AORIOTYPUS ARMATUS AND ITS RELATIONS WITH ITS HOSTS. 451 23. Agriotypus armatus (Walk.) (Hymenoptera) and its Relations with its Hosts. By KATHERINE FISHER *. [Received February 16, 1932 : Read April 5, 1932.1 (Text-figures 1-8.) INTRODUCTION. Of all the dozen species of Hymenoptera known to be aquatic in habit, one of the largest and, perhaps, most interesting is Agriotypus armatus. First found on the Clyde by Dr. Walker, and described by Curtis in 1832 (3), it was not until 1858 that it was recognized by von Siebold (11) as a parasite of Trichoptera. Since that time many attempts have been made to elucidate its life-history, notably by Klapalek (6) in 1889, and quite recently by Clausen (2), who dealt with a closely related species, A. gracilis (Waterston), which is found in Lake Hakone, Japan. My first introduction to the insect was in the spring of 1929, when I found two females crawling up the side of a basin in which I was rearing caddis-flies of the genus Silo, taken from a small stream in the Hindhead district in Surrey. At first I thought them to be ordinary Ichneumonids which had fallen into the water by mischance, but peculiarities in their appearance led me to show them to Mr. 0. W. Richards, of the Entomology Department, Imperial College of Science, who confirmed my suspicion that they were Agriotypus armdw. During the following winter I made a collection of cases of Silo pallipes in which the curious band-like appendage advertised the presence of the para- site (text-fig. 1, a). On opening some of the cases I found that the insect hibernates, not in the form of a pupa, as had previously been supposed, but as an imago. The fact that it spends the winter beneath a foot of water as a fully developed adult with open spiracles led me to believe that the band- like appendage to the case, which has been so frequently described and illustrated, must be in the nature of a respiratory device, and I determined to attempt to rear the species in captivity and put on record the various stages in its life-history. This task was rendered far from easy by the extreme delicacy of the host, and it is only now, at the end of two years, that I am able to give even a tolerably complete account of the development of the parasite. TECHNIQUE. A number of parasitised and unparasitised cases of Silo pallipes taken from the Hindhead stream, and also of Goera pilosa from the Lambourne River, near Newbury, were kept in tanks with six inches of running water, and various water-weeds and floating objects were supplied for the convenience of emerging parasites. Under these circumstances it was possible to watch the females descending into the water to lay their eggs and to watch mating take place. When the host lam= or pup= had been infected, they were placed in glass tubes 2-3 mm. in diameter (inside) and 15-20 mm. long, drawn out slightly at one end and weighted down on either side with pebbles stuck on by means * Communicated by Prof. F. BALFOUE-BROWNE, M.A., F.Z.S. PROO. ZOOL. 80&-1932. 30
Transcript
AORIOTYPUS ARMATUS AND ITS RELATIONS WITH ITS HOSTS. 451
23. Agriotypus armatus (Walk.) (Hymenoptera) and its Relations with its Hosts. By KATHERINE FISHER *.
[Received February 16, 1932 : Read April 5, 1932.1
(Text-figures 1-8.)
INTRODUCTION. Of all the dozen species of Hymenoptera known to be aquatic in habit,
one of the largest and, perhaps, most interesting is Agriotypus armatus. First found on the Clyde by Dr. Walker, and described by Curtis in 1832 (3), it was not until 1858 that it was recognized by von Siebold (11) as a parasite of Trichoptera. Since that time many attempts have been made to elucidate its life-history, notably by Klapalek (6) in 1889, and quite recently by Clausen (2), who dealt with a closely related species, A. gracilis (Waterston), which is found in Lake Hakone, Japan.
My first introduction to the insect was in the spring of 1929, when I found two females crawling up the side of a basin in which I was rearing caddis-flies of the genus Silo, taken from a small stream in the Hindhead district in Surrey. At first I thought them to be ordinary Ichneumonids which had fallen into the water by mischance, but peculiarities in their appearance led me to show them to Mr. 0. W. Richards, of the Entomology Department, Imperial College of Science, who confirmed my suspicion that they were Agriotypus armdw.
During the following winter I made a collection of cases of Silo pallipes in which the curious band-like appendage advertised the presence of the para- site (text-fig. 1, a). On opening some of the cases I found that the insect hibernates, not in the form of a pupa, as had previously been supposed, but as an imago. The fact that it spends the winter beneath a foot of water as a fully developed adult with open spiracles led me to believe that the band- like appendage to the case, which has been so frequently described and illustrated, must be in the nature of a respiratory device, and I determined to attempt to rear the species in captivity and put on record the various stages in its life-history. This task was rendered far from easy by the extreme delicacy of the host, and it is only now, at the end of two years, that I am able to give even a tolerably complete account of the development of the parasite.
