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On The Egg of The Tick, Ixodes Ricinus L.: B Y D. R. ARTHUR, M.So., From The Department of Zoology
On The Egg of The Tick, Ixodes Ricinus L.: B Y D. R. ARTHUR, M.So., From The Department of Zoology
CONTENTS
PAGE PAGE
1. Introduction . . . . 53 5. D e v e l o p m e n t a n dh a t c h i n g . 57
2. Materials and methods 53 6. S u m m a r y . . . . . 59
3. The egg—general features 53 References ' . . . . . 60
4. The membranes of t h e egg . 56
100 7-1
0-50 mm.
O'lmm.
0-5 m m.-
-Y.P.
6c
0"5mm.
Fig. 1. The egg of Ixodes ricinus L. Fig. 4. Initial visible differentiation of egg {dorsal view).
Fig. 2. Transverse section of egg membranes of Ixodes Fig. 5. Initial visible differentiation of egg (lateral
ricinus L. view).
Fig. 3. Globular contents of egg of Ixodes ricinus im- Fig. 6. Stages in the development of the yolk 'plate'
mediately after oviposition. (see text) from the dorsal aspect.
Key to Lettering: A.P. anterior pole of egg; a.b. air LI, L2, L3, legs 1, 2 and 3; P. palp; S.L. secretory
bubble; cap. capitulum; ch. chorion; che, chelicerae, layer from Gene's organ; V. vitellus; V.g. globules in
overlying hypostome; E.G. embryonic cuticle; E.S. egg contents;' V.M. vitelline membrane; X. initial
excretory sac; Ex. excretory globules; En.ch. endo- area of visible differentiation; Y.P. yolk 'plate', as
chorion; Ex.ch. exochorion; g.m. granular material; seen in dorsal view.
D. R. ARTHUR 55
crevices, or in the centre of the egg mass, results in a Bischoff (1927) is of the opinion that the increase is
certain amount of flattening. due to the intake of food material by the embryo,
All measurements were made on fresh eggs under but the writer believes that it is due to the absorption
a binocular microscope. The length was measured as of water from the surrounding medium, the signifi-
a straight line joining the two poles of the egg, and cance of which will be dealt with later, in connexion
the width as the greatest diameter of the egg midway with the cuticular membranes. It has been shown
between the two poles. In / . ricinus the eggs were by McLeod (1935)i Milne (1944) and others that the
measured at three stages of development, com- maintenance of high humidity (over 80 %) in the
parable samples being taken in each case. The stages microclimate is essential for the development of the
were measured as follows: immature stages of this tick, including the egg phase.
(1) Freshly laid eggs. From the time of oviposi- It is well known that eggs of ticks soon shrivel up,
tion to 24 hr. later. with the collapse of the egg wall, under dry condi-
tions. It is of interest to note that the eggs of the
(2) Partially developed eggs. At about the 33rd- majority of the insects, in which this size-increase
35th day after oviposition. phenomenon has been observed, develop under con-
(3) Fully developed eggs. Usually from batches ditions of high humidity, in many cases approaching
from which some eggs had already hatched. saturation point.
Table 1. Length of eggs of Ixodes ricinus (in mm.)
Frequency in mm. Total p. « *
Standard
no. oi J\T lulllllUlyll error oi
0-52 0-54 0-56 0-58 0-60 0-62 0-64 samples mean deviation
mean
(1) Freshly laid eggs 3 12 37 64 49 14 1 180 0-575 0-20 0-015
(2) Eggs on 33-35 day — 17 19 32 78 31 3 180 0-586 0-17 0013
of development
(3) Fully developed — — 1 23 49 22 5 100 0-597 0-017 0-0017
eggs (actual)
(4) Fully developed — — 1-8 41-4 88-2 39-6 9 180 — — —
eggs based on 180 (estimated)
samples
Table 2. Width of eggs of Ixodes ricinus (in mm.)
