J. Dinnik and F. Zumpt.
The Integumentary Sense Organs of the Larvae of Rhipicephalinae (Acarina).
Psyche 56(1):1-17, 1949.

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PSYCHE
VOL. 56 MARCH, 1949 No. 1
THE INTEGUMENTARY SENSE ORGANS OF THE
LARVA3 OF RHIPICEPHALINB (ACARINA)'
BY J. DINNIK and F. ZUMPT'
In 1938 Delpy published a short paper describing the location and morphology of the so-called spiracles or respiratory plates ("stigmates respiratoires") of vari- ous Ixodid larvze. He examined for the purpose Hya- lomrna dromedarii Koch, H. irnpressum Koch, Boophilus annulatus Say, Rhipicephalus bursa Can. and Fanz., and Hamaphysalis ciwnabarima punctata Can. and Fanz. Delpy's description is brief and lacks illustrations. He thought that he saw within each "spiracle" 1 or 2 pores, sometimes reduced in size, leading into an atrium pro- vided with two valves at the entrance. The base of the atrium he described as pierced with an opening, and Delpy considered it possible that a tracheal tube was at- tached at this point.
With regard to their position, Delpy distinguished coxal and abdominal spiracles. The coxal spiracles are in three pairs, placed behind each of the six COXE. The abdominal spiracles vary greatly in number and position according to the genus. Hmnaphysalis is said to have four pairs, Hyalomma and Rhipicephalus only one pair, while they are entirely lacking in Boophilus. Delpy was not the first, however, to describe supposed spiracles in Ixodid larv~. Salmon and Stiles (1902) saw 1 Preliminary Study No. 10 for a Revision of the Genus Rhipicephalus Koch.
Nos. 1 to 8 of this series were published in the Zeitschrift fur Para- sitenkunde from 1939 to 1943.
No. 9 is to appear in Dechiana (Festschrift f. Prof. Reichensperger) .
2 Now at The South African Institute for Medical Research, Johannesburgj South Africa.
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2 Psgche [Mar.
them before, and they were also mentioned by Oudemans (IgO6), Zebrowski (1926) and Cooley (1938). All these authors were mistaken in the interpretation of the function of the organ they had seen. The larv~ of the Ixodidz do not possess any special respiratory organs. Only Samson (1908) correctly recognized that the so-called ' ' larval spiracles ' ' described by Salmon and Stiles were actually tge terminal pores of i&egumentary sense organs. This correction was, however, overlooked up to quite recently. Even Vitzthum, in his account of the Acarina for "Bronn's Klassen und Ordnungen des Tierreichs" (1940), adopted in detail the description and views of Delpy.
K. W. Neumann (1942) and Elishewitz (1942) first re- examined these structures in an attempt to decide whether they were respiratory organs or integumentary glands. Serial sections of larvz of Demnacento~, Ha- maphysalis, Hyalomrna and Ixodes convinced Neumann that neither the Ixodime (Prostriata) nor the Rhipi- cephalinz (Metastriata) have respiratory organs and that the structures thus far interpreted as spiracles are really integumentary glandular organs.
According to Neumann, these organs are in a direct view more or less oval in outline.
"A broad ellipsoid
chitinized frame at the periphery is attached to the sur- rounding cuticula by means of a narrow, prominent, striated edge. The lumen also is oval and contains two parallel, non-contiguous lips. Two small protuberances of the frame extend on each side into the lumen, keeping the lips from touching each other. By lowering the ob- jective, a small circular opening may be recognized in the center between the lips?
"In a side view of the entire organ or in a section, the structure is also more or less elongate oval. The walls consist of a rather thick layer of chitin, decreasing in thickness from the base toward the surface opening. A short duct leads from the base toward the interior of the body. On either side of the mouth of this duct a tooth, anchored to the base of the organ, extends up into its lumen. Serial sections show that these teeth arise from a folding of the walls. Their length is approximately three-fourths of that of the entire organ.''



