
Wilson
1966).
Other
female
Al-
loceraea
are
structurally
rather
similar
but
distinctly
smaller
(2.5-2.9
mm
long).
The
sambar
deer
or
another
large
ungulate
may
be
the
host
of
adult
H.
(A.)
vietnamensis,
but
it
is
now
known
only
from
vegetation.
Alloceraea
males,
nymphs,
and
larvae
each
also
have
a
laterally
convex
or
otherwise
laterally
projecting
basis
capituli
lacking
posterior
cornua
and
elongate
palpi
lacking
a
ventral
spur,
but
their
dental
formulae
are
2/2.
These
are
the
only
males
with
a
2/2
dental
formula
in
the
entire
genus
Haemaphysalis.
The
palpal
segment
3
pit
containing
segment
4
is
somewhat
more
posteriorly
displaced
in
other
Alloceraea
species
than
it
is
in
H.
(A.)
metnamensis.
The
various
spurs
and
spurlike
angles
of
the
body
append-
ages
(capitulum
and
legs)
that
function
as
hair-hooking
devices
in
so
many
7
I
Ip
rl
I
r
H.
rn
.
g
alaima•
H.
bripmn•ri
H.
sulcato
H.
kashmiransis
Ti
'
1
r
1
r
r
H.
troguli
H.
lagrangiti
H.
cuspidal!
H.
oculoota
I
1'
I'
GGt
11
,
H.
asiotica
H.
calve
H.
spiniy
•ra
H.
a
nomala
524
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
525
t.1
H.
SIMPLEX
H.ELONGATA
H.SLIBELONGATA
H.TIPTONI
Figure
10.10
Ventral
views
of
male
and
female
Haemaphysalis
parasites
of
tenrecs
showing
virtual
absence
of
spines
and
hooking
devices
in
H.
(Ornithophysalis)
simplex
(which
feed
in
the
host
ears)
and
the
variety
of
palpal,
coxal,
and
trochantal
spurs
and
hooking
devices
in
H.
(Elongiphysalis)
species
which
feed
among
the
body
spines
and
harsh
hairs.
other
haemaphysalines
are
obsolete
or
only
very
slightly
developed
in
each
Alloceraea
stage
[but
moderately
large
in
immature
H.
(A.)
kitaokaij.
Alloceraea
structure
apparently
represents
an
Aponomma-like
primitive
prototype
haemaphysaline
that
evolved
in
the
late
Paleozoic
or
early
Mesozoic
era
(see
"Premammalian
Evolution
of
Ticks").
Ecologically
and
zoogeographically,
contemporary
Alloceraea
are
notably
absent
in
humid
tropical
forests.
Only
the
highland-inhabiting
H.
(A.)
vietnamensis
is
found
in
the
Oriental
region
east
of
the
Indian
subcontinent,
where
the
genus
Haemaphysalis
probably
originated.
Many
contemporary
SA
haemaphysalines
are
common
in
tropical
Asian
forests
where
two,
three,
or
more
species
can
be
found
infesting
a
single
mammal.
Competi-
tion
from
rapidly
evolving
SA
species
may
have
resulted
in
the
extinction
Figure
10.9
Male
coxae
and
trochanters
of
selected
structurally
advanced
Haemaphysalis
species,
showing
absence
or
virtual
absence
of
hair-hooking
spurs
in
H.
(Ornithophysalis)
species
(megalaimae
and
bremneri)
parasitizing
birds
and
marsupials,
the
slight
development
of
these
spurs
in
H.
traguli,
a
parasite
of
the
small-sized
Mouse
Deer
(Tragulus),
and
the
variety
of
hair-hooking
spurs
in
species
adapted
to
Artiodactyls.
526
Acari
of
the
SP
structural
type
in
tropical
forests
(except
the
subgenus
Sharifiella
in
Madagascar).
The
marginal
tropical-temperate
forest
habitat
(1450
m
altitude)
of
H.
(A.)
vietnamensis
apparently
more
closely
approximates
the
early
haemaphysaline
habitat-climatic
type
than
that
of
the
other
Alloceraea
species.
H.
(A.)
kitaokai
is
confined
to
temperate
Japan
and
mountains
of
Hunan
(China)
and
Taiwan,
H.
(A.)
aponommoides
to
Himalayan
and
South-
ern
Chinese
highlands
(2000-4900
m
altitude),
and
H.
(A.)
inermis
to
tem-
perate
European
lowlands.
This
distribution
pattern
appears
to
represent
a
general
ecological
shift
(Darlington
1957)
away
from
the
ancestral
ecolog-
ical-environmental
type
of
the
genus.
The
presence
of
H.
(A.)
vietnamensis
in
a
tropical-temperate
forest
margin
appears
to
satisfy
the
Horton's
postu-
late
(1973)
that
"if
environments
similar
to
the
ancestral
environment
still
occur
in
the
original
center
of
dispersal,
then
primitive
species
are
still
likely
to
occur
there."
Lizards
are
important
hosts
of
immature
H.
(A.)
inermis
in
Palearctic
lowlands.
However,
reptiles
are
rare
or
absent
in
the
highland
and
more
northern
habitats
where
other
Alloceraea
species
have
survived.
Immatures
of
each
contemporary
Alloceraea
species
commonly
feed
on
shrews
and
rodents;
bird
hosts
have
also
been
recorded.
Adults
chiefly
parasitize
Ar-
tiodactyla
such
as
the
yak,
a
variety
of
deer,
wild
and
domestic
sheep
and
goats,
and
occasionally
carnivores
(bear,
wild
cat,
etc.).
Adults
also
infest
domestic
cattle,
buffaloes,
and
horses.
Few
other
Haemaphysalis
species
are
associated
with
domestic
herbivores;
the
fact
that
all
SP
adults
(except
Sharifiella)
feed
on
domestic
animals
is
apparently
significant
in
the
survival
of
this
relict
group.
Notable
biological
peculiarities
also
characterize
the
Alloceraea
species
that
have
been
studied
in
this
respect.
Female
H.
(A.)
inermis
(see
Brumpt
in
Nuttall
and
Warburton
1915)
and
H.
(A.)
kitaokai
deposit
fewer
than
1000
eggs
(Kitaoka
and
Morii
1967),
or
less
than
25%
of
the
total
egg
production
of
most
other
Haemaphysalis
species.
Each
egg
and
the
resulting
larva
is
unusually
large
for
this
genus.
Immatures
feed
fully
in
90
minutes
to
6
hours
[see
also
Nosek
1973,
for
H.
(A.)
inermis];
immatures
of
other
Haemaphysalis
species
(and
of
most
other
ixodid
species)
require
two
to
seven
days
to
feed.
In
the
cold,
high
Himalayas,
adult
H.
(A.)
aponommoides
is
active
through
much
of
the
year
(Hoogstraal
and
Mitchell
1971).
How-
ever,
adults
of
related
species
inhabiting
warmer
lower
altitudes
are
active
chiefly
in
winter.
"Uncountable
numbers"
of
adult
H.
(A.)
kitaokai
parasitize
Japanese
deer
when
the
temperature
is
near
or
below
0°C
(Kita-
oka
and
Fujisaki
1972).
Adult
H.
(A.)
inermis
quest
for
hosts
in
early
and
late
winter
and
in
spring,
and
are
easily
observed
moving
about
on
snow
and
on
twigs
and
grass
above
the
snow
surface
(Macicka
1958).
This
cold-
season
adult
activity
pattern,
an
adaptation
to
prevent
desiccation
during
activity
on
hot,
dry
summer
days,
suggests
that
the
water
balance
proper-
ties
of
SP
species
may
not
differ
greatly
from
those
of
SA
species
in
humid
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
527
tropical
forests.
The
unique
leathery
Alloceraea
integument
is
probably
also
specially
adapted
for
water
conservation.
Among
SP
haemaphysalines,
the
chromosomes
of
only
H.
(A.)
kitaokai
have
been
studied
(Oliver,
Tanaka,
and
Sawada
1974).
This
species
pos-
sesses
fewer
chromosomes
(9
=
18
+
XX,
d
=
18
+
X)
than
is
typical
of
several
studied
species
in
the
SA
subgenera
(9
=
20
+
XX,
d
=
20
+
X).
The
current
working
hypothesis
of
these
authors
is
that
the
"primitive"
chromosome
condition
in
the
genus
Haemaphysalis,
and
probably
in
most
genera
of
the
family
Ixodidae,
consists
of
a
2n
number
of
20
autosomes
plus
two
sex
chromosomes
in
females
and
20
autosomes
plus
one
sex
chromo-
some
in
males.
The
absence
of
a
pair
of
chromosomes
in
H.
(A.)
kitaokai
might
have
reduced
the
genetic
variability
of
this
species
and
confined
it
structurally,
and
in
some
respect
biologically,
to
a
primitive
type
of
exis-
tence.
Subgenus
Allophysalis
Hoogstraal
The
eight
species
in
the
subgenus
Allophysalis
display
a
combination
of
SP
structural
conformity
and
of
stepwise
or
abrupt
advances
in
SP
ranks.
Certain
Allophysalis
nymphs
and/or
adults
approach
a
SA
pattern
in
part,
but
no
larvae
do
so.
These
eight
relict-type
ticks
avoid
competition
from
other
ticks
in
rocky
biotopes
in
the
1600-3800
meter
altitude
range
of
Asian
mountains.
The
Allophysalis
species
are
H.
(A.)
tibetensis
Hoogstraal
of
Tibet;
H.