Frequency in mm. Total Standard
» QJ. — — J — — J
Tin of A P L UlLLLLXj vlx
The frequency distribution of the samples with In Tables 3 and 4, on the basis previously in-
regard to the length and width are presented in dicated, the length and breadth of the eggs of
Tables 1 and 2 under 0*2 mm. magnitude classes. I. ricinus, I. hexagonus and / . canisuga are given
There is an apparent departure from normality due for comparative purposes. All dimensions apply to
to the grouping effect, and the means are calculated eggs oviposited up to 24 hr.
as for a normal population distribution. From these Whilst it has been shown (Tables 1 and 2) that
data it is seen that the egg increases in size with there is a variation in size between eggs at various
development. The length increases from 0-575 to stages of development, it is equally apparent from
0-597 mm., a total mean increase of 3-8 %; but there Tables 3 and 4 that there is a variation in egg size
is no indication if this differs before and after the both between the three species of the genus and
33rd-35th day period. Correspondingly there is an between those of individuals of the same species
increase in width from 0-440 to 0-449 mm., a total directly on oviposition. In one case, for example, it
mean increase of 2-04 %, this being twice as marked was noted that from an exceptionally laterally dis-
before the 33rd-35th day as after. tended and dorso-ventrally depressed female of
The swelling of eggs, bounded by a firm pellicle I. ricinus the mean length of the eggs directly on
such as the chorion, is a relatively rare occurrence, oviposition was 0-70 mm., with a range from 0-65
although it has been recorded by some authors in to 0-75 mm., and the mean breadth of 0-49 mm. with
particular in the Orthoptera, Dermaptera, Rhyn- a range from 0-47 to 0-54 mm. As development
chota, Hymenoptera, Coleoptera and Diptera. proceeded, the examination of the eggs showed the
56 On the egg of the tick, Ixodes ricinus L.
increase to be of the same order as that indicated in the egg it is commonly seen as a thickened en-
Tables 1 and 2. Despite the existence of this varia- velope showing a distinctive laminated appearance
tion in the eggs, there is no evidence from the infor- (Fig. 11).
mation collected that the egg size varies according Each egg is surrounded by a secretion immedi-
to the time at which they are deposited during the ately on oviposition, this being produced by Gent's
oviposition period, i.e. between those deposited at organ (Nuttall, 1911.). I t has been observed pre-
the commencement and the end of the ovipositing viously that, following damage to this organ, ovi-
season. position ceases for a while and, when continued, the
Immediately after egg deposition the individual eggs are laid directly from the oviduct. Such eggs
egg of/, ricinus weighs 0-00006 g. axe not covered with a secretion, with the result that
Table 3. Length of eggs of Ixodes ricinus, I. canisuga and I. hexagonus (in mm.)
Frequency in mm.
No. of Arithmetic
Species 0-48 0-50 0-52 0-54 0-56 0-58 0-60 0-62 0-64 samples mean
/ . ricinus 3 12 37 64 49 14 1 180 0-575
I. canisuga 12 32 35 189 43 12 0 2 325 0-540
I. hexagonus 3 2 79 140 199 54 3 1 481 0-558
Table 4. Width of eggs of Ixodes ricinus, I. canisuga and I. hexagonus (in mm.)
Frequency in mm.
No. of Arithmetic
Species 0-39 0-41 0-43 0-45 0-47 0-49 0-51 samples mean
/ . ricinus 14 39 47 100 0-44
I. canisuga 5 49 326 60 2 442 0-43
I. hexagonus 2 0 2 163 24 13 1 224 0-44
they soon shrivel and dry up. Similar observations
4. T H E MEMBRANES OF T H E EGG were apparent when Gent's organ was not pricked
When the egg is laid direct from the oviduct it is en- but simply stimulated with a fine glass rod. Gen6
closed by two envelopes, the chorion and the vitelline (quoted by Nuttall, 19^.1) supposed that in addition
membrane. The egg shell, or chorion, consists of two to covering the egg, this secretion has the further
layers, the exo- and endochorion (Fig. 2), which function of hardening the 'chitinous' envelope of
differ in structure and properties. The exochorion is the egg, and that the organ may convey spermatozoa
applied like a thin varnish over the egg surface and in some way from the female uterus to the egg as she
stains less deeply with acid fuchsin than does the is laying. This secretion forms an additional layer to
endochorion. I t is less compact than the latter and the egg membranes, although it is derived from
in some examples is only feebly developed. The endo- accessory glands. Probably this secretion also acts
chorion, lying beneath the exochorion, is a relatively as a cement to hold the eggs together in a cluster.