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IWQ 2 Dbik md Zuvnpt-Rhipicephalima 3
&(To what do these several parts correspond7 The broad frame is the wally the lips are the teeth? and the eircuhr opening i~ the month of the short duct." (See Pl. I, fig. I.)
<(The organ is securely anchored in the cuticula by the upper third of its length. The subjacent hypodermal cells are broader than high and surround the organ. The adjacent cells ( ?generative cells) are much higher than broad. Only two seem to be present, placed parallel to the margins of the lips. A large cell, considerabIy broader than high? lies beneath the organ, in close can- tact with the entire basal surface,
The duct mentioned
before is never long enough to pierce this basal cell, but ends with it without tapering downward. The duct is never lined with a tmidium. So far as can be detected? the plasma of this cell is slightly granulary but a promi- nent dear spot in the center may be interpreted as an internal ve~ide. It follows from this description that the structure is an integumentary glandular organ, not a larval respiratory organ with a spiracle and a rudi- mentary trachea.'
So much for K. W. Neummn's account of the mor- phology of his integumentary sense organ. In addition he discusses the number and position of these organs in various genera and believes to be justsed in stating that originally two pairs were present. Accordhg to his ac- count, all the spiracle-like organs show essentially the same structure, though they are sometimes reduced in size, and they seem undoubtedly to be peculiar to the larm.
He does not mention any other integumentary sense organs besides the so-called ~'spixacles.'~ P. Schulze (1942a) published a detailed study of the integumentary sense organs of adult ticks and found? besides true sensory set* (sensilla trichoidea), four other types of sensilk which he called SemJa awif ormia (ear- shaped organs ), 8emsik sagit fif orw& ( arrow-shaped o~gans ), h'ems%a has‰âÂiform (spear-shaped organs), and #emsilla Laiemiforwaia (lantern-shaped organs). Large numbers of these organs axe hated within the hard and soft chitinized integument of the body. Qn the other band they are Rpame on the leg^ and palps and,



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4 Psyche [Mar.
strangely enough, seem to be entirely missing on the chelicerte.
Characteristic for these sensilla is their con- nection with two glandular cells which extend partially into the sensory duct. These cells secrete into the duct a substance which emerges at the surface after passing an end organ.
P. Schulze assumes that the secretion serves as a protective coating against evaporation within the sensillum and on the outer surface, and also as a chem- ical means of recognition between opposite sexes and in- dividuals of one species.
The sensory fuGction of the sensilla auriformia seems to be of a proprio-receptive nature, serving to perceive changes or shifts within the chitin. It is probable that the other three types, grouped together as " tuft-shaped" sense organs or .krobylophores, are vibro-chemoreceptive organs, which react at the same time to chemical as well as to seismic stimulation. They evidently play an im- portant part in the sexual life of the ticks. We examined the larv8 of Rhipicephalus sa~guiaeus Latr., Rh. appe~diculatus Neum., Rh. bursa Can. and Fanz., Rh. evertsi Neum., R7%. sirnus Koch, Hyalornrna drornedarii Koch, and Boophilus calca~atus Birula. The larvte were merely mounted whole on microscopic slides in Berlese's medium, a procedure which we found to be superior for our purpose to all other methods of mounting. Owing to prevailing conditions we were un- able to make sections.
We were able to ascertain that the larvte are not equipped with peculiar integumentary sense organs. On the contrary we found much the same organs present as in the adults and nymphs. In the larvte, however, sen- silla laterniformia seem to be lacking and the other types of sensilla are to some extent more primitive in develop- ment. The organs are distributed over the entire body in fixed numbers and in a definite arrangement. A detailed account of the three types of sensilla men- tioned above follows.
I. Sensilla sagittiformia (arrow-shaped organs) The sensillu~ sagittiforme represents a new mode of sensory organ, called by P. Schulze a krobylophore sen-



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19491 Dinnik and Zumpt-Rhipicephali~e 5
sory organ, because a tuft-shaped structure is its most striking characteristic.
In the adult tick he described
this organ as follows in side view (Pl. I, fig. 2) : "The distal portion of the chitinized passage or lumen appears arrow-shaped.
Below this lies a narrow pagoda-shaped
'tuft' chamber and farther inside a small, more or less spheroidal 'terminal chamber. '
This is separated from
Text-figure 1. A) Sensillum sagittiforme of the opisthosoma of ~h&~i- cephalus appendiculatus Neum. B, Same in the larva. C) Same in the nymph. D) Sensillum hastiforme of Rhipicephalus append& culatus Neum.
E, Same in the nymph. I?, Same in the adult female.
the middle chamber by projecting ledges which leave room only for a small circular opening.
The innermost
chamber is attached to a simple duct into which the glan- dular cells extend, enveloping the nerve cells. The sur- rounding chitin is especially thick beneath the lower por- tion of the 'arrow points.' The nerve cells decrease in size as they enter the 'terminal chamber.' The axial fiber is attached to a strong scolopale which enlarges t0