(A.)
pospelovashtromae
Hoogstraal
of
southern
USSR
and
Mongolia
(Figs.
10.11-10.14);
H.
(A.)
danieli
Cerny
and
Hoogstraal
of
northern
Pakis-
tan
and
Afghanistan;
H.
(A.)
demidovae
Emel'yanova
of
Mongolia;
H.
(A.)
garhwalensis
Dhanda
and
Bhat
of
northern
India
and
Nepal;
H.
(A.)
xin-
jiangensis
Teng
of
western
China;
H.
(A.)
warburtoni
Nuttall
of
southern
China
and
Nepal;
and
H.
(A.)
kopetdaghica
Kerbabayev
of
Turkmen
SSR
and
northern
Iran.
Each
immature
Allophysalis
(except
the
nymph
of
warburtoni)
has
a
short,
broadly
angular
basis
capituli
(Fig.
10.14).
This
probably
illustrates
one
of
many
designs
that
appeared
and
disappeared
during
evolution
from
the
short,
rounded
Alloceraea
basis
capituli
pattern
to
the
rectangular,
cornua-
bearing
pattern
of
SA
species.
Immature
Allophysalis
basis
capituli
patterns
range
from
short,
remark-
ably
laterally
expanded
types
(pospelovashtromae,
demidovae,
danieli,
garh-
walensis)
to
posterolaterally
convex
and
cornua-bearing
(warburtoni
nymph:
the
first
comua
seen
in
this
genus).
Immature
palpi
remain
elongate
(da-
vate),
as
in
Alloceraea,
but
have
become
compact
in
kopetdaghica.
The
first
ventral
spur
on
immature
palpi
is
seen
in
the
warburtoni
nymph.
Some
Allophysalis
nymphs
and
larvae
bear
the
first
large
coxal
spurs
seen
in
this
genus
[except
for
immature
H.
(A.)
kitaokai].
The
Allophysalis
adult
basis
capituli
is
variously
shaped
and
armed
with
unusually
variable
cornua.
In
each
species,
the
female
basis
capituli
con-
I
1'0,..
'I
41
II
E
.
10
E
R
,
i
t
!
••
'Ir.,
4
7 ,
II
-,
i
;.•
-.•
/:-0,
A
la
B
rP
G.:
1
dla
1
,,
I
E
E
r
l
I
a
a
.
C
D
Figure
10.11
Haemaphysalis
(Allophysalis)
pospelovashtromae.
(A,
B)
Male,
dorsal
and
ventra
views;
(C,
D)
female,
dorsal
and
ventral
views.
528
A
r
,
tr1,411:
`1.
tir.i"
"-
,
4„
r
4
.)
..4
Ayh
o•••
_
I I
,47"
-
7•4
(
7:
42
:3'
4
7
;
3-
-
-
Z *.
4'
-77
41
:
.•‘•
. .
.
/
/
T
,•••
I
G
F
B
D
- -
716
%'
-
}P
,a4
L
0
ru
Figure
10.12
Haemaphysalis
(Alibphysalis)
pospelocashtromae.
(A—H)
Male:
(A,
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome;
(D)
genital
area;
(E)
spiracular
plate;
(F)
coxae
and
trochanters
Ito
IV;
(G)
femur
IV,
internal
view;
(1
-
i)
tarsi
Ito
IV.
(I—P)
Female:
(I,
I)
capitulum,
dorsal
and
ventral
views;
(K)
hypostome;
(L)
genital
area;
(M)
spiracular
plate;
(N)
coxae
and
trodanter
Ito
IV;
(0)
femur
IV;
(P)
tarsi
I
to
N.
529
530
Acari
1
A
B
IdClil
II
O
C
D
Figure
10.13
Immature
Haemaphysalis
(Allphysalis)
pospelovashtromae.
(A,
B)
Nymph,
dorsal
and
ventral
views;
(C,
D)
larva,
dorsal
and
ventral
views.
forms
more
closely
to
the
primitive
(Alloceraea)
type
than
does
that
of
the
male.
Female
Allophysalis
palpi
remain
elongate,
as
in
Alloceraea,
but
are
only
moderately
elongate
in
kopetdaghica.
Male
palpi
are
shorter
or
com-
pact,
though
not
broadened.
The
adult
palpus
for
the
first
time
bears
a
small
ventral
spur
which
is,
however,
medially
rather
than
posteriorly
directed.
This
medially
directed
spur
type
is
the
primitive
progenitor
of
that
characterizing
bird-parasitizing
and
primitive
mammal-parasitizing
species
of
the
SA
subgenus
Ornithophysalis.
Adult
dental
formulae
are
now
4/4,
as
in
almost
all
other
haemaphysalines,
but
5/5
or
6/6
in
some
warbur-
7
it
0
v4.
C
r
L
/
/
F
r
I
---4
\it
(
t
,
'
J
Nu
..„
Figure
10.14
Immature
Hatinaphysais
(Arlpiry%dis)
pospeiczasirtrarnae.
(A—F)
Nymph:
(A.
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome;
(D)
spiracular
(E)
Crilae
and
trochanters
I
to
IV;
(F)
tarsi
I
to
IV.
(G—K)
Larva:
(G,
II)
capitulum,
dorsal
and
ventral
views;
(1)
hypostome;
(J)
come
and
trochanters
II,
III;
(K)
tarsi
11,
DI
y
t
e.
,4
t r
r
4
AI
531
532
Acari
toni.
The
3/3
adult
formula,
earlier
observed
in
Alloceraea,
will
be
found
again
in
adults
of
only
a
few
SA
species
specially
adapted
to
parasitizing
tenrecs,
rodents,
and
rabbits.
Adult
coxal
spurs
are
now
moderately
sized
or
fairly
large
and
exhibit
various
triangular,
spatulate,
lanceolate,
or
hook-
like
forms
characteristic
of
haemaphysalines
specialized
for
parasitizing
Artiodactyla.
All
tarsi
are
short
and
bear
an
unusually
large
apicoventral
hook.
Female
external
genital
structures
differ
distinctly
from
each
other
and
also
from
those
of
all
other
haemaphysalines.
Individual
unfed
male
H.
(A.)
warburtoni
may
be
small
(2.2
mm
long)
but
average
2.8
mm
long,
as
in
all
other
Allophysalis
species
except
H.
(A.)
tibetensis,
which
is
quite
large
(3.3
mm
long).
Unfed
females
are
at
least
as
large
(3.4-3.8
mm
long)
as
those
of
H.
(A.)
vietnamensis.
Each
Allophysalis
adult
parasitizes
members
of
the
rich
Asian-mountain
artiodactyl
fauna
and
less
often,
domestic
artiodactyls,
marmots,
and
hu-
mans.
Adult
activity
is
recorded
chiefly
during
spring
and
fall,
and
that
of
immatures
from
late
spring
to
fall.
Adults
are
recorded
from
domestic
goats,
sheep,
cattle,
yaks,
and
a
dog
(one
specimen),
and
from
the
wild
goral,
serow,
thar,
musk
deer,
and
ibex.
Immatures
parasitize
rodents,
chiefly
Alticola,
Cricetulus,
and
Marmota,
and
also
hares
and
the
rock-
dwelling
pika
Ochotona
(Lagomorpha).
Both
adult
and
immature
H.
(A.)
kopetdaghica
were
taken
from
an
immature
wild
goat,
Capra
hircus
aegagrus
Erxleben,
which
was
probably
sick
(Hoogstraal
and
Wassef
1979).
Large
ground-feeding
birds
such
as
the
monal
pheasant
are
also
important
hosts
of
immature
H.
(A.)
warburtoni
(Hoogstraal
1971).
The
biology
and
ecology
of
H.
(A.)
pospelovashtromae
in
the
USSR
have
been
reviewed
by
Grebenyuk
(1966)
from
literature
and
personal
observa-
tions
in
Kirghiz
SSR.
Immatures
infest
a
variety
of
alpine
rodents,
pikas,
and
hares,
occasionally
artiodactyls
and
carnivores,
and
are
common
on
ground-feeding
birds
in
the
Caucasus.
Its
life
cycle
extends
over
three
years
(Sartbaev
1955;
Ogandzhanian
and
Martirosian
1965).
Notably,
im-
matures
feed
for
about
seven
days,
thus
differing
from
those
of
Alloceraea.
Each
female
deposits
at
least
1000
eggs.
Subgenus
Aboimisalis
Santos
Dias
Aboimisalis
immatures
retain
the
primitive
SP
basis
capituli
form.
Adults
are
structurally
more
advanced
and
show
a
slight
step
in
the
generic
trend
to
broad
palpi.
The
species
include:
H.
(A.)
cornupunctata
Hoogstraal
and
Varma
of
Nepal,
northern
India,
Pakistan,
and
Afghanistan;
H.
(A.)
punc-
tata
Canestrini
and
Fanzago
of
southwestern
Asia
and
much
of
Europe
(Figs.
10.15-10.18);
H.
(A.)
chordeilis
(Packard)
of
Canada
and
the
United
States;
and
H.
(A.)
cinnabarina
Koch
of
Brazil.
The
Eurasian
stem
of
this
subgenus
is
represented
by
H.
(A.)
cornupunctata,
confined
to
altitudes
between
1600
and
3200
m,
and
by
H.
(A.)
punctata
of
lowland
semideserts,
steppes,
and
open
forests.
The
American
species
are
structurally
much
like
"
1
e
A
B
It
wf
.
.
E
is
Or
.
C
D
E
E
Figure
10.15
Haemaphysalis
(Aboimisalis)
punctata.
