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The structure and function of thetarsus I sensillar field in mites of thegenus Halarachne (Halarachnidae:Gamasida)P.J.A. Pugh aa British Antarctic Survey, Natural Environment ResearchCouncil, High Cross, Madingley Road, Cambridge, CB3 0ET, UKPublished online: 17 Feb 2007.

To cite this article: P.J.A. Pugh (1996) The structure and function of the tarsus I sensillar fieldin mites of the genus Halarachne (Halarachnidae: Gamasida), Journal of Natural History, 30:7,1069-1086, DOI: 10.1080/00222939600770571

To link to this article: http://dx.doi.org/10.1080/00222939600770571

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JOURNAL OF NATURAL HISTORY, 1996, 30, 1 0 6 9 - 1 0 8 6

The structure and function of the tarsus I sensillar field in mites of the genus Halarachne (Halarachnidae: Gamasida)

P. J. A. PUGH

British Antarctic Survey, Natural Environment Research Council High Cross, Madingley Road, Cambridge CB3 0ET, UK

(Accepted 12 May 1995)

The sensillar field on tarsus I of Halarachne (Halarachnidae: Gamasida), a respiratory tract endoparasite of seals (Pinnipedia) is associated with 12 hair- or peg-like receptor sensilla in the larva and 13 or 14 in the adult. These include thermo-/hygroreceptors, each with a double wall traversed by 3 or 4 slit-like pores (dw/WP-sensilla), olfactory chemoreceptors of small inorganic molecules, each with a single wall spanned by several small and simple pores (sw/WP-sensilla), gustatory chemoreceptors with a single terminal pore (TP-sensilla), and aporous NP-sensilla which have thermoreceptive and/or other unknown functions. Some sensilla are sessile and others socketed, the latter having a possible additional/alternative mechanoreceptive function. One mechanoreceptor is a probable trichobothrium-like vibration receptor which has not been previously described in the Anactinotrichida. This range of sensilla combined with the absence of sw/WP-sensilla, i.e. olfactory chemoreceptors covered with numerous, large centrally-plugged pores, suggests that although Halarachne spp. can locate large endothermic animals, they lack the ability to discriminate between different species.

KEYWORDS: Acari, Halarachne, receptor morphology, sensilla, parasite.

Introduction Legs, and in particular the first pair of legs, are important sensory appendages in

the Acarina. Among the anactinotrichid mites (Opilioacarida, Holothyrida, Ixodida and Gamasida), the podomeric morphology and articulation gives leg I an antenniform appearance, while the antenna like function is provided by the surface ornamentation of numerous sensory setae ( = sensilla, singular sensiltum) (Evans, 1963, 1992; Sabelis, 1981; Wooley, 1988). Leg I sensory reception has been particularly studied in the ticks (Ixodida) which gather exogenic stimuli from Haller 's organ, an array of sensilla on the dorsal surface of tarsus I (Sonenshine, 1991). Haller 's organs have antenna-like attributes in that they can for example detect certain chemicals and other cues at long range while normal behaviour, particularly host location, is dependent upon their integrity and function (Lees, 1948, Holscher et al., 1980; Waladde and Rice, 1982).

Although Haller 's organ is unique to ticks, arrays of tarsal I sensilla occur throughout the Acarina (Haarlcv, 1943; Hughes 1959; van der Hammen, 1961, 1965, 1966, 1989; Evans, 1968, 1992; Bostanian and Morrison, 1973; Coons and Axtell, 1973; Mills, 1974; Egan, 1976; Jagers op Akkerhuis et al., 1985). In the Gamasida, particularly complex sensillar arrays have been recorded on tarsus I in two families, namely the Spinturnicidae which infest bats (Chiroptera) (HaarlCv, 1943; Evans, 1968),

0022-2933/96 $12"00 © 1996 Taylor & Francis Ltd.

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1070 P . J . A . Pugh

and the Halarachnidae, which are respiratory tract endoparasites of seals and primates (Oudemans, 1926; Finnegan, 1934; HaarlCv, 1943; Newell, 1947; Gretillat, 1959a, 1959b; Popp, 1961; Domrow, 1962).

The family Halarachnidae comprises three genera, of which two are parasites of seals (Pinnipedia), with Halarachne infesting true seals (Phocidae), Ortholarachne infecting walruses (Odobaenidae), fur seals and sealions (Otariidae), while the third genus, Pneumonyssus, parasitizes non-human primates. Adults of Halrachne and Orthohalarachne anchor themselves, via their tarsal claws, to the lining of the anterior nasopharaynx and choanae in the nasal passages of their pinniped hosts, while Pneumonyssus is associated with lesions within the primate lung (Chandler and Ruhe, 1940; Hughes, 1959; Hull, 1970; Kim and Bang, 1970; Yunker, 1973; Kurochkin and Sobolewsky, 1975).