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6 Psyche [Mar.
form a knot and then tapers down, becoming pointed again upon entering the 'pagoda-shaped chamber' in which the 'tuft' is located. This tuft has much the shape of a gas flame and is not chitinized but of a uni- form structure, although at times it seems to be some- what fibrillar. ' '
The larvae we examined all show, contrary to Delpy's description, four pairs of spiracle-like structures, three of them behind the coxae, the fourth on the opisthosoma (PI. 2, figs. 4 and 5). A comparison of their inner structure (Text-fig. 1A-C) with P. Schulze 's description and drawings clearly shows that these so-called ' 'larval spiracles " are in reality sensilla sagittif ormia. The finer structure of the organ is best seen in the opisthosomal pair of the larvae of Rhipicephalus appendiculatus and Boophilus calcaratus. It is pear-shaped and pierces with its conical end the integument on the dorsal face of the fourth festoon. The walls are of thick chitin, the chitinous capsule being 0.012 to 0.016 mm. long and 0.011 to 0.014 mm. broad. A funnel-shaped fold is visible within the capsule. The narrow ends of this capsule, pointing toward the opening, are less strongly chitinized and look in direct view like a pair of lips lying within the capsule (compare PI. 1, fig. 1). Within these lips lies the tuft-like structure, surrounded by a fine pagoda-like contour.
The sensilla sagittiformia behind the second and third coxae are very similar in structure to the opisthosomal pair described above. On the other hand, the pair lo- cated behind the first coxae at the edge of the scutum seems to have a strikingly thick-walled capsule which is fully embedded in the chitin of the scutum. It is 0.019 to 0.022 mm. long, 0.016 to 0.022 mm. wide at the base, with the opening 0.011 to 0.014 mm. in diameter. The "tuft" is difficult to recognize here, but is shaped as in the other pairs.
2. Sensilla hastiformia (spear-shaped organs) The sensilla hastiformia, as described by P. Schulze for the adult ticks, are much smaller than the arrow-



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19491 Dinnik and Zmpt-Rhipicephalhis 7
shaped organs.
He was unable to make out all the de-
tails of the terminal apparatus, but he presumed that they correspond in general to those of the sensilla sagit- tiformia and that a tuft-shaped structure is also present. The main difference lies, according to Schulze, in the upper portion of the passage leading to the outside. This lacks the long receding arrow-points, so that the "pagoda-shaped chamber," formed by these points, is also missing. The passage is distinctly spear-shaped, in as much as it expands into two mainly horizontal pro- jections at the base.
The larval sensillum hastiforme could only be recog- nized as such after comparing it with the corresponding organ in nymphs and adults (Text-fig. 1, D-F). It lies as a short funnel-shaped structure in the lower part of the integument, which it pierces by means of a narrow passage, ending between the outer folds. The funnel- shaped portion is approximately 0.008 mm. in diameter and 0.005 mm. deep. The walls are about 0.002 mm. thick and the passage is roughly 0.008 mm. long. We were also unable to recognize the finer structure of the organ, nor could we find anything comparable to a "tuft." In direct view the organ has the appearance of a ring", 0.008 mm. in diameter. Further details cannot be recognized, but by lowering the objective the duct leading inside the body may be followed. The larvae of Rhipicephalus appendiculatus Neum., Rh. sanquheus Latr., Rh. bursa Can. and Fanz., and Rh. evertsi Neum. studied by us, all have 54 sensilla hasti- formia on the body proper; we did not examine the legs. The sensilla are placed strictly symmetrically and neither their position nor their number seem to vary to any extent (PI. 3, fig. 6). One pair is located on the capitulum, occupying the position taken by the areae porosae of the adult female tick. Five pairs are situated on the scutum and nine pairs on the alloscutum, four of these dorsal, one subdorsal and four sublateral. In addi- tion eight pairs are found on the edge of the alloscutum, one sensillum being placed on the edge of each festoon (or parmula), except on the middle festoon. The ar-