(A,
B)
Male,
dorsal
and
ventral
views;
(C,
D)
female,
dorsal
and
ventral
views.
533
T
A
C
/
I
e
B
_?
1
)1
F
D
E
G
1
O
I
r
r
r
'
L
Figure
10.16
Haemaphysalis
(Aboimisalis)
punctata.
ventral
views;
(C)
hypostome;
(D)
genital
area;
(E)
to
IV;
(G)
femur
IV,
inner
view;
(H)
tarsi
I
to
IV.
ventral
views;
(K)
hypostome;
(L)
genital
area;
(M)
to
IV;
(0)
femur
IV;
(P)
tarsi
I
to
IV.
N
(A—H)
Male:
(A,
B)
capitulum,
dorsal
and
spiracular
plate;
(F)
coxae
and
trochanters
I
(I—P)
Female:
(I,
I)
capitulum,
dorsal
and
spiracular
plate;
(N)
coxae
and
trochanters
I
534
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
535
1
1
I
E
E
1
f
r
:
rr
4.
J
E
E
In
0
Figure
10.17
Immature
Haemaphysalis
(Aboimisalis)
punctata.
(A,
B)
Nymph;
(C,
D)
larvae,
dorsa
and
ventral
views.
their
Euroasian
counterparts.
H.
(A.)
cinnabarina
is
known
only
from
two
females
collected
before
1844
(Hoogstraal
1973).
Notably,
only
two
other
haemaphysaline
species
(subgenus
Gonixodes)
occur
in
the
Americas.
The
lateral
expansion
of
the
immature
Aboimisalis
basis
capituli
is
the
most
extreme
of
all
SP
forms,
especially
in
nymphs
(Fig.
10.5).
Immature
palpi
have
become
compact;
they
lack
salience
in
H.
(A.)
cornupunctata
but
0
0
D
F
E
C
O
G
0
H
L
K
Figure
10.18
Immature
Haemaphysalis
(Aboimisalis)
punctata.
(A—F)
Nymph:
(A,
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome;
(D)
spiracular
plate;
(E)
coxae
and
trochanters
Ito
IV;
(F)
tarsi
Ito
IV.
(G—L)
Larva:
(G,
I-1)
capitulum,
dorsal
and
ventral
views;
(I)
hypostome;
(J)
spiracular
plate;
(K)
coxae
and
trochanters
I
to
III;
(L)
tarsi
I
to
III.
J
536
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
537
are
slightly
salient
in
H.
(A.)
punctata
and
H.
(A.)
chordeilis,
and
the
ventral
spur
is
slight
or
obsolete.
Dental
formulae
are
2/2.
Coxal
spurs
are
obsolete
to
moderate
sized.
Adult
Aboimisalis
differ
from
their
SP-type
immatures
in
having
a
rectan-
gular
basis
capituli
characteristic
of
SA
species.
Cornua
extend
from
this
base
in
each
male
but
in
females
only
in
H.
(A.)
cornupunctata.
Adult
palpi
are
quite
compact,
slightly
broader
than
in
the
few
males
of
earlier
subgen-
era
in
which
the
palpi
tended
to
be
more
compact.
Dental
formulae
are
4/4
to
6/6.
Coxal
spurs
are
moderate
sized
in
females,
but
male
coxae
I
to
III
spurs
are
much
reduced
and
coxa
IV
spur
is
very
long
and
lanceolate.
This
lanceolate
spur
type
reappears
in
several
SA
species
associated
with
Ar-
tiodactyla.
The
short
tarsi
are
ventrally
hooked
as
in
Allophysalis
and
Sharifiella.
The
adult
remains
large
in
Eurasian
species
(length
about
3.0
mm
in
males,
about
3.4
mm
in
females)
but
is
moderate-sized
in
the
Ameri-
can
species.
Biologically
and
ecologically,
each
Aboimisalis
species
differs
distinctly.
All
our
records
(including
unpublished)
and
those
of
Dhanda
and
Kulkarni
(1969)
for
both
immature
and
adult
H.
(A.)
cornupunctata
are
from
wild
or
domestic
artiodactyls.
Immatures
and
adults
are
sometimes
taken
from
one
artiodactyl
host,
but
immatures
are
not
found
on
insectivores
or
rodents
examined
in
the
same
collecting
localities
in
Nepal,
India,
Pakistan,
and
Afghanistan.
Parasitism
of
the
same
kind
of
host
by
immatures
and
adults,
seen
among
SP
subgenera
only
in
Sharifiella,
occurs
in
few
species
of
SA
subgenera.
All
H.
(A.)
cornupunctata
records
are
from
the
spring
and
fall
seasons.
Ecologically,
H.
(A.)
cornupunctata
is
similar
to
most
other
SP
ticks
but
quite
different
from
the
three
other
Aboimisalis
species.
Adult
H.
(A.)
punctata
parasitize
wild
and
domestic
artiodactyls,
rarely
other
vertebrates.
Immatures
feed
chiefly
on
small
hosts
(Sartbaev
1961;
Grebenyuk
1966;
Tovornik
1970;
Nosek
1971).
Numerous
ground-feeding
birds
are
important
hosts
and
carry
nymphs
and
larvae
when
migrating
(Hoogstraal
et
al.
1963,
1964).
Immatures
also
parasitize
lizards,
insecti-
vores,
rodents,
and
hares,
less
often
artiodactyls
and
carnivores.
The
ecological
adaptability
and
geographic
range
of
H.
(A.)
punctata
are
greater
than
in
most
other
haemaphysalines.
However,
this
species
does
not
reach
alpine
levels
or
penetrate
into
the
interior
of
humid
temperate
forests.
Its
life
cycle
usually
extends
over
a
2-year
period.
In
most
areas
adult
H.
(A.)
punctata
feed
during
fall
and
spring
but
in
mild
latitudes
also
in
winter
and/
or
summer.
Immatures
are
active
from
spring
to
fall.
H.
(A.)
punctata
egg
numbers
3000-5000
per
female,
and
immature
and
adult
feeding
periods
are
similar
to
those
generally
reported
for
SA
species.
Larvae
feed
for
three
to
five
days,
nymphs
for
four
to
seven
days,
and
females
for
six
or
more
days.
The
North
American
H.
(A.)
chordeilis,
which
is
especially
common
in
Canada
(Gregson
1956;
Kohls
1960),
infests
grouse
and
other
game
birds
but
rarely
mammals.
There
are
no
definitive
biological
or
ecological
studies
538
Acari
of
H.
(A.)
chordeilis.
The
long
coxa
IV
spur
of
the
male
[similar
to
those
of
H.
(A.)
punctata
and
H.
(A.)
cornupunctata]
sets
this
species
apart
from
practi-
cally
all
other
bird-infesting
haemaphysalines,
which
are
characterized
by
conservative
spur
development.
The
H.
(A.)
chordeilis
spur
probably
reflects
a
dominant
feature
of
Aboimisalis
structure
rather
than
a
useful
adaptation
for
parasitizing
birds.
In
review,
among
the
17
SP
species,
15
have
coevolved
with
Artiodac-
tyla,
1
with
birds,
and
1
(see
below)
with
tenrecs.
Subgenus
Sharifiella
Santos
Dias
The
single
species
of
Sharifiella,
H.
(S.)
theilerae
Hoogstraal,
conforms
to
SP
group
criteria
but
also
displays
unusual
characters
which
are
probably
functionally
adaptive
to
parasitizing
the
spiny
tenrecs
of
Madagascar
(see
following
section:
Haemaphysalis
and
Tenrecs).
The
short,
rounded
basis
capituli
of
each
stage
lacks
cornua.
The
elongate
palpi
are
either
impercep-
tibly
(larva)
or
slightly
(nymph
and
adult)
broadened
posteriorly
and
lack
a
discrete
ventral
spur.
Dental
formulae
are
2/2
in
immatures
and
3/3
in
adults.
A
small
spur
near
the
external
margin
of
each
coxa,
as
well
as
a
second
spur
near
the
internal
margin
of
some
coxae,
are
both
unique
in
the
entire
genus.
The
very
short,
ventrally
hooked
tarsi
bear
large
claws
but
extraordinarily
small
pulvilli.
As
is
common
among
tropical
haemaphy-
salines,
this
species
is
small
(male
2.0
to
2.3
mm
long).
This
is
one
of
the
few
SP
species
from
outside
Eurasia
and
which
parasitizes
only
small
hosts.
The
SP
subgenus
Sharifiella
is
compared
with
SA
tenrec-infesting
haemaphysalines
in
the
following
section.
These
structurally
and
phy-
logenetically
disparate
haemaphysaline
parasites
of
a
single
mammalian
family
provide
rich
clues
to
tick
and
mammal
coevolution.
HAEMAPHYSALIS
AND
TENRECS
(MALAGASY
INSECTIVORES)
Six
Haemaphysalis
species
are
specific
parasites
of
Malagasy
tenrecs
(Insec-
tivora:
Tenrecidae)
(Hoogstraal
et
al.
1974;
Uilenberg
et
al.
1980).
Their
hosts
are
the
four
coarse-haired,
spiny
tenrecs,
Setifer
setosus
(Schreber),
Echinops
telfairi
Martin,
Tenrec
ecaudatus
(Schreber),
and
Hemicentetes
semi-
spinosus
(Cuvier),
and
the
soft-furred
Microgale
(Nesogale)
talazaci
(Major)
(Eisenberg
and
Gould
1970)
(Table
10.1).