thick, opaque, elastic layer, which gives the egg its Single eggs, or small clusters, may be removed from
shape and partly its consistency and it may be re- the parent cluster by means of a needle, and if care be
garded as the 'egg shell'. I t is of nearly uniform taken, the exochorion need not be torn or visibly
structure and thickness over the whole egg. In some damaged. Further, if after being so separated, eggs
cases it has been noted that the exochorion peels off are examined, no mark indicating where the eggs
with the swelling of the eggs, and there is some have been in contact can be seen.
evidence that between the exo- and endochorion Individual eggs, removed from the parent cluster
there is an oily or lipoid layer. At least it can be said with care, show the surrounding gel-like layer, which
that the two membranes are quite unconnected and in a saturated atmosphere appears to attract
that the exochorion, when removed, leaves the endo- moisture, and globules of water may be found
chorion with a shiny, smooth, glistening surface. adhering to it. When immersed in solutions of NaCl
Within the chorion one finds the vitelline membrane, (0-001-0-06 %) the secretory covering swells up to a
which is clearly visible when the egg is mounted. width considerably greater than that of the chorion
Initially the vitelline membrane appears as a itself. I t appears, however, to be of a waxy nature
structureless basement membrane which is closely because, if egg clusters are treated with ether, they
adherent to the cortical layer of protoplasm beneath rapidly disintegrate. The removal of a portion of the
it. During the early stages the vitelline membrane secretory layer results in an increased loss of moisture
came away with the chorion when the latter was and, where such an area is extensive, the egg be-
dissected from the egg. With the development of comes desiccated.
D. R. ARTHUR 57
embryonic dorso-ventral curvature of the whole
5. DEVELOPMENT AND HATCHING length of the body. Again, the mouthparts are not
From a survey of the literature it would appear that visible when viewed dorsally.
the only controlled experiments on the development The following observations on the process of de-
of the egg of / . ricinus are those by Olenev (quoted velopment of the tick egg to the hatching stage were
by McLeod, 1935). He observed that whereas under undertaken on living eggs which were maintained in
natural conditions eggs took 8 weeks to hatch, under the laboratory at temperatures ranging from 16 to
artificial conditions at 25-30° C. they hatched in 23° C. in a saturated atmosphere. The preoviposition
3 weeks. Death ensued when the relative humidity period varies with the season and with the individual,
0-5 mm.
0-5 mm.
0-5 mm. —ch.
Fig. 7. Lateral view of developing tick in egg between Fig. 86. Dorsal view of egg, showing excreta visible
30 and 39 days at conditions of experiment (see text). through the integument (37-43 days). (Key to
Fig. 8a. Lateral view of developing tick between 39 and lettering on p. 54.)
61 days at conditions of experiment (see text).
fell below 80 %. McLeod (1935) has shown that the but usually lasts 15-22 days (McLeod, 1935).