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8 Psyche [Mar.
rangement of these eight pairs is therefore metameric and seems to be derived from the primitive segmentation of the opisthosoma.
The "foveae dorsales " of the larva consist of only one sensillum hastiforme each. The integumental folds bend around their openings, whereas on the contrary the open- ings of the other sensilla hastiformia lose themselves among the folds of the integument. Aside from the fact Text-figure 2. Arrangement of the integumentary sense organs of the larva of Hyalomma dromedarii Koch: Fd, fovese dorsales; Sa, sensilla aurif ormia ; Sh, sensilla hastif ormia ; Ss, sensilla sagitti- f ormia.
that the openings are more conspicuous, they do not dif- fer from the usual type of sensilla hastiformia. Ventrally the body bears four pairs of sensilla hasti- formia. One pair lies very close to the sensillum sagitti- forme of the third coxa. In Rh. appendiculatus it is en- closed by the capsule of the sensillum sagittiforme, so that it is difficult to see. Though closely adjacent to it in the other species, the sensillum hastiforme is never- theless clearly set off.
The number and the arrangement of the sensilla hasti- formia of the larva of Boophilus calcaratus Birula (PI. 3, fig. 7) are similar to those of the Rhipicephalus, ex-



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19491 Dinnzk and Zumpt-Rftipicephalince 9 cept that we were unable to discover the two foremost pairs on the ventral side and that they seem to be missing '
also on the fourth and fifth festoons counting from the middle.
The larva of Hyalomma dromedarii Koch (Text-fig. 2) possesses more sensilla hastiformia than that of Rhipi- cepftalus. It should be mentioned especially that the middle festoon also bears a terminal -and a dorsal un- paired sensillum. In addition a sensillum hastiforme is located on the dorsal side adjacent to each of the second, third and fourth festoons. It is noteworthy that two pairs of sensilla hastiformia, instead of one pair, were found on the capitulum of one specimen in the position of the are= porosse of the adult female. 3. ~ensilla aurif ormia (ear-shaped organs) The sensilla auriformia discovered by P. Schulze (1942a) in adult ticks may be traced back with certainty to setae or hairs. They are located directly under the cuticula and consist each of a flat disk, usually inclined a little toward one side, so that it closes outwardly the sensory duct ascending from below, like a lid with over- lapping edges (PI. 1, fig. 3). The disks vary in details and have the shape of an ear, a megaphone or a bell. Their openings face various directions, so that it is pos- sible to see one sensillum in direct view and the other in side view when examining two of them placed close to- gether.
The larval ticks also possess these sensilla in typical form, but the organs are smaller than in the adult. The
disk is approximately 0.009 mm. in diameter. Arrange- ment and number again seem to be strictly uniform, but all the disks lean in one particular direction. Ten pairs of sensilla auriformia were found on the al- loscutum of all larvae of Rhipicephal'us examined. Five pairs may be seen dorsally some distance from the median line and five pairs on the edge of the allos'cutum. Neither capitulum nor scutum seem to have any. Twelve pairs are located on the ventral side, two of them be-



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10 Psyche [Mar.
tween the coxse, the remainder on the opisthosoma, five of the latter in the festoons.
The same number of sensilla auriformia is found in the larvas of Hyalomma dromedarii Koch (Text-fig. 2) as in RMpicephalus and their arrangement is similar. In the larva of Boopftilus calcaratus Birula (PI. 3, fig. 7) the pair behind the third COX= and the first pair on the edge are missing, but the remaining sensilla aurifor- mia are as in the larva of Rhipicephalus. The larvas of- the Rhipicephalinse do not possess pecu- liar integumentary sense organs, as K. W. Neumann (1942) believed, but rather the same types found in the nymphs and adults. The organs are merely in a more primitive state of development and the sensilla laterni- formia appear to be missing. Sensilla sagittiformia, sensilla hastiformia and sensilla auriformia may be dem- onstrated. These organs are strictly specific in number and arrangement within the genera Rhipicephalus, Hya- lomma and Boophilus.
BIBLIOGRAPHY
COOLEY, R. A.
1938, as cited by K. W. Neumann (1942).
DELPY, L.
1938. Morphologie et disposition des stigmates respiratoires chez les larves hexapodes des Ixodidae.
Bull. Soe. Path. Exot., vol. 31,
pp. 298-300.
ELISHEWITZ, H.
1942. On the structure of the so-called "stigmata" of larval ticks. Jl. Parasitology, vol. 28, Suppl., p. 25. NEUMANN, K. W.
1942. Die ' ' Dorsalplatte ' ' der Argasidenlarve als Teil eines Atmungs- systems und die angeblichen ' ' Atemplatten ' ' der Ixodenlarven. Zeitschr. Morph. Oekol. Tiere, vol. 38, pp. 420-434. OUDEMANS, A. C. 1906, as cited by H. Vitzthum (1943). SALMON, D. E. and STILES, C. W.
1902. The cattle ticks (Ixodoidea) of the United States. 17th Ann. Rept. Bur. Anim. Ind. U. S. Dept. Agric., for 1900, (1901), pp. 380-491, Pis. 74-98.
SAMSON, K.
1908. Die Eiablage und die Larve der Zecke Rhipicep'halus sanguineus Latr. Sitzungsber. Ges. Naturf. Freunde Berlin, pp. 46-50. SCHULZE, P.
1942a.Ue'ber die Hautsinnesorgane der Zecken, besonders uber eine bisher unbekannte Art von Arthropoden-Sinnesorgane, die