Three
of
the
six
species
parasitizing
coarse-haired,
spiny
tenrecs—H.
elongata
Neumann,
H.
subelongata
Hoogstraal,
and
H.
tiptoni
Hoogstraal—
constitute
the
distinctive
SA
subgenus
Elongiphysalis
Hoogstraal,
Wassef,
and
Uilenberg
(Fig.
10.10).
These
are
exclusive
parasites
of
S.
setosus,
T.
ecaudatus,
and
H.
semispinosus.
H.
(E.)
subelongata
is
a
primary
parasite
of
T.
ecaudatus,
the
most
widely
distributed
tenrec,
which
is
found
in
a
variety
of
habitats.
H.
(E.)
tiptoni,
apparently
confined
to
rain
forests,
feeds
chiefly
on
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
539
Table
10.1
Host
Associations
(%)
of
Haemaphysalis
Species
on
Tenrecsa
H.
(0.)
b
H.
(E.)
b
H.
(E.)
b
H.
(E.)
5
H.
(S.)
b
Tenrec
species
simplex
elongata
subelongata
tiptoni
theilerae
58`
24
C
8`
10`
Sealer
setosus
51
26
0
0
10
Tenrec
ecaudatus
1
31
92
38
90
Hemicentetes
semispinosus
d
1
36
4
62
0
Echinops
telfairi
38
2
0
0
0
Microgale
talazacie
6
3
0
0
0
"Tenrec"
(unident.)
3
2
4
0 0
Source:
After
Hoogstraal
et
al.
1974.
°Percent
association
based
on
179
lots
in
Hoogstraal
Tick
Collection.
b
H.
(a)
=
H.
(Ornithophysalis);
H.
(S.)
=
H.
(Sharifiella);
H.
(E.)
=
H.
(Elongiphysalis).
`Number
of
lots.
d
Previously
listed
as
H.
semispinosus
and
H.
nigriceps.
`All
ticks
are
immature.
H.
semispinosus,
but
also
on
T.
ecaudatus.
H.
(E.)
elongata
commonly
infests
each
coarse-haired
species
except
E.
telfairi
of
the
arid
southwest.
Only
immatures
of
H.
(0.)
simplex
and
H.
(E.)
elongata
are
known
from
the
soft-
furred
Microgale
talazaci.
Three
other
haemaphysalines
specific
to
coarse-haired
tenrecs
are
H.
(Ornithophysalis)
simplex
Neumann,
H.
(0.)
simplicima
Hoogstraal
and
Was-
sef
(both
SA
species),
and
H.
(Sharifiella)
theilerae
Hoogstraal
(a
SP
species).
H.
(0.)
simplex
parasitizes
S.
setosus
in
different
ecological
zones
in
north-
western
lowland
and
mountain
forests
(excluding
rain
forests)
and
cul-
tivated
areas.
H.
(0.)
simplex
also
parasitizes
E.
telfairi
in
arid
southwestern
plains,
as
does
H.
(0.)
simplicima.
H.
(S.)
theilerae
infests
the
common
T.
ecaudatus,
and
infrequently
S.
setosus,
in
eastern
mountains
and
lowlands
from
northern
to
southern
Madagascar.
H.
(Elongiphysalis)
species
have
unique
multiple
lanceolate
coxal
spurs
for
grasping
coarse
hairs
and
spines
(Fig.
10.10).
Certain
trochantal
spurs
are
also
extraordinarily
developed
for
this
purpose.
H.
(E.)
elongata,
which
is
common
on
different
tenrec
species,
displays
a
wide
range
of
structural
variation
of
the
capitulum,
and
of
the
coxal
and
trochantal
spurs;
this
polytypic
species
perhaps
represents
a
diversification
process.
H.
(Ornithophysalis)
simplex,
which
has
minute
spurs
similar
to
those
of
most
bird-infesting
haemaphysalines,
successfully
coexists
on
S.
setosus
with
the
strikingly
spurred
H.
(E.)
elongata.
H.
(0.)
simplex
feeds
in
the
practically
hairless
ears
and
does
not
invade
the
spiny-coarse
pelage.
H.
(E.)
elongata,
on
the
other
hand,
feeds
chiefly
among
the
dorsal
spines
and
540
Acari
coarse
hairs
(Hoogstraal
1953).
H.
(0.)
simplicima
appears
to
be
a
rare
(per-
haps
unsuccessful)
species;
its
spurs
are
all
but
obsolete,
but
we
do
not
know
its
feeding
site
on
the
tenrec
host.
Among
the
20
species
of
Ornithophysalis,
11
parasitize
birds
or
birds
and
mammals
in
the
Oriental,
Australian,
Malagasy,
Palearctic,
and
Ethiopian
regions,
two
are
confined
to
Australian
marsupials,
two
to
Australian-New
Guinea
rodents,
two
to
Malagasy
tenrecs,
and
four
to
Oriental
rodents.
In
Madagascar,
H.
(0.)
madagascariensis
Colas-Belcour
and
Millot
is
a
parasite
of
a
large
ground-feeding
bird,
the
coucal.
In
northeastern
Australia
and
southeastern
New
Guinea,
H.
(0.)
doenitzi
Warburton
and
Nuttall
parasitizes
ground-feeding
birds.
These
lines
of
bird-infesting
ticks
appar-
ently
adapted
to
primitive
mammals
(marsupials
and
tenrecs
in
the
Austra-
lian
and
Malagasy
regions)
and
to
certain
rodents
(in
the
Australian
region)
at
an
early
period
in
mammalian
evolution.
H.
(Sharifiella)
theilerae
is
a
SP
species
and
apparently
the
least
successful
of
the
six
haemaphysaline
parasites
of
tenrecs.
The
primitive,
slightly
spe-
cialized
H.
(S.)
theilerae
competes
with
highly
specialized
H.
(Elongiphysalis)
species
which
thrive,
often
in
dense
clusters,
on
the
same
hosts.
If
ticks
of
the
SP
subgenera
Allophysalis,
Alloceraea,
Aboimisalis,
and
Sharifiella
had
become
extinct
before
our
time,
it
would
have
been
much
more
difficult
to
determine
the
steps
in
phylogeny
and
structural
adapta-
tions
of
Haemaphysalis
ticks
and
in
their
coevolution
with
mammals.
STRUCTURALLY
INTERMEDIATE
(SI)
HAEMAPHYSALINES
Subgenus
Herpetobia
Canestrini
The
subgenus
Herpetobia
Canestrini
(Hoogstraal
and
McCarthy
1965),
a
relict,
pivotal
branch
in
Haemaphysalis
phylogeny,
is
structurally
inter-
mediate
between
SP
and
SA
groups.
All
Herpetobia
immatures
and
adults
have
a
SA-pattern
rectangular
basis
capituli.
Their
palpi,
however,
which
are
compact,
but
are
slightly
salient
in
certain
nymphs,
represent
the
forerunner
of
the
broad
palpi
characterizing
SA
haemaphysalines.
Aside
from
these
critical
phylogenetic
characters,
the
four
Herpetobia
species
dif-
fer
quite
considerably
from
each
other
structurally
and
biologically.
The
type
species
of
the
subgenus,
H.
(H.)
sulcata
Canestrini
and
Fan-
zago,
ranges
from
Kashmir,
southern
USSR,
and
southwestern
Asia
to
Yemen
and
Sinai,
and
is
also
found
in
southern
Europe
(Grebenyuk
1966;
Aeschlimann
et
al.
1968;
Sacca
et
al.
1969;
Tovornik
and
Brelih
1973;
Rageau
1973;
Hoogstraal
and
Valdez
1980).
The
other
Herpetobia
species
occur
in
and
near
the
western
and
central
Himalayas.
These
are
H.
(H.)
kashmirensis
Hoogstraal
and
Varma
of
northern
India,
Pakistan,
and
Afghanistan
(Hoogstraal
and
McCarthy
1965)
(Figs.
10.19-10.22);
H.
(H.)
nepalensis
Hoogstraal
of
northern
India,
Nepal,
and
Tibet;
and
H.
(H.)
sundrai
Sharif
8
V..4
B
,
r!i:
I
a
C
D
Figure
10.19
Adult
Haemaphysalis
(Herpetobia)
kashmirensis.
(A,
B)
Male;
(C,
D)
female,
dorsal
and
ventral
views.
541
D
7
7
01
,
0
r
r'
-0-I
Ti
III
"-a
i
v
1
1
ti
TT
I
I
1/
L
'
p
7
7
542
L
M
N
III
a
ik.-
,s
4.,
d.
-
.
.—,,-
-1.-4
-
-•
I
E
E
-
fir
eflt,:.
.
lit'
-
-
T-
-
--
t
=.4,
.
i
4
•,-•
.
.
.-e
,
4E
-
"
----
_
,
•'
'
' !
t
'Jo
t .
-
-•
A
B
E
I0
E
Figure
10.21
Immature
Haemaphysalis
(Herpetobia)
kashmiremis.
(A,
B)
Nymph;
(C,
D)
larva,
dorsal
and
ventral
views.
Figure
10.20
Adult
1-faerrtaphysalis
(Herpetobia)
kashmirertsis.
(A—H)
Male:
(A,
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome;
(D)
genital
area;
(E)
spiracular
plate;
(F)
coxae
and
trochanters
I
to
IV;
(G)
femur
IV;
(11)
tarsi
I
to
IV.
(I—P)
Female:
(I,
J)
capitulum,
dorsal
and
ventral
views;
(K)
hypostome;
(L)
genital
area;
(M)
spiracular
plate;
(N)
coxae
and
trochanbars
I
to
IV;
(0)
femur
IV;
(P)
tarsi
I
to
IV.