lower limiting humidity for egg development cor- Detailed observations on the early development
responds with the later stages, being in the neigh- phases of the living eggs are not possible owing to the
bourhood of 80% saturation. Under the latter density of the internal contents. A contraction of
conditions it has been shown (Arthur, 1945) that the the cytoplasm and yolk from the anterior pole is the
head of the emerging larva is flexed ventrally and is first external evidence of development; this when
not visible from the dorsal aspect. This is not so at seen dorsally is in the form of a crescent with back-
or near maximum saturation limits according to wardly directed horns (Fig. 4). Laterally the
Campbell (1946); the latter also notes that when eggs direction of development is ventro -posteriorly and is
are subjected to temperatures above 25° C, a most emphasized in this plane (Fig. 5). The process of
typical abnormality encountered in those individuals external change is a gradual one and follows the
which survived and hatched is a persistence of the path indicated by the arrows in the figure. Dorsally
58 On the egg of the tick, Ixodes ricinus L.
there appears to be a distinct 'plate' (Fig. 6a-c) forcing the blastoderm cells, hitherto distributed
which, with increased differentiation, shows a uniformly to fill the space that is left'.
gently concave anterior border, this concavity be- The legs in their first stage are unsegmented and
coming more accentuated as development proceeds. enclosed within a membrane, the first or' embryonic'
This plate corresponds to the dorsal distribution of cuticle which surrounds each limb in an unsegmented
the vitellus in the egg. The less dense layer im- sac (Fig. 7). Owing to the shortness of the sacs the
mediately anterior to the yolk 'plate' corresponds legs are sinuate. When seen from the ventral view
to the future cephalothorax and appears to be the the appendages are closely apposed to one another
0-5 mm.
12
0-60 mm.
Pig. 9. Ventral view of developing tick in egg to show Fig. 11. Section through the egg membranes at the
position of mouthparts. hatching stage showing thickened vitelline membrane
Fig. 10. The same embryo as seen at the anterior pole, (compare with Fig. 2).
showing the capitulum and palps orientated at 90°.to Fig. 12. Larval tick preparatory to emergence. (Key to
the longitudinal axis of the egg. lettering on p. 54.)
centre of differentiation. When once this has com- and to the body generally. The first pair of legs lie
menced its activity, it provides the focus from which close against each other on either side of the mid-
all subsequent processes of development spread, ventral line. The tips of the second pair are almost
although in an undeveloped egg it displays no visible level with those of the first pair and the third pair of
difference from any other part. A similar centre to legs extend further to the posterior.
this is present in insects (Wigglesworth, 1939), which Thirty to thirty-five days after oviposition a
is said to act' not by giving out a diffusible substance, number of globules are visible in the internal brown
but by initiating a contraction wave in the yolk mass. From a lateral view these globules are
system, spreading forwards and backwards and arranged in the form of a horseshoe (Fig. 7), the
D. R. ARTHUR 59
ventral limb of which leads to the neighbourhood of In the pre-eclosion phase the larva extends the
the apex of legs 1 and 2. By the 37th-43rd day, posterior part of the body against the chorion, and
when viewed under reflected light, the eggs show an the initial splitting takes place at this posterior point
extensive white area (Figs. 8a, 6), in the vicinity of from whence it passes forwards. The initial force
the tips of the legs. This white mass consists of employed to break open the egg appears to be
globules of uric acid, enclosed in a sac formed at the muscular, the posterior border of the abdomen lies in
junction of the gut and the Malpighian tubules. This close apposition to the chorion and any abdominal
sac, when distended with this excreta, is readily muscular movements would tend to increase the
visible through the transparent egg shell. The afore- force against the shell at this point (Fig. 12). There is
mentioned globules, arranged in a horseshoe pattern reason to believe that the rupture of the egg shell
(Fig. 7), are the initial waste products on the way to along the longitudinal axis forms a distinct line of
the sac. The legs now show distinct evidence of weakness, as similar cleavages have been obtained
segmentation, and at this stage the capitulum and by the treatment of newly deposited eggs with dilute
palps are clearly visible, lying at an angle of about 90° and concentrated acids.
to the longitudinal axis of the tick body (Figs. 9,10). No air appears to be swallowed after hatching.