The life cycles of both Halarachne and Orthohalarachne comprise the four stages typical of the Gamasida; but the protonymph, deuteronymph and dioceous adults are non-motile (Evans et aL, 1961; Krantz, 1978, Evans and Till, 1979). Only the larva is mobile and able to seek a new attachment site within the same host, or, during nose-to-nose social contact between seals, infect a new host (Newell, 1947; Gretillat, 1959a, 1959; Dahme and Popp, 1961; Kurochkin and Sobolewsky, 1975).

Host location in larval Halarachnidae is supposedly mediated via the 'sinnenfeld' ( = sensory field) or tarsal organ (Oudemans, 1926; Haarlov, 1943), a flat area on the distal dorsal surface of tarsus I which bears several sensilla. This structure, hereafter referred to as the 'sensillar field', has been illustrated numerous times, but never examined in detail. The present scanning electron microscope (SEM)-based investiga- tion will appraise the structure and possible function(s) for each sensillum within the sensillar field of Halarachne. The implications of these observations particularly with regard to host location will then be discussed.

Materials and methods Larvae and adult females of Halarachne halichoeri Allman were obtained during

post mortem examination of grey seal, Halichoerus grypus Fabricius (Phocidae), carcasses stranded on British beaches. All mites were collected, fixed and subsequently washed in several changes of 70% ethanol. Some were then hydrated to distilled water, placed in 20% aqueous glycerol with ca 1% Decon 90 (Decon Laboratories, Hove, England), cleaned in an ultrasonic bath, washed in distilled water and dehydrated to absolute ethanol. The remaining specimens were not cleaned but dehydrated directly from 70% ethanol. Both cleaned and non-cleaned mites were transferred to absolute acetone via an ethanol/acetone series and critical point dried using liquid carbon dioxide.

Whole specimens, and detached first legs of the same, were mounted on aluminium stubs using double-sided adhesive carbon discs (Agar Scientific Ltd.), gold coated in a Bio-Rad SC502 sputter coating unit, examined and photographed in a model S-360 Leica SEM. Low magnification images were obtained using an acceleration voltage of 10kV, probe current of 200pA, working distance of 10-15ram and the in-built electronic frame store. Higher magnification/resolution pictures were obtained using 6-9 kV, 20-40 pA, 4-7 mm and recorded as live images directly from the record screen.

Some larvae were subsequently placed in an FEI 611 focused ion beam (FIB) 611 machine, in which some of their sensiUar field sensilla were severed via precision ion milling. In this procedure, a 6nA beam of gallium ions was focused into a spot of 50--400nm diameter and scanned over a line (line milling) or a user-defined box

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Tarsus I sensillar field in Halarachne 1071

(peg-milling) positioned as to sever individual sensilla and thus reveal their internal morphology (Young et al., 1993). Milled specimens were removed from the FIB machine, re-coated with gold, and returned to the SEM for examination and photography.

Larvae of Halarachne miroungae Ferris were collected from chemically anaes- thetized adult southern elephant seals, Mirounga leonina L. (Phocidae: Pinnipedia) at Husvik Harbour, South Georgia, during a study on elephant seal diving behaviour (Boyd and Arnbom, 1991). Quantities of mucus containing H. miroungae larvae were removed from the external nares of the immobilized seals using a small spoon and placed in a sealed polythene container. The mucus was subsequently transferred to coarse tissue paper in a plastic tray and placed under a bright light. The mite larvae crawled away from the light and into the tissue, cleaning themselves of much adherent mucus and other debris before being transferred via a fine paint brush on to clean tissue paper and sealed in a polythene container, where cleaning was continued for a further 24h. Specimens were subsequently fixed in alcoholic Bouin's solution further 24h. Specimens were subsequently fixed in alcoholic Bouin's solution (Grimstone and Skaer, 1972), returned to the UK at ca 4°C and prepared for and observed in the SEM in the same manner as those of H. halichoeri.