This
structurally
intermediate
species
has
a
structurally
advanced
ba,i,
capihrli
but
adult
and
immature
palpi
are
essentially
compact
or
only
vertu'
slightly
broadened.
543
4
-6)
E
E
0
III
IV
C
B
E
E
0
G
/
I
II
H
K
J
Figure
10.22
Immature
Haemaphysalis
(Herpetobia)
kashmirensis.
(A—F)
Nymph:
(A,
B)
capitulum,
dorsal
and
ventral
views;
(C)
hypostome;
(D)
spiracular
plate;
(E)
coxae
and
trochanters
Ito
IV;
(F)
tarsi
Ito
IV.
(G—K)
Larva:
(G,
H)
capitulum,
dorsal
and
ventral
views;
(I)
hypostome;
(I)
coxae
and
trochanters
I
to
III;
(K)
tarsi
I
to
III,
showing
the
slight
palpal
broadening,
the
unusual
3/3
and
4/4
dental
formula
of
the
larva
and
nymph,
respectively,
and
absence
of
spurs.
544
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
545
of
northern
India
and
Nepal
(Dhanda
and
Bhat
1971)
[H.
(H.)]
himalaya
Hoogstraal
is
probably
a
junior
synonym
of
H.
(H.)
sundrai].
This
geo-
graphical-ecological
pattern
is
much
like
those
of
the
SP
subgenera
Al-
loceraea
and
Allophysalis;
the
western
lowland
dispersal
of
H.
(H.)
sulcata
recalls
that
of
H.
(A.)
inermis
in
the
SP
category.
The
many
structural
variations
in
samples
of
each
Herpetobia
taxon
[except
H.
(H.)
nepalensis]
indicate
the
need
for
laboratory
and
field
studies
to
settle
interrelated
biological-taxonomic
questions.
As
in
SP
subgenera,
numerous
Herpetobia
species
have
probably
become
extinct.
The
four
con-
temporary
Herpetobia
species
form
a
truncated
branch
illustrating
host-
related
structural
developments
which
subsequently
disappear
or
reappear
in
a
few
SA
groups.
The
SA
subgenus
Haemaphysalis
apparently
evolved
from
Herpetobia
and
spread
fanwise
eastward
through
tropical
forests
of
the
Oriental
region
and
into
the
temperate
eastern
Palearctic
region
(especially
the
USSR,
China,
Korea,
and
Japan).
Larval
Herpetobia
lack
cornua
and
discrete
coxal
spurs,
retaining
the
features
of
their
reptile-parasitizing
progenitors.
The
first
larval
palpal
ven-
tral
spur
is
seen
in
H.
(H.)
sundrai.
Immature
dental
formulae
are
conven-
tionally
2/2,
but
are
3/3
and
4/4
in
the
H.
(H.)
kashmirensis
larva
and
nymph
and
3/3
in
the
H.
(H.)
sundrai
nymph.
Herpetobia
nymphs
differ
in
their
degree
of
cornua
development,
palpal
salience,
chaetotaxy,
and
other
ways,
and
are
sensitive
indicators
of
interrelated
biological
and
mamma-
lian
host
factors
as
well
as
taxonomic
relationships.
Adult
Herpetobia
are
moderate
to
large
in
size
(male
length
2.8-4.0
mm),
though
individual
H.
(H.)
sulcata
may
be
smaller.
Their
cornua
are
moder-
ately
large
to
large
in
males
and
obsolete
or
small
in
females.
The
compact
adult
palpi
are
usually
ridged
posterodorsally
in
H.
(H.)
sulcata
and
H.
(H.)
kashmirensis
(an
evolutionary
experiment
that
failed
to
survive).
Each
species
except
H.
(H.)
nepalensis
has
a
prominent
but
quite
variable
ventral
spur
on
palpal
segment
3.
This
ventral
spur
is
exceptionally
variable
in
different
population
samples
of
H.
(H.)
sulcata,
but
short
and
broad
or
internally
directed
in
adults
of
other
Herpetobia
species.
The
4/4
dental
formulas
of
adult
H.
(H.)
sulcata
and
H.
(H.)
nepalensis
increase
to
5/5
to
7/7
in
the
other
species.
H.
(H.)
sulcata
male
coxal
spurs
(Fig.
10.9)
are
lanceol-
ate
on
IV,
a
moderately
large
hook
on
I,
and
conventionally
triangular
but
variable
in
size
on
II
and
III.
These
characters
are
common
among
male
haemaphysaline
parasites
of
Artiodactyla.
Female
coxal
spurs
of
H.
(H.)
sulcata
are
obsolete
to
moderate
in
size.
H.
(H.)
kashmirensis
male
coxal
spurs
are
hooklike
(Fig.
10.9),
and
female
spurs
are
either
hooklike
or
triangular;
those
of
H.
(H.)
sundrai
are
a
conventional
elongate
triangle
on
I
and
a
broad
triangle
on
II,
III,
and
IV.
In
H.
(H.)
nepalensis,
unusual
rounded
ridges
are
the
forerunners
of
the
spurs
of
other
species.
Herpetobia
female
external
genitalia
are
uniquely
indented
in
H.
(H.)
sulcata,
unusually
subcircular
in
H.
(H.)
nepalensis,
but
conventionally
rectangular
in
the
other
species.
These
and
other
unmentioned
unusual
and
variable
features
546
Acari
among
Herpetobia
adults,
and
differences
between
immature
and
adult
stage
structural
patterns,
suggest
a
wide
area
for
investigation
of
inter-
related
phylogenetic
and
host-adaptation
factors.
Ecologically,
Herpetobia
is
a
subgenus
of
temperate
open
forests,
steppes,
semideserts,
and
rocky
mountainsides.
Adult
Herpetobia
parasitize
wild
artiodactyls
(mouflon,
sambar
deer,
chital,
muntjac,
thar,
blackbuck,
yak,
cow-yak
hybrid,
etc.)
as
well
as
all
domestic
artiodactyls.
Other
hosts
are
uncommon.
Immature
H.
(H.)
nepalensis
and
H.
(H.)
sundrai
infest
the
same
hosts
as
adults.
Hosts
of
immature
H.
(H.)
kashmirensis
and
H.
(H.)
sulcata
differ
greatly
from
those
of
adults.
Larval
and
nymphal
H.
(H.)
kashmirensis
chiefly
infest
the
lizard
Agama
tuberculata.
We
have
a
record
of
both
imma-
ture
and
adult
H.
(H.)
kashmirensis
infesting
a
single
A.
tuberculata
in
north-
ern
India.
Hosts
of
immature
H.
(H.)
sulcata
include
numerous
lizards,
snakes,
and
tortoises,
birds
nesting
in,
on,
or
near
the
ground
(roller,
stonechat,
nuthatch,
lark,
sparrow,
etc.),
and
occasional
small-
or
medium-
sized
mammals.
There
are
records
(unpublished)
of
the
immature
and
adult
activity
of
H.
(H.)
nepalensis
of
the
Himalayas
from
each
month
of
the
year.
Adult
H.
(H.)
sulcata
are
generally
most
active
in
spring
and
fall,
and
immatures
from
spring
to
early
fall.
STRUCTURALLY
ADVANCED
(SA)
HAEMAPHYSALINES
The
11
SA
haemaphysaline
subgenera
contain
a
total
of
132
species.
The
basis
capituli
of
both
immatures
and
adults
in
this
group
is
rectangular
(never
expanded
laterally)
and
usually
bears
posterior
cornua.
The
palpi
of
immatures
and
adults
mostly
show
some
basal
broadening
of
segment
2;
some
retain
a
compact
(but
not
elongate)
form.
The
salience
begins
with
a
slight
extension
of
the
posterior
breadth
and
reaches
the
broadly
triangular
outline
characterizing
most
species
of
this
genus.
The
dental
formula
is
2/2
in
immatures
and
4/4
in
adults,
rarely
3/3
or
4/4
in
the
former,
and
occasion-
ally
3/3
or
5/5
to
7/7
in
the
latter.
Adults
vary
in
length
between
2.2
and
3.5
mm;
a
few
are
even
smaller;
but
very
few
exceed
3.5
mm.
All
of
these
132
species,
except
the
two
in
the
American
subgenus
Gonixodes,
occur
in
the
Old
World.
No
SA
populations
occur
above
1500
m
altitude
in
the
Himalayas
or
elsewhere,
and
few
reach
even
this
altitude.
Most
species
occur
in
humid,
wooded
zones.
The
few
species
that
inhabit
semiarid
environments
are
found
chiefly
in
littoral
zones,
floodplains
or
riparian
forests,
vegetated
valleys
or
foothills,
or
oases.
Of
the
132
SA
species,
six
parasitize
only
birds
and
seven
parasitize
birds
and
small-
or
medium-
sized
mammals
(see
subgenus
Ornithophysalis).
Three
species
of
the
sub-
genus
Haemaphysalis
chiefly
infest
mammals
but
also
feed
on
birds.
(Imma-
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
547
tures
of
one
Gonixodes
species
frequently
feed
on
birds
as
well
as
on
leporids.)
The
115
remaining
SA
haemaphysaline
species
have
coevolved
with
mammals
(chiefly
Artiodactyla
and
Carnivora,
also
Insectivora,
Hy-
racoidea,
Primates,
Lagomorpha,
and
Rodentia)
and
never
or
practically
never
parasitize
birds
or
reptiles.