TECHNIQUE. A number of parasitised and unparasitised cases of Silo pallipes taken
from the Hindhead stream, and also of Goera pilosa from the Lambourne River, near Newbury, were kept in tanks with six inches of running water, and various water-weeds and floating objects were supplied for the convenience of emerging parasites. Under these circumstances it was possible to watch the females descending into the water to lay their eggs and to watch mating take place.
When the host lam= or pup= had been infected, they were placed in glass tubes 2-3 mm. in diameter (inside) and 15-20 mm. long, drawn out slightly a t one end and weighted down on either side with pebbles stuck on by means
* Communicated by Prof. F. BALFOUE-BROWNE, M.A., F.Z.S. PROO. ZOOL. 80&-1932. 30
452 - .
MISS R. FISHER : AGRIOTYPUS ARMATUS AND
Text-figure 1.
I n)m. . ' Parasitised case of 8. pallipes.
a. Band-like appendage.
Text-figure 2.
Artificial cam coiitaining larva of ho8t.
ITS RELATIONS WITH ITS HOSTS. 463
of Chatterton compound to resemble the natural cases as much as possible (text-fig. 2). Later fully-grown parasite larvae were placed in similar tubes and kept on damp cotton-wool in a Petri dish. Although the mortality in these tubes was high, no insect kept in them surviving ecdysis, they were of considerable value for observing the habits of both host and parasite, and uninfected host larvae lived in them for several weeks.
. LIFE-HISTORY OF THE HOST.
The chief hosts of Agriotypus are three species of Go&Gnce-Go&-a p i h a , Silo pallipes, and Silo nigricornis. It has been reported from Odol-~tocerum albicorne (Odontocerids). I have reared them myself from G. pilosa and 8. pallipes, but although I supplied the female parasites with a number of different species of caddis-larvae outside the Gogrinme, some of which make cases resembling fairly closely those of Goera, they showed no interest in them whatever, even though cases of Goera and Silo were missing and the parasites were ready for oviposition. Several times it happened that the females ovi- posited in the empty cases from which they themselves had emerged in preference to inhabited cases of caddis belonging to other families.
In order to make the life-history of the parasite easier to follow, i t is probably an advantage to begin by giving a short account of that of the host. Silo pallipes is found in swiftly running brooks in hilly districts, the stream from which I take my supplies being about two feet in width and nine inches to a foot deep. Goera inhabits small rivers such as the Colne and the Lambourne but otherwise the life-history of the two species is SO similar that one account will do for both species.
The adult insects begin to appear about the middle of May, and continue to emerge through the summer. The larvae construct their cases by cementing together grains of sand to form a very slightly curved tube, a little narrower behind than in front, and embellished with two or three small pebbles on either side. Those of Silo are very regularly constructed of the finest sand, and measure about 7 mm. by 4.5 mm. Those of Goera are made of much coarser material, less neat in appearance, and their size varies more. In general they are about 13 mm, by 9 mm. In each case the hind orifice is covered by a stout silken web having a small round hole to permit the free passage of water and excreta. The 1arvs spend their time wandering slowly about on the stones a t the bottom of the brook, grazing upon the alge which carpet them. When fully grown they fix the po3terior end of the case to the stones, generally in a crevice or on the under surface, thus closing the anal end. The mouth of the case is closed with a small pebble, which is held in place by little ropes of silk arranged like the spokes of a wheel, so that the water can pass into the case. When about to pupate, Goera spins an additional sketchy cocoon inside the tube. I was able to watch the construction of this cocoon and to examine the fixture of the pebble in the case of one or two individuals inhabitingthe glass tube mentioned earlier.
From a fixing of the case until the occurrence of pupation the larvae undergo a quiescent period which varies greatly in length. Some individuals continue to feed through the winter. Others, more fully developed, fix their cases and hibernate as larvae, to cut themselves free again and to resume feeding the following spring, or else hibernate in the quiescent pre-pupal condition. A few pass the winter as PUPS, and these are the first to emerge as adults in the following May. Throughout larval and pupal life a current of water is kept in motion through the case by regular movements of the men. They may be kept. alive Both larvs and pupae are very delicate.
30*
454 MISS K. FISHER : AGRIOTYPUS ARMATUS AND
for a couple of days if laid on damp cotton-wool, even when