Results and discussion

Sensillar structure The number of sensilla differs between species and life stage. For example:

O. chabaudi Gretillat and O. letalis Popp larvae have 11; H. halichoeri and H. miroungae larvae, H. mageUanica Finnegan and O. chabuadi females, 12; H. halichoeri, O. diminuata (Doetschmann) and O. zalophi (Oudemans) larvae and females, 13; H. americana Banks and O. attenuata (Banks) females, 14 (Kramer, 1885; Finnegan, 1934; HaarlCv, 1943; Newell, 1947; Gretillat, 1959a, 1959b; Popp, 1961; present study). These numbers are comparable with those in the ixodid Haller's organ, but are very low relative to the 10(0-60000 sensilla on the insect antenna (Steinbrecht, 1987). The halarachnid sensillar array may be described via a schematic similar to that applied to the ixodid tick Haller's organ (Axtell et al., 1973), while the 'normal' (i.e. ad, al, pd and pl) podomeric setae are numbered in the usual manner (Evans and Till, 1979).

Halarachne halichoeri females (Figs 1, 2A, 3; Table 1): As shown in the micrographs (Fig. 1), illustration (Fig. 2A) and schematic interpretation (Fig. 3), the sensillar array comprises five transverse 'horizons' of sensilla. These include two proximals (Pxl, Px2), three medials (M1, M2, M3), one posterior (Psl), two (anterior and posterior) laterals (AL, PL) flanking an array of four closely spaced centrals (C1, C2, C3, C4), and one distal (D1) sensillum. The sensilla within each horizon are numbered proximal to distal.

The paired proximal Px-series sensilla are short, smooth, aporous, solid and have basal sockets. Two of the three M-series sensilla (M2 and M3) are elongate, possess distal longitudinal wall slits, whereas M1 has a few wall-pores. All three have basal sockets and M1 (or M2) and M3 are paired. The posterior (Ps) sensillum is a smooth and hollow peg set in basal socket.

The lateral (AL and PL) sensilla which flank the central series are finely striated, tapered, possess a solitary sub-apical pore and each one is set in a flexible socket. The central (C) array comprises four sensilla. C1 is short, solid, inserted in a deep socket.

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FIG. 1. The tarsus I sensillar array of H. halichoeri female. (A) Dorsal aspect showing position of tarsus I (arrow). Scale: 500 #m. (B) Distal region of left tarsus I showing the sensillar array. See Fig. 2A for annotation. Scale: 10 pm. (C) Basal fracture through D1 sensillum showing its solid wall (w), hollow lumen (1) and basal socket (s). Scale: 1 #m. (D) The proximal, central and lateral sensilla. Scale: 5 #m. (E) The trich-like C1 sensillum in its deep pit-like socket. Scale: 1 #m. (F) The sessile and aporous C3 sensillum which resembles the insect 'thin-sensillum'. Scale: 1 #m. (G) The posterolateral (PL) sensillum showing the terminal pore (arrow) and basal socket. Scale: 2/~m. (H) This medial M2 sensillum has been partially damaged by the FIB or electron beam of the SEM to show the deep linear grooves parallel to the sensillar axis (arrow). Scale: 2#m. (I) A smooth-walled Px sensillum with a basal socket. Scale: 1 pro.

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Tarsus I sensillar field in Halarachne 1073

I 20 pm

a13 11

Px2 ~ Pxl |

i

B

I I

FIG. 2. The right side tarsus I sensillar fields of: (A) H.halichoeri larva (based on Fig. 1B). (B) H. miroungae larva (based on fig. 4D [reversed]). (C) H. halichoeri female (based on Fig. 6D). The sensilla (roman) and setae (italics) are numbered as indicated in the text.

C2 is blunt, sessile, mounted on a basal conical mound and equipped with a few minute simple wall-pores. C3 is sessile, smooth, round-tipped and without pores, while C4 is sessile, smooth and has a dilated base. D1 is a large, socketed, thick-walled and has a few simple wall pores.

Halarachne halichoeri larva (Figs 2B, 4, 5; Table 2): The sensillar field is similar to that of the adult, but differs in a number of respects. The proximals are sessile, very small, with a solid core surrounded by a space and a solid outer wall. The two latero-medials (M 1 and M3) are of dimorphic length, being either short (4.7 < 5.8 #m) or long (7-0 < 9.0/~m). M1 has small and simple wall-pores. M2 is very long, has a narrow lumen surrounded by a thick wall perforated by number of small and irregular cavities and traversed by (three?) deep but narrow channels each with a small dilated chamber close to the lumen. The channels correspond to the surface grooves. The lateral setae, in contrast to those of the adult female, do not have apical pores. C1 is solid; C3 and the dorsal seta pd2 are both absent.

Halarachne mirounga larva (Figs 2C, 6; Table 3): The sensillar field is very similar to that of H. halichoeri larva but differs in the following respects. The proximal series sensilla are reduced to very small papillae; C3 is absent, but in one specimen a minute stubby peg is present in its position.