The
structural
adaptations
and
radiation
of
SA
haemaphysaline
adults,
and
their
coevolution
with
mammals
should
be
studied
in
conjunction
with
Hoogstraal
and
Aeschlimann
(1982),
who
discuss
the
ticks
associated
with
each
mammalian
order
and
list
most
of
the
ticks
specific
to
each
order
or
family.
Haemaphysaline
host-adapted
structures
are
more
pronounced
in
males
than
in
females,
presumably
because
females
are
somewhat
larger,
and
possibly
stronger,
and
do
not
wander
on
the
host
in
search
of
several
mating
partners,
as
do
males.
These
adaptations
are
less
pronounced
in
nymphs,
and
even
less
so
in
larvae,
presumably
because
these
tiny
ticks
can
slip
between
the
host
hairs
and
do
not
have
to
"fight
their
way"
through
the
pelage
to
reach
a
feeding
site.
Subgenus
Ornithophysalis
Hoogstraal
and
Wassef
The
Ornithophysalis,
an
early
SA
assemblage
of
20
Old
World
species,
illus-
trates
(1)
phylogenetically
abrupt
palpal
basal
broadening
but
absence
or
mild
development
of
spurs
on
the
capitulum
(Figs.
10.7,
10.8),
coxae,
and
trochanters
(Fig.
10.9)
(characterizing
bird-infesting
haemaphysalines);
(2)
the
generally
slight
development,
if
any,
of
these
spurs
and
other
hair-
hooking
devices
in
species
parasitizing
the
phylogenetically
ancient
Mar-
supialia
and
two
species
parasitizing
the
tenrec
(Insectivora);
and
(3)
the
survival
of
Ornithophysalis
characters,
with
only
slight
modifications,
in
Oriental
species
adapted
to
Rodentia
(Hoogstraal
and
Wassef
1973).
Notably,
haemaphysalines
that
have
adapted
to
Rodentia
in
the
Ethio-
pian
region
are
members
of
the
subgenus
Rhipistoma,
probably
the
most
recent
of
haemaphysaline
subgenera,
in
contrast
to
Ornithophysalis,
one
of
the
earliest
types
of
SA
haemaphysaline,
which
has
no
members
confined
to
mammals
in
the
Ethiopian
region.
The
host
associations
of
the
20
Ornithophysalis
species
are
as
follows:
Birds—H.
(0.)
doenitzi
Warburton
and
Nuttall;
H.
(0.)
phasiana
Saito,
Hoogstraal
and
Wassef;
H.
(0.)
madagascariensis
Colas-Belcour
and
Millot;
H.
(0.)
hoodi
Warburton
and
Nuttall;
H.
(0.)
megalaimae
Rajagopalan
(Figs.
10.8,
10.9);
H.
(0.)
minuta
KohIs.
Birds
and
marsupials—H.
(0.)
bremneri
Roberts
(Figs.
10.8,
10.9).
Marsupials—H.
(0.)
petrogalis
Roberts;
H.
(0.)
lagostrophi
Roberts.
Tenrecs
(Insectivora)—H.
(0.)
simplex
Neumann
(Fig.
10.10);
H.
(0.)
simplicima
Hoogstraal
and
Wassef.
Birds
and
small-sized
mammals
(chiefly
rodents)—H.
(0.)
howletti
Warburton;
H.
(0.)
humerosa
548
Acari
Warburton
and
Nuttall;
H.
(0.)
ornithophila
Hoogstraal
and
Kohls;
H.
(0.)
tauffliebi
Morel;
H.
(0.)
pavlovskyi
Pospelova-Shtrom.
Rodents—H.
(0.)
ban-
dicota
Hoogstraal;
H.
(0.)
sciuri
Kohls;
H.
(0.)
kadarsani
Hoogstraal;
and
H.
(0.)
ratti
Kohls.
H.
(0.)
minuta,
known
only
from
birds,
is
one
of
the
smallest
ixodid
species.
It
has
a
typical
Ornithophysalis
facies
but
exceptional
(for
this
sub-
genus)
spurs
on
the
palpi,
coxae,
and
trochanters.
This
exception
supports
a
well-founded
generalization:
the
smaller
the
size
of
the
adult
tick
(espe-
cially
those
of
medium-sized
and
large-sized
hosts)
the
more
luxurient
are
certain
of
its
spurs
(and
often
the
more
atypical
is
its
life
cycle).
H.
(0.)
humerosa
is
extraordinarily
modified
for
slipping
between
bird
feathers
or
mammal
hairs;
it
has
an
extremely
narrowly
elongate
(louselike)
body
(see
Roberts
1970;
Fig.
39).
Hair-hooking
devices
are
virtually
absent
in
H.
(0.)
humerosa;
the
cornua
are
small,
all
other
spurs
are
minute
or
obsolete.
A
tendency
toward
narrow
and
elongate
bodies
also
occurs
in
the
tenrec
parasite
H.
(E.)
elongata
(but
here
the
spurs
are
extreme)
and
in
the
African
carnivore
parasite
H.
(Rhipistoma)
leachi
and
related
species.
Ornithophysalis,
with
its
broad
palpi,
appears
to
have
evolved
abruptly
from
SP
subgenera
with
compact
palpi
[see
H.
(Aboimisalis)
punctata]
when
birds
and
mammals
replaced
reptiles
as
the
world's
dominant
verte-
brates.
Significantly,
of
the
20
contemporary
Ornithophysalis
species,
six
parasitize
only
birds,
five
parasitize
both
birds
and
various
mammals,
three
parasitize
birds
and
marsupials
or
only
marsupials,
two
parasitize
only
tenrecs,
and
four
parasitize
Oriental
or
Australian
rodents.
The
only
haemaphysalines
which
specifically
parasitize
the
phylogenetically
ancient
tenrecs
(Insectivora)
are
the
SP
species
H.
(Sharifiella)
theilerae
and
the
three
SA
species
constituting
the
subgenus
Elongiphysalis,
which
represents
a
highly
specialized
branch
from
Ornithophysalis.
Except
for
the
few
species
of
the
subgenus
Haemaphysalis
that
parasitize
birds
as
well
as
mammals,
all
other
SA
haemaphysaline
adults
are
specific
to
mammals
and
never
feed
on
birds,
although
immatures
of
a
few
SA
species
may
infest
birds.
The
four
contemporary
Ornithophysalis
species
specific
to
Oriental
and
Austra-
lian
rodents
suggest
an
early
association
between
these
ticks
and
mammals
in
the
Oriental
and
Australian
regions
and,
together
with
other
evidence,
with
the
origin
of
the
genus
Haemaphysalis
in
the
Oriental
region.
The
Australian
and
Oriental
marsupial-
and
rodent-infesting
species
probably
evolved
from
species
like
the
contemporary
bird-parasitizing
H.
(0.)
doenitzi
of
the
Oriental
region
and
eastern
New
Guinea
and
Australia.
The
Malagasy
tenrec-parasitizing
species
probably
evolved
from
species
like
the
contemporary
bird
(coucal)-infesting
H.
(0.)
madagascariensis.
H.
(0.)
tauffliebi,
which
parasitizes
both
birds
and
small-
or
medium-sized
mam-
mals
in
the
Ethiopian
region,
probably
evolved
from
a
species
similar
to
the
common
bird-parasitizing
H.
(0.)
hoodi
of
this
region.
It
is
probably
significant
phylogenetically
that
the
"basic"
Oriental-Australian,
Mala-
gasy,
and
Ethiopian
bird-parasitizing
Ornithophysalis
(doenitzi,
madagas-
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
549
cariensis,
hoodi)
are
difficult
to
distinguish
from
each
other
but
that
no
such
problem
is
presented
by
the
closely
related,
more
geographically
restricted,
species
that
parasitize
certain
birds
or
both
birds
and
small
mammals.
Subgenus
Haemaphysalis
Koch
The
subgenus
Haemaphysalis
apparently
evolved
from
Herpetobia
(or
a
re-
lated,
now
extinct
ancestor)
in
the
Indian
subregion
of
the
Oriental
region
and
fanned
southeastward
into
the
Oriental
region
and
northeastward
into
the
Palearctic
region.
The
type
species
of
the
subgenus,
H.
(H.)
concinna
Koch,
also
ranges
westward
in
wooded
zones
from
Japan
to
northern
Iran,
Italy,
and
France.
The
subgenus
Haemaphysalis
contains
16
contemporary
species
[including
H.
(H.)
japonica
Warburton
(Fig.
10.8)
with
two
subspecies]
in
six
species
groups.
Four
species
in
three
groups
(flava,
campanulata,
and
bir-
maniae
groups)
remain
in
the
Indian
subregion
[one
of
these
four
species,
H.
(H.)
campanulata
Warburton,
is
also
found
in
the
eastern
Palearctic
re-
gion];
there
are
two
related
species
elsewhere
in
the
Oriental
region
and
six
related
species
in
the
eastern
Palearctic
region.
A
few
of
the
Palearctic
species
also
occur
in
northern
mountains
of
the
Oriental
region.
Two
groups
(concinna
and
japonica
groups)
with
three
species
are
Palearctic.
The
sixth
group,
with
a
single
species,
H.
(H.)
silacea
Robinson,
is
a
relict
in
southeast
Africa
(Ethiopian
region)
(Hoogstraal
1963).
Wild
and
domestic
Artiodactyla
(various
deer,
wild
pigs,
the
Serow,
Goral,
Blackbuck,
etc.)
are
the
chief
hosts
of
most
adults
(11
of
the
16
species)
of
the
subgenus
Haemaphysalis.