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Krobylophoren. Zeitsehr. Morph. Oekol. Tiere, vol. 38) pp. 379-419.
1942b. Die Riickensinnesf elder (foveae dorsales) der Zecken. Zeitsehr.
Morph. Oekol. Tiere, vol. 39, pp. 1-20.
VITZTHUM, H.
1943. Aearina, In BronnJs Klassen und Ordnungen des Tierreiehes) vol. 5, section IV) book 5) part 3) p. 363. ZEBROWSKI, G.
1926. A preliminary report on the morphology of the American dog tick. Trans. Amer. Ent. See.) vol. 51) pp. 331-369) Pls. 12-14.



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Fig. 1.
Larval integumentary sense organ of Haemaphysalis punctata Can. and Fanz.) redrawn from K. W. Neumann (1942). A) in direct
view; B, in side view: aR) sensory duct; Bbl, internal vesicle; Bz, generative cell; C) cutieula; Dz) gland cell; Hyp, hypodermis; L) lips; Oe, mouth of the sensory duct; R, frame; Rm) fringe; V, protrusions of the frame; Z, tooth.
Fig. 2. Schematic drawing of a sensillum sagittiforme of Hyalomma, after P. Schulze : Astr) axial fiber ; Dp, projecting ledges ; Dr) gland cell ; Ek) terminal chamber; KEst) knot of the scolopale; NE) enveloping eell nucleus ; Sch) tuft ; Schk) tuft chamber ; Sg) sensory cell group outside the duct. The chitinous structure surrounding the sense organ has been omitted.
Fig. 3.
Schematic drawing of a sensillum auriforme on the alloscutum of a female Hyalomma, after P. Schulze: Astr, axial fiber; Dz, shaded zone of the disk; Gh) papilla with terminal apparatus in central area of the disk; Hz) unshaded zone; Nk) enveloping cell nucleus; Pa, pigmented and thickened section of the duct; Sk) sensory eell nucleus; Tf) supporting plicature. The chitinous structure sur- rounding the sensory organ and gland cells has been omitted. The
disk covering the sensory cell and the terminal apparatus is assumed to be transparent.




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Gh
HZ
D Z
Pa
Astr
Sk
- Nk




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Psyche
[Mar.
Fig. 4.
Dorsal view of larva of Rhipicepha1u.s appendiculatus Neum., show- ing sensory organs: Fd, fovez dorsales; HO, Haller 's organ; Sa, sensilla aurif ormia ; Sh, sensilla hastif opia ; Ss, sensilla sagitti- f ormia.
Fig. 5.
Ventral view of larva of Rhipicephalus appendiculatus Neum., show- ing sensory organs : Sa, sensilla aurif ormia : . Sh, sensilla hasti- f ormia ; Ss, sensilla sagittif ormia.




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DINNIK AND ZUMPT-RHIPICEPHALIN~E




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Psyche
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Fig. 6.
Arrangement of the integumentary sense organs of the larva of Rhipicephalus sanguineus Latr.: Fd, fovese dorsales; Sa, sensilla aurif ormia ; Sh, sensilla hastif ormia ; Ss, sensilla sagittif ormia. Fig. 7.
Arrangement of the integumentary sense organs of the larva of Boophilus calcaratus Birula: Fd, fovese dorsales; Sa, sensilla auri- f ormia ; Sh, sensilla hastif ormia ; Ss, sensilla sagittif ormia.



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DINNIK AND ZUMPTÌÔRHIPICEPHALIN




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