The functions of individual sensilla (Table 4). Acari possess a limited range of sensilla when compared with insects. There are for

example only seven basic types in the Ixodida (Altner, 1977; Axtell, 1979, Altner and

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a:

b:

C:

d:

e:

f: g:

h:

0

@

@

@

@

®

@

r pd2#

o1@ 0

c4 0 AL (~r %1 ~02

~r(~ PL Psl (~

M3 (~ M2 ® ®M1

~r(~Px2 ~r(~ Pxl

20 pm I

p/3

/ FIG. 3. General schematic of the right side tarsus I sensillar field of H. halichoeri female. Key:

a function unknown, b-sw/WP sensillum with simple wall pores, c-sessile TA- ('thin') sensillum, d-solid ('trich-like') sensiUum, e-TP sensillum, f~lw/WP sensillum, g-solid mechanreceptor, h-basal socket on any of the above sensilla. #--absent in larva. *-morphologically different in larva. The following podomeric setae are illustrated as 'usual' (Krantz, 1978): ad2-anterodorsal sata. a12 al3-anterolateral setae, pd2 pd3-pos- terodorsal setae, p12 pl3-posterolateral setae.

Prillinger, 1980; Hess and Vlimant, 1986), compared with 20 on the lepidopteran antenna alone (Steinbrecht, 1987). Although it is inadvisable to ascribe precise function to particular sensilla based exclusively upon morphological criteria there is pronounced conservatism in the structure and function of arthropod sensilla which makes broad generalizations feasible (Evans, 1992).

There are five basic sensillar types reported in the Gamasina (Farrish and Axtell, 1966; Jalil and Rodriguez, 1970; Coons and Axtell, 1973; Woolley, 1988; Evans, 1992). Gamasid sensilla include: (1) Aporous (NP-) sensilla which may also be temperature receptors or have other unknown functions. The remaining types all have pores indicative of chemoreception, for example (2) gustatory TP-sensilla, each with a single terminal-pore, and WP-sensilla covered in numerous small (wall-) pores. The WP-sensilla include both (3) those with simple pores and a single wall (sw/WP-type) which respond to organic (host-specific) molecules, and (4) those with a double wall (dw/WP-type) which are probably multifunctional hygro- or thermo-sensilla. The sensilla may be sessile (NP, TP, dw/WP and sw/WP types), or set in flexible sockets (NP, TP, dw/WP types), indicative of possible additional mechanoreceptive functions.

The Px-series sensilla (of the adult) have no recorded homologues on the gamasid

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Tab

le 1

. T

he s

ensi

llar

arr

ay o

f H

ala

rach

ne

hali

choe

ri a

dult

fem

ale.

Cod

e In

sert

ion

Len

gth

(#m

) B

asal

q5

(#m

) S

hape

(le

ngth

and

tip

) S

culp

ture

ad2

sock

et

70.0

2.

94

pd2

sock

et

53.0

2.

85

D1

sock

et

12.0

-14.

5 4

.14

.4

C4

sess

ile

7.8-

8.5

2-8-

2.9

C3

sess

ile

13.0

2.

32-2

.57

C2

sess

ile

6-0-

7.0

2.8-

2.9

C 1

cu

p 6-

8-8.

3 1.

8 A

L

sock

et

8.4-

9.3

2.19

P

L

sock

et

8.1-

8-8

1.87

-2.0

5 P

s 1

sock

et

7.3

2-95

-3.3

0 M

3 so

cket

6.

7 2.

10

M2

sock

et

12-9

2.

35-2

.72

M1

sock

et

7.9-

9.0

2.30

-2.6

7 P

x2

sock

et

2.9

1.81

P

x 1

sock

et

2-8

1.75

elon

gate

set

a el

ogna

te s

eta

stou

t, r

ound

ed

bulb

ous

base

, sl

ende

r co

nica

l, r

ound

ed

stou

t, r

ound

ed

shor

t, po

inte

d tr

ich

tape

nng,

poi

nted

ta

peri

ng,

poin

ted

coni

cal,

rou

nded

ta

peri

ng,

poin

ted

tape

nng,

poi

nted

ta

penn

g, p

oint

ed

coni

cal,

rou

nded

co

nica

l, r

ound

ed

(dis

tal)

sm

ooth

sm

ooth

fe

w s

mal

l w

all-

pore

s sm

ooth

sm

ooth

~.

nu

mer

ous

smal

l di

stal

por

es,

basa

l m

ound

~"

sm

ooth

=~

fi

ne l

ongi

tudi

nal

stri

ae,

sub-

apic

al p

ore

fine

lon

gitu

dina

l st

riae

, su

b-ap

ical

por

e ,.

sm

ooth

de

ep l

ongi

tudi

nal

groo

ves

deep

lon

gitu

dina

l gr

oove

s fe

w w

all-

pore

s sm

ooth

sm

ooth

(p

roxi

mal

)

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1076 P . J . A . Pugh

i!'=

==,,.,=' = ;= i~iiii iii- ; i

R F~G. 4. The tarsus I sensillar array of H. halichoeri larva. (A) Non-cleaned tarsus I showing

the the sensilla of the sensillar array embedded in a plaque of bacteria and mucus (arrow). Scale: 50#m. (B) Cleaned tarsus I showing the sensillar array (arrow). Scale: 50pm. (C) The peg-like Dl-sensillum with fine surface striae and the basal socket on top of a raised 'cone-like' socket (arrow). Scale: 2#m. (D) Detail of the sensillar array. See Fig. 2B for annotation. Scale: 10#m. (E) Fractured Dl-sensillum showing a large central lumen (1) and a wall (w) perforated by small simple pores (arrow). Scale: 1 #m. (F) The proximal central and lateral sensilla. The deep grooves (arrow) are 'scars' lefts by ion-milling of selected sensilla. Scale: 5 #m. (G) The sessile, aporous and peg-like C2 (foreground), with the smooth walled basally dilate C3 analogue of the insect 'thin sensillum' (background). Scale: 2 #m. (H) Base of fractured C3 sensillum showing the thin aporous wall (arrow) and open lumen. Scale: 1 #m.

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Tarsus I sensillar field in Halarachne 1077

FIG. 5. The tarsus I sensillar array of H. halichoeri larva. (A) Ion beam milled AL-sensillum showing the aporous wall and large open lumen. The oblique 'streak' (arrow) is debris left by ion milling. Scale: 1/~m. (B) Aporous Ps-sensillum on a basal mound. Scale: 1 #m. (C) Ion beam milled Ps-sensillum showing the large open lumen and solid wall. Scale: 1 #m. (D) The Px and M-series sensilla. Material (debris or secretion?) is clearly visible in the longtidudinal slits of M3 (arrow). Scale: 2 #m. (E) Damaged M3-sensillum showing distal longitudinal wall slits (arrow). Scale: 1 #m. (F) Ion beam milled M2-sensillum milled close to base showing the small lumen (1) and thick wall (w) perforated by small 'cavities' and traversed by deep grooves with a diluted 'chamber' (arrow) close to the lumen. Scale: 1/~m. (G) Ion beam milled Ml-sensillum showing preforated wall (w) and material within the large lumen (1). Scale: 500nm. (H) Ion beam milled sessile Px-sensillum showing the narrow space (arrow) between the solid core and imperforate wall. Scale: 500nm.

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oo

Tab

le 2

. T

he s

ensi

llar

arr

ay o

f H

ala

rach

ne

hali

choe

ri l

arva

.

Cod

e In

sert

ion

Len

gth

(am

) B

asal

~b

(am

) S

hape

(le

ngth

and

tip

) S

culp

ture

(dis

tal)

ad

2 so

cket

pd

2 A

BS

EN

T

D 1

so

cket

C

4 se

ssil

e C

3 A

BS

EN

T

C2

sess

ile

C 1

cu

p A

L

sock

et

PL

so

cket

P

si

sess

ile

M3

sess

ile

M2

sess

ile

M1

sess

ile

Px2

se

ssil

e P

xl

sess

ile

100

5.0

elon

gate

set

a sm

ooth

16-5

-18.

7 4.

8-5.

3 st

out,

rou

nded

10

.6-1

1.7

3.4

bulb

ous

base

, sl

ende

r

12-8

-16.

0 3.

5 co

nica

l, r

ound

ed

8.0

1.7

shor

t, p

oint

ed t

_ric

h 11

.9-1

2.9

2.3

tape

ring

, po

inte

d 10

.7-1

1.2

2.4

tape

ring

, po

inte

d 9.

3 3.

5 co

nica

l, r

ound

ed

5.3-

5-8/

7.0-

9-1

2.2/

2.7-

3-5

tape

ring

12

.7-1

6.8

3.0

tape

ring

, po

inte

d 4.

7/8.

4-9-

7 2.

8 ta

peri

ng

2-2-

2.5

2.1

coni

cal,

rou

nded

2.

3-2-

5 1.

3 co

nica

l, r

ound

ed

few

sm

all

wal

l-po

res

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Tarsus I sensillar field in Halarachne 1079

FIG. 6. The tarsus I sensillar of H. miroungae larva. (A) Dorsal aspect showing sensillar array on tarsus I (arrow). Scale: 200/~m. (B) Tarsus I showing the sensillar array. See Fig. 2C for annotation. Scale: 10 #m. (C) Detail of the sensillar array. Scale: 5/~m. (D) The C- and L- series sensilla. Scale: 5/~m. (E) D 1 sensillum showing surface grooves and basal mound (arrow). Scale: 2 #m. (F) No terminal pore is not visible in this socketed AL-sensillum. Scale: 1 #m. (G) Two of the three M-series sensilla. Scale: 2 lam. (H) The button-like Px sensillum. Scale: 1 #m.

tarsus, but they do resemble the csl (conical smooth-walled aporous) mechanoreceptors in the ixodid Haller's organ (Leonovich, 1983). The internal 'vase-like channels' (sensu Foelix and Axtell, 1971), of the M2 and M3 sensilla are characteristic of dw/WP thermo- or hygroreceptors (Leonovich, 1983, 1985; Hess and Vlimant, 1986; Leonovich and Belozerov, 1992), while their basal sockets imply that these are probable dual function thermo-/hygro-contact mechanoreceptors. The other M1 sensillum may be a fine pored

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Table 3. The sensillar array of Halarachne miroungae larva.

Length Basal ~b Shape Code Insertion (btm) (am) (length and tip) Sculpture

(distal) ad2 socket 150 3.7 elongate seta pd2 ABSENT D1 socket 11-9-12-8 3.9-4.3 stout, rounded fine striae C4 sessile 8.4-9-8 2.9-3.1 bulbous base, slender smooth C3 sessile 2.7 1.55 conical, rounded C2 sessile 8.0-8.3 2.6-2.9 conical, rounded C1 cup 7.0 1.1 short, pointed trich AL socket 9-7 1.9-2.0 tapering, pointed PL socket 7.0-7.6 2.1-2.2 tapering, pointed Psi socket 5-6 2.6-3.0 conical, rounded M3 sessile 4.7-5.9 2.2-2-4 tapering M2 sessile 11.1 2-7 tapering M1 sessile 4.2-5.0 2.1-2-4 tapering P X 2 sessile < 0-3 1-9 papilla P × 1 sessile 1 1.4-2.0 papilla

smooth

MOSTLY ABSENT smooth/pimpled smooth pimpled surface smooth? rough few longitudinal striae ? pimpled

(proximal)

Table 4. Sensillar array of Halarachne: summary of form and function.

Code Pair Insertion Core Pores Possible function(s)/similarities

D1 socket hollow sw? C4 sessile hollow - - C3 sessile hollow - - C2 sessile hollow sw? C 1 cup solid - - AL PL socket hollow TP(#) PL AL socket hollow TP(#) Ps 1 socket hollow - - M3 M1 socket(*) hollow dw M2 socket(*) hollow dw M1 M3 socket(*) hollow sw P × 2 P × 1 socket(*) solid - - P × 1 P X 2 socket(*) solid - -

(distal) olfactory? mechanoreceptor 'thin sensillus' thermoreceptor? unknown, absent in larva olfactory chemoreceptor? air-movement mechanoreceptor contact chemo-mechanoreceptor contact chemo-mechanoreceptor unknown/mechanoreceptor hygro/thermo-mechanroceptor hygro/thermo-mechanroceptor chemo-mechanoreceptor contact mechanoreceptor? in adult contact mecbanoreceptor? in adult

(proximal)

Note: 'similarities with known structures in quotation marks' (see text). * = sessile in larva; # = NP-type in larva.

(sw) chemoreceptor , whi le the pos ter ior (Ps) sens i l lum is a contac t -mechanoreceptor , though its hol low core indicates another (unknown) function.

A L and PL are gusta tory (TP-) sensi l la and their basal sockets suggest that these are gus ta tory-contac t -mechanoreceptors , i.e. l ike most gusta tory sensi l la that have a dualfunct ion (Sonenshine, 1991). C 1 is reminiscent o f a t r ichobothr ium which responds to a i rborne vibrat ions and yet, in the Acar ina , t r ichobothr ia are unique to the Act ino t r ich ida (Evans, 1992). The stout nature o f C1 suggests that it resonates in sympathy with low f requency sounds and has a high s t imulat ion threshold whi le the or ientat ion of the socket, i.e. facing towards the ambulac rum along the mid- l ine axis,

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Tarsus I sensillar field in Halarachne 1081

suggests that it may have a vector (directional) response. C2 is a sw/WP-sensillum with simple wall-pores (cf. Altner and Prillinger, 1980; Leonovich, 1985; Hess and Vlimant, 1986), and a probable olfactory chemoreceptor. The functions of C3 are unknown, while C4 resembles the thin sensillum (TA), a thermoreceptor which occurs in both insects and ticks (Steinbrecht, 1989; Leonovich and Belozerov, 1992).