Carnivora
are
secondary
hosts
of
some
of
these
11
species.
Adults
of
the
three
members
of
the
campanulata
group
are
not
restricted
to
Artiodactyla.
H.
(H.)
campanulata
parasitizes
carnivores
and
also
ar-
tiodactyls
in
Japan,
Korea,
northeastern
China,
the
USSR,
and
southern
India.
H.
(H.)
pentalagi
Pospelova-Shtrom
parasitizes
the
Japanese
Black
Rabbit
(Pentalagus)
in
the
Amami
Group,
Japan
(Hoogstraal
and
Yamaguti
1970).
H.
(H.)
verticalis
Itagaki,
Noda
and
Yamaguchi
parasitizes
the
Suslik
(Citellus)
and
Jird
(Meriones)
in
northeastern
China
(Emel'yanova
and
Hoogstraal
1973).
Host
data
for
the
flava
group
are
limited.
H.
(H.)
indoflava
Dhanda
and
Bhat
(Himalayan
region
and
Madras
of
India)
are
recorded
from
dogs,
and
others
are
from
the
jackal,
fox,
wild
pig,
cattle,
and
man.
The
immature
stages
are
unknown.
Adult
H.
(H.)
flava
Neumann
infest
wild
and
domestic
carnivores
as
well
as
Artiodactyla
(wild
pigs,
deer,
cattle)
in
Japan,
Korea,
the
eastern
USSR,
and
China.
The
third
member,
H.
(H.)
megaspinosa
Saito,
parasitizes
Artiodactyla
(wild
pigs,
deer,
Serow)
in
Japan.
Immatures
of
the
artiodactyl-
and
carnivore-parasitizing
species
gener-
ally
feed
on
rodents
and
also
on
hedgehogs.
Immatures
of
the
widely
distributed
H.
(H.)
concinna
(Japan
to
France)
also
frequently
infest
ground-
550
Acari
feeding
birds
and
are
the
only
ones
of
this
subgenus
known
to
do
so.
Immatures
and
adults
of
the
rabbit
and
rodent
parasites
H.
(H.)
pentalagi
and
H.
(H.)
verticalis
feed
on
the
same
hosts.
The
basis
capituli
of
each
stage,
except
some
larvae,
bears
moderate
to
fairly
large
cornua.
Small
but
distinctive
ventral
cornua
are
present
in
im-
matures
of
H.
(H.)
indoflava
and
H.
(H.)
birmaniae,
and
also
appear
in
a
less
developed
form
in
the
immatures
of
a
few
other
species
in
this
sub-
genus.
Ventral
cornua
are
rare
in
the
genus
Haemaphysalis
but
reappear
in
immatures
of
both
species
of
Gonixodes
and
in
adults
of
H.
(G.)
leporispalus-
tris.
Immature
H.
(H.)
birmaniae
are
also
unusual
in
that
they,
like
adults,
parasitize
Artiodactyla
(rather
than
Rodentia).
The
functional
adaptation
of
ventral
cornua
in
relation
to
the
hosts
of
adults
and/or
immatures
in
which
they
appear
should
be
investigated.
Unfortunately,
immature
H.
(H.)
in-
doflava
are
unknown.
Palpi
of
Haemaphysalis
immatures
and
adults
are
only
slightly
advanced
from
the
compact
form
characterizing
Herpetobia
[and
the
SP
group
H.
(A.)
punctata;
see
H.
(H.)
japonica
in
Fig.
10.8].
These
palpi
are
slightly
more
elongate,
either
broader
posteriorly
(as
in
some
Herpetobia
nymphs)
or
campanulate
with
a
moderate
posterior
flange,
but
are
not
broadly
ex-
panded
(as
in
Ornithophysalis,
Elongiphysalis,
and
Rhipistoma)
except
in
H.
(H.)
verticalis,
the
Japanese
Black
Rabbit
parasite.
Ventral
spurs
of
palpal
segment
3
are
mostly
moderately
large,
but
are
small
in
H.
(H.)
megaspi-
nosa,
in
which
the
exceptionally
large
coxal
IV
spur
apparently
compen-
sates
for
the
small
palpal
spur.
Except
for
the
ventral
spur
of
segment
3
and
some
posterior
broadening,
the
palpi
of
the
subgenus
Haemaphysalis
are
not
specialized
for
mammal-
hair
hooking—with
a
single
unique
exception.
The
H.
(H.)
concinna
palpal
segment
3,
especially
that
of
the
male,
is
remarkable
(Fig.
10.8).
The
inter-
nal
margin
of
each
segment
3
is
uniquely
concave
so
that
the
two
palpi
can
surround
a
hair
and
function
as
a
hair-grasping
device.
This
host-adaptive
feature,
as
well
as
the
ability
of
H.
(H.)
concinna
immatures
to
parasitize
birds,
may
contribute
to
the
fact
that
this
species
is
"the
most
successful"
(most
widely
distributed
and
prevalent)
in
this
subgenus,
which
consists
of
mostly
uncommon
and
geographically
restricted
species.
Adult
coxal
spurs
are
reduced
in
the
rabbit-
and
rodent-parasitizing
species
of
the
subgenus
Haemaphysalis.
The
coxa
I
spur
of
the
artiodactyl
and
carnivore
parasites
is
usually
quite
large,
and
the
II,
III,
and
IV
spurs
are
variable
(small
to
large).
However,
in
both
sexes
of
H.
(H.)
megaspinosa,
the
IV
spurs
are
very
large.
In
male
H.
(H.)
flava,
the
IV
spur
is
lanceolate
as
in
a
few
species
of
Aboimisalis
and
Herpetobia
and
others
which
we
discuss
later.
The
female
H.
(H.)
flava
IV
spur
is
larger
than
usual.
The
trochanters
do
not
bear
ventral
spurs
in
many
Haemaphysalis
species,
but
do
so
on
leg
I
in
H.
(H.)
concinna
(d),
H.
(H.)
flava
(d,
.9),
and
one
or
both
sexes
of
the
birmaniae
group:
birmaniae;
darjeeling
Hoogstraal
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
551
and
Dhanda;
goral
Hoogstraal;
traubi
KohIs;
roubaudi
Toumanoff;
filippovae
Bolotin.
Possibly
owing
to
the
limited
range
of
its
palpal
and
other
functional
adaptations
for
coevolution
with
artiodactyls
and
carnivores,
the
subgenus
Haemaphysalis
in
itself
[except
H.
(H.)
concinna]
does
not
include
an
out-
standingly
successful
assemblage
of
Haemaphysalis
ticks.
H.
(H.)
silacea
is
treated
here
following
the
overview
of
the
Oriental
and
Palearctic
members
of
the
subgenus
Haemaphysalis
because
of
its
relict
status
in
the
fauna
of
southeast
Africa
(Zululand
and
eastern
Cape
Prov-
ince).
Structurally
and
biologically
this
species
does
not
stand
apart
from
the
ordinary
members
of
the
subgenus
Haemaphysalis
(Hoogstraal
1963)
except
that
its
adults
infest
a
greater
variety
of
hosts
than
do
the
Oriental
and
Palearctic
species.
Hosts
of
the
silacea
adults
are
antelopes,
livestock,
mongooses,
hares,
and
birds.
H.
(H.)
silacea
immature
stages
are
known
only
from
laboratory-reared
specimens.
Together
with
the
bird-
parasitizing
H.
(Ornithophysalis)
hoodi
and
the
bird-
and
mammal-
parasitizing
H.
(0.)
tauffliebi,
this
is
probably
the
most
ancient
form
of
SA
haemaphysaline
in
the
Ethiopian
region
and
represents
a
Gondawanian
relict.
Subgenus
Gonixodes
Duges
The
two
members
of
the
subgenus
Gonixodes—H.
(G.)
leporispalustris
(Pack-
ard)
(Alaska
to
Argentina)
and
H.
(G.)
juxtakochi
Cooley
(Mexico
to
Argen-
tina)—are
the
only
SA
haemaphysalines
of
the
Nearctic
and
Neotropical
regions.
[Sketches
of
both
species
appear
in
Cooley
(1946);
the
H.
kochi
Aragao
in
the
Cooley
report
is
a
preoccupied
name
and
synonymous
with
H.
juxtakochi.]
Gonixodes
apparently
evolved
from
the
subgenus
Haemaphy-
salis
(or
a
related
extinct
branch).
Both
Gonixodes
species
have
a
typical
SA
basis
capituli.
Adult
and
immature
H.
(G.)
leporispalustris
and
immature
H.
(G.)
juxtakochi
also
have
unusual
ventral
cornua,
which
we
first
observed
in
some
species
of
the
subgenus
Haemaphysalis.
The
campanulate
palpi
are
rather
broadly
expanded
posteriorly
in
H.
(G.)
leporispalustris
but
rather
elongate
and
only
slightly
expanded
in
H.
(G.)
juxtakochi.
The
palpal
seg-
ment
3
ventral
spur
is
short
and
internally
directed
(bird-parasitizing
type)
in
H.
(G.)
leporispalustris,
whose
armatures
parasitize
birds,
leporids,
and
less
often
other
small
mammals,
whereas
adults
are
restricted
to
leporids.
These
palpal
spurs
are
exceptionally
strong
in
adult
H.
(G.)
juxtakochi,
and
strong
in
immatures.
Most
coxal
spurs
in
this
subgenus
are
rather
well
developed
or
quite
large
[coxa
I
spur
of
male
and
nymphal
H.
(G.)
jux-
takochil.
Adult
H.