During the 48 hr. before emergence, the body of The posterior end of the body invariably emerges
the tick comes tofillthe egg more completely, and is first, and the anterior portion may be retained for
bathed in the amniotic fluid. Occasionally, rhythmic some hours within the egg shell. Ultimately, by slow
movements of the head are seen, and it is suggested movements of the legs, the entire body comes out
that at this period the larva swallows the amniotic and the larva crawls a short distance from the egg
fluid in much the same way as insects do. The gut is shell. At the experimental conditions referred to in
filled with the remains of the vitellus in the form of the present paper, the ticks remained quiescent for
small globules and granular material. When the 5-10 days. During eclosion the excretory sac is
amniotic fluid mixes with the gut contents the small charged with waste matter, and the newly emerged
globules unite to form relatively large droplets. All larva continues to discharge the contents over a
the free fluid in the egg is consumed and the larva period of several days until the sac is completely
increases considerably in size before hatching. emptied. Elimination of excretory products usually
Within 24 hr. of hatching the outward form of the begins at the time of hatching, and frequently a
egg changes, becoming longer and thinner. Pre- quantity of waste material remains in the egg shell.
paratory to emergence the mouthparts are directed After emergence the gut undergoes a well-defined
forwards and are but slightly depressed ventrally series of changes, simultaneously with the process of
from the longitudinal axis. This depression is also excretion and hardening of the chitinous integu-
a common feature in mature larvae. The legs, having ment. In the newly emerged larva the gut fre-
now ruptured the ' embryonic' cuticle, are no longer quently appears as a simple sac charged with yolk
apposed to the body (Fig. 12). (the 'plate' observed earlier), but within a short
Air enters the egg, presumably by diffusion period of time the yolk is mostly digested and the
through the shell, and occasionally some air may be typical lobed appearance is assumed. Essentially
swallowed by the larva. This, however, is not a con- comparable developmental processes are apparent in
stant process and does not seem to play an essential I. hexagonua and I. canisuga, and the process of
part in the mechanism of hatching. According to hatching is similar in all three.
Sikes & Wigglesworth (1931) the swallowing of air
may (i) distend the larva while still inside the egg,
and so assist the movement of body fluids; (ii) in 5. SUMMARY
those cases in which the larva escapes from the egg The egg of Ixodes ricinus L. is described, and the
while still enclosed in the embryonic cuticle, it may increase in size during development is noted. It is
swallow air a second time, blowing itself up until the suggested that the increase is due to the absorption of
cuticle is forced to split; and (iii) the young larva may water. The egg wall consists of exo- and endochorion
swallow air until its skin has stretched and attained with a thin vitelline membrane, which becomes
a size much greater than the egg from which it came. thicker as development proceeds and assumes a
The two latter considerations do not apply to the laminated appearance. The secretion layer of Gend's
tick I. ricinus, and the inconstancy of the swallowing organ is described, and appears to function as a
of air does not lend much support for (i). cement for holding the eggs together in the cluster.
There is no evidence in the tick that there is an Chemical tests show it to be of a waxy nature.
increased pressure inside the egg consequent on It is deduced from experimental evidence that the
embryonic development. The egg is turgid, and egg shell is not absolutely rigid, and the weight of
though it can be deformed by external pressure at evidence favours the view that the shape of the egg
this advanced stage without any effect on the larva, shell is maintained by the internal pressure of the
the shell returns to its normal shape by its elasticity. egg contents, and the elasticity of the shell.
60 On the egg of the tick, Ixodes ricinus L.
The development processes as seen in the living for supplies of material; to Mr T. W. Tyssul Jones,
egg are described. Hatching from the egg shell is M.Sc, for his assistance in checking the measure-
brought about by a muscular force acting on a ments of the egg dimensions, and to Mr L. Cowley,
limited area at the posterior pole of the egg. M.Sc, Assistant Curator (Department of Zoology),
National Museum of Wales, and Dr P. Tate, Molteno
The writer is indebted to Mr Robert David, of Institute of Parasitology, Cambridge, for reading the
Longlands Farm, Pyle, Dr A. D. Lees, of the Agri- original script and for making many useful sugges-
cultural Research Council, and Mr Simeon, of the tions and modifications.
Glamorgan War Agricultural Executive Committee,
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