D1 is very similar in shape, relative size and position to the large precapsular distal sensillum (dsl) of the Ixodidae (Leonovich, 1983), features which suggest that this is a chemo-mechanoreceptor. But D1 differs from the dsl sensillum in two respects. Firstly, it has a few simple wall pores as opposed to numeorous large ones and second, it is socketed as opposed to sessile. This is an unusual combination of characters, because anactinotrichid olfactory sensilla are usually sessile and covered with large pores (Jagers op Akkerhuis et al., 1985; Sonenshine, 1991; Evans, 1992).

General functions of the sensillar field Electrophysiological evidence is not available to support individual sensillar

function, but simple experiments (Pugh, unpublished observations), suggest that though larvae of H. miroungae do not respond to any identifiable component of 'seal smell', they will respond to contact (touch), vibration, elevated air temperature, humidity and carbon dioxide concentrations; all of which are features characteristic of seal breath. Possible receptors for these stimuli have been identified in the sensillar field, though work on other Gamasida suggests that receptors may occur on the leg ambulacra, palps and chelicerae (Jackson and Ford, 1973; Hislop and Prokopy, 1981; Jagers op Akkerhuis et al., 1985).

Touch. All of the socketed sensilla and most of the (similarly socketed) tarsal setae are probable tactile contact mechanoreceptors (Evans, 1992).

Vibration. Although Anactinotrichida do not possess trichobothria they do respond to vibration. For example Ornithodorus concanensis (Argasidae: Ixodida) can detect air vibrations via receptors on the first pair of legs (Webb et al. 1977). The C 1 sensillum is probably a vibration receptor, but there are undoubtedly other vibration receptors beyond the sensillar field, for example the distal tarsal sense organ (Hess and Vlimant, 1984).

Olfactory chemoreception. The detection of large organic molecules in the vapour phase via sw/WP-sensilla (Evans, 1992). Tick sw/WP sensilla are sessile and have plugged-pores (sensu Altner and Prillinger, 1980), while those on insect and tarsi I of the Gamasida are simple-pored (Farrish and Axtell, 1966; Jalil and Rodriguez, 1970; Coons and Axtell, 1973; Woolley, 1988). This structural disparity between acarine and insect and olfactory sensilla suggests they have different functional mechanisms (Leonovich, 1987).

Olfactory sensilla are invariably substrate specific (Haggart and Davis, 1980, 1981; Waladde, 1982; Jagers op Akkerhuis et al., 1985; Hess and Vlimant, 1986; McDowell and Waladde, 1986; Evans, 1992). Variations in the number and disposition of olfactory chemosensilla are indicial of differences in chemosensitivity. In the Ixodida for example, the host-hunting Ixodidae have better developed olfactory senses than the host-ambushing Argasidae, a behavioural difference which is consistent with differences in the morphology of their respective olfactory sensillar arrays (Zolotarev and Sinitsyna, 1965; Foelix and Axtell, 1971, 1972).

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Only three sw/WP olfacto-sensilla (M1, C2 and D1) are present in Halarachne, all of which are ornamented with relatively few small and simple pores and hence may be able to detect some smaller inorganic molecules for example carbon dioxide, ammonia and lactic acid (cf. Sonenshine, 1991). The absence of plugged-pore sensilla suggests that Halarachne lacks the sensory ability to detect large air-borne organic molecules which are usually associated with odour.

Gustatory chemoreception. Contact/taste chemoreceptors which respond to large organic molecules dissolved in a liquid medium are more usually associated with the palps and chelicerae (Evans, 1992). The paired AL/PL sensillaa of adult, but not larval, Halarcachne are probable gustatory receptors which, like the sw/WP tarsal sensilla of Phytoseiulus (Phytoseidae: Mesotigmata), have the typical non-plugged terminal pores (Jagers op Akkerhuis et al., 1985).

Temperature and humidity. The C4 'thin sensillum' is a possible thermoreceptor, however the M-series 'triad' comprising two thermo/hygro-sensitive sensilla and a possible inorganic chemnoreceptor is a more typical thermo-/hygro-receptor unit. Within such a triad, each sensillum responds to different but related stimuli for example increasing humidity, decreasing humidity and temperature changes (Foelix and AxteU, 1972; Leonovich 1977; Waladde and Rice, 1984; Steinbrecht, 1988, 1992). Thermo- receptors not only detect air temperature, but shadow and other thermal gradient effects (Evans, 1992). The morphology of the 'M-series triad' is not identical to the 'triads' described either for ticks or insects, again reflecting the different origins of tick and halarachnid receptor systems proposed for the olfactory sensilla.

Organization within the sensillar field The C-series air movement, hygro- thermo or olfactory chemo-receptors are

encircled by several groups of mechanoreceptors, including the Px, M, Ps L and D-series sensilla, while the whole of the sensillar is surrounded by very elongate (dual function?) mechnoreceptor (al, pl, ad and pd) setae. The sensillar arrangement is similar to that in the ixodid Hailer' s organ pit (Axtell et al., 1973; Goethe et al., 1991), though it is more usual that the WP- and TP-sensilla are concentrated in the distal half of a podomere, while the NP- sensilla are more proximal (Evans, 1992).

Although the halarachnid sensillar field and the ixodid Haller's organ are strikingly similar, they are not necessarily homologous. Indeed the common features shared by the sensillar fields of different families within the Gamasida are more suggestive of convergence than 'actual relationships' (Haarlcv, 1943), i.e. they are more likely to be analogous rather than homologous structures.

Other Observations

Adherent material. The sensilla of the larvae collected live from the external nares of the seals were usually clean, but those larvae and adults obtained duringpost-mortem examination of seal carcasses were covered in a thin adherent plaque of mucus and bacteria (Fig. 4A, cf. 4B). This plaque could be removed by ultrasound cleaning, but raises the question of whether the sensilla function when embedded in this material and, if so, how?

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Tarsus I sensillar field in Halarachne 1083

Sensillar changes. Observations in the field as well as those reported in the literature (Newell, 1947; Gretillat, 1959a, b; Hughes, 1959; Dahme and Popp, 1961; Kurochkin and Sobolewsky, 1975), confirm that only the larvae ofHalarachne spp. are dispersive. Yet females have one additional (C4) sensillum and one additional (pd2) seta, compared with the larval sensillar field. Furthermore the proximal (Px) sensilla become larger and change from sessile to socketed, while the lateral (L) sensilla change from simple mechanoreceptors to more complex dual function olfactory-mechanoreceptors. Why less mobile or even immobile females require these additional olfactory sensilla and better developed-mechanoreceptors is unresolved. It may be that females are not immobile and that they use these sensilla to locate the smaller immobile males in the nasal passages of the host. To date however, only the palpal organ of the Ixodida has been implicated in sex recognition (Soneneshine, 1991).

Conclusions Simple experiments suggest that Halarachne spp. larvae respond to a range of

short-/long range stimuli, none of which are host specific, but could indicate the presence of any large endotherm. The sensillar field, which most probably receives these stimuli, is ornamented with an array of sensilla similar to those of the 'pit' in the ixodid tick Haller's organ. During appetence, or host-seeking behaviour, ticks use the pit to receive a variety of non-specific stimuli to locate a large endotherm and then rely upon specific odours received via sw/WP sensilla as the main cues to identify suitable hosts amongst a potentially broad spectrum of large animals (Waladde and Rice, 1982).

But, unlike the ticks, Halarachne spp. do not possess anything comparable to the capsular array of isolated plugged- (or at least large-) pored sw/WP olfactory chemreceptors. Nor are similar but non-encapsulated sensilla present on either the legs, palps or chelicerae. So although Halarachne spp. can probably locate a large endotherm, they do not have the ability to distinguish between potential hosts, i.e. seals, and other endotherms. This is not a problem however because seals usually form large mono-specific colonies/rookeries on beaches and so the dispersive larvae of Halarachne spp. are only likely to contact other conspecific seals and so therefore have no requirement for a host recognition system.

Acknowledgements I am indebted to the following for their assistance: The British Antarctic Survey

(BAS) for providing facilities; Dr Tom Arnbom, Department of Zoology, University of Stockholm; C. Chambers, H. MacAlister and A. Morton of BAS; Ailsa Hall and Patrick Pomeroy of the Sea Mammal Research Unit (SMRU), Cambridge, Dr J. Baker, Department of V e t e ~ Pathology, Lhfiversity o f Liveaq~ol and Dr Anne Baker of the Arachnida and Myriapoda Sectiom Department of Zoology, The Natural History Museum, London, for providing numerous samples of halarachnid mites; Mr K. Robinson of the Electron Microscope Unit, BAS, for his help with electron microscopy, and in particular for developing many of the techniques used in this study; Dr R. Young of FEI Europe, Cambridge for his help with the development of ion milling and use of the FIB machine; Dr I. Boyd of BAS, Dr M. Fedak and Mr B. McConnell of SMRU who provided me with much valuable information regarding seal biology, and Dr P. Convey, Mr K. Robinson of BAS and an anonymous referee for commenting on the manuscript.

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