(G.)
juxtakochi
chiefly
parasitize
Neotropical
deer
(Mazama);
immatures
primarily
parasitize
these
deer
and
the
agouti
(Dasy-
procta:
Rodentia).
The
great
differences
in
spur
development
of
these
two
species
are
obviously
associated
with
the
bird
feathers
and
leporid
pelage
552
Acari
invaded
by
H.
(G.)
leporispalustris
and
with
the
coarser
pelage
of
the
deer
hosts
by
H.
(G.)
juxtakochi.
Subgenus
Kaiseriana
Santos
Dias
Kaiseriana
consists
of
33
species
[subspecies
attributed
to
H.
(K.)
cornigera
are
tentatively
considered
as
full
species].
Adults
are
structurally
special-
ized,
some
extremely,
for
parasitizing
Artiodactyla;
most
also
feed
on
Car-
nivora,
but
other
hosts
are
exceptional.
Immatures
parasitize
small
mam-
mals,
especially
Rodentia,
and
those
of
a
few
species
feed
on
Artiodactyla
and
Carnivora
as
well
as
Rodentia.
Only
immatures
of
the
biologically
distinctive
H.
(K.)
longicornis
Neumann
occasionally
parasitize
birds.
Most
Kaiseriana
species
have
been
illustrated
and
described
or
redescribed
by
Hoogstraal
in
the
Journal
of
Parasitology
since
1963;
thus
to
save
space,
we
omit
the
names
of
taxon
authors
and
give
this
subgenus
rather
less
atten-
tion
than
it
deserves
in
relation
to
coevolution
with
mammals.
Twenty-seven
of
the
33
Kaiseriana
species
are
Oriental
in
distribution
[three
of
these
(hystricis,
mageshimaensis,
yeni)
extend
into
the
eastern
Palearctic
and
one
(bancrofti)
extends
into
Australia
and
New
Guinea];
two
are
eastern
Palearctic
(ias,
longicornis);
one
(novaeguineae)
is
Australian-
Papuan;
and
three
(aciculifer,
parmata,
rugosa)
are
Ethiopian.
The
three
Kaiseriana
species
in
Australia-New
Guinea
require
special
consideration
owing
to
the
absence
of
native
Artiodactyla
and
Carnivora
in
this
region.
H.
(K.)
longicornis
(bispinosa
group)
was
introduced
into
Austra-
lia
with
cattle
from
northeastern
Asia
within
the
last
100
years
(Hoogstraal
et
al.
1968).
H.
(K.)
novaeguineae
(cornigera
group)
of
New
Guinea
and
Aus-
tralia
is
unknown
elsewhere;
we
suggest
that
Oriental
populations
either
remain
to
be
discovered
(probably
in
the
Indonesian
archipelago)
or
be-
came
extinct
after
novaeguineae
was
introduced
with
domestic
pigs
or
deer
into
New
Guinea
and/or
Australia.
H.
(K.)
bancrofti
(hylobatis
group)
is
known
only
from
a
single
authenticated
collection
(unpublished)
from
the
Oriental
region
(vegetation,
Java)
but
is
common
on
livestock,
kangaroos,
and
other
marsupials,
and
birds
in
certain
coastal
areas
of
Australia
and
New
Guinea.
Livestock
or
birds
probably
introduced
bancrofti
into
the
Aus-
tralian
region.
H.
(K.)
bancrofti
is
closely
related
to
only
one
other
species,
hylobatis,
a
seldom-seen
Indonesian-Malaysian
species
with
host
data
re-
markably
atypical
for
the
rather
strictly
host-specific
subgenus
Kaiseriana.
Our
records
of
adult
hylobatis
(unpublished)
are
from
wild
pigs
(Sus)
(two
collections),
a
Langur
monkey
(Presbytis)
(one),
the
Banded
civet
(Arctictis)
(one),
a
rodent
(Rattus)
(one),
a
gymnure
(Hylomys:
Insectivora:
Erinaceidae)
(one),
a
domestic
dog
(one),
humans
(two),
a
ground-
frequenting
bird
(Centropus)
(one),
and
vegetation
(eight).
Our
three
collec-
tions
of
immatures
are
from
human
(one),
Rattus
(one),
and
vegetation
(one).
An
atypical
host-related
biological
pattern,
like
this
one
of
hylobatis,
may
be
the
reason
why
the
related
bancrofti
is
not
known
outside
the
Tick
and
Mammal
Coevolution,
with
Emphasis
on
Haemaphysalis
553
Australian
region,
except
for
our
single
collection
from
forest
vegetation
on
Java
(Oriental
region).
The
hallmark
of
Kaiseriana
is
a
hair-hooking
spur
extending
from
the
posterodorsal
margin
of
the
adult
palpal
segment
3
(Hoogstraal
et
al.
1965)
(Fig.
10.8:
lagrangei,
shimoga,
cuspidata,
yeni).
In
cornigera
group
males
this
spur
is
supplemented
or
replaced
by
a
gap
in
the
external
surface
of
the
palpus
(Fig.
10.8:
shimoga);
this
efficient
hair-grasping
gap
is
formed
by
the
broad
posterior
expansion
and
apical
recurvature
of
the
movable
segment
3
and
the
anterior
narrowing
of
segment
2.
The
generally
small,
often
frail
cornigera
group
adults
have
moderately
to
very
large
cornua
on
the
basis
capituli,
an
extraordinary
variety
of
hair-hooking
devices
on
the
greatly
broadened
palpi
(Fig.
10.8),
and
pronounced
spurs
on
most
or
all
coxae.
The
coxa
IV
spur
is
lanceolate
in
spinigera
(Fig.
10.9),
novaeguineae,
aciculifer,
and
rugosa;
double
(scissorlike)
in
anomala
(Fig.
10.9),
cornigera,
shimoga
taiwana,
and
ias;
and
a
combined
short
and
large
(lanceolate)
spur
in
psalis-
tos.
Notably,
in
the
West
African
rugosa,
the
species
most
distant
from
the
Oriental
origin
of
the
cornigera
group,
the
palpi
are
campanulate,
and
the
posterodorsal
margin
of
palpal
segment
3
is
uniquely
recurved
internally
rather
than
medially
spurred
(Hoogstraal
and
El
Kammah
1972).
Asian
adults
of
the
cornigera
group
are
chiefly
associated
with
deer
(Sam-
bar,
Sika,
Chital,
Timor
Deer,
Muntjac,
etc.),
and
also
with
wild
bovines
(Guar,
Anoa,
Banteng,
Serow,
etc.)
and
wild
pigs
(Sus
species).
A
few
adults
parasitize
wild
carnivores
and
the
domestic
dog
and
man.
The
African
members
(aciculifer
and
rugosa)
parasitize
numerous
artiodactyls
(Bush-
buck,
Sitatunga,
Reedbuck,
Waterbuck,
Kob,
Impala,
Hartebeest,
Oribi,
Gazelle,
Duiker,
Dik-dik,
Buffalo,
etc.)
and
infrequently
carnivores.
Asian
and
African
domestic
cattle
and
other
livestock
are
infested
when
feeding
in
the
vicinity
of
wild
hosts
of
cornigera
group
ticks.
Thus
cattle
introduced
into
previously
unspoiled
biotopes
account
for
greater
population
densities
of
anomala
in
Uttar
Pradesh
and
Himachel
Pradesh
(Hoogstraal
et
al.
1967,
1972);
of
spinigera,
the
chief
vector
of
Kyasanur
Forest
disease
virus
(To-
gaviridae:
Flavivirus),
in
Karnataka,
India
(Hoogstraal
1981);
and
of
aciculifer
in
Africa
(unpublished).
Kaiseriana
species
(nadchatrami
group)
with
only
moderately
broadened
campanulate
adult
palpi
(as
in
the
subgenus
Haemaphysalis),
but
with
a
small
dorsal
spur
on
segment
3
(signifying
the
subgenus
Kaiseriana),
ap-
pear
to
have
coevolved
with
wild
pigs
(Sus
species),
which
are
still
abun-
dant
in
many
Oriental
forests.
In
the
nadchatrami
group
(nadchatrami,
semer-
mis,
kinneari,
papuana,
susphilippensis),
cornua
and
coxal
spurs
are
unenlarged.
Adults
of
this
group
infest
other
artiodactyls
and
carnivores
but
apparently
prosper
best
where
there
are
populations
of
pigs.
The
vir-
tual
lack
of
hair-hooking
devices
in
pig-parasitizing
haemaphysalines
is
correlated
with
the
hosts'
sparse
hairs,
which
offer
no
obstacles
to
tick
movement
toward
a
feeding
and
mating
site.
Other
Kaiseriana
species
(bispinosa
group)
have
campanulate
adult
palpi
554
Acari
like
those
of
the
pig-associated
species
(nadchatrami
group),
but
they
have
larger
dorsal
and
ventral
spurs
on
segment
3,
a
distinctively
elongate
spur
on
coxa
I,
fairly
large
spurs
often
present
on
the
other
coxae,
and
a
distinct
ventral
spur
on
trochanter
I
(Figs.
10.8,
10.9:
lagrangei,
cuspidata,
yeni).
The
bispinosa
group
evolved
together
with
Oriental
and
eastern
Palearctic
deer,
antelopes,
and
wild
cattle;
its
species
are
bispinosa,
ramachandrai,
renschi,
lagrangei,
davisi,
luzonensis,
longicornis,
mageshimaensis,
yeni,
aculeata,
bar-
neata,
and
cuspidata.
Adults
of
the
bispinosa
group
may
infest
carnivores
and
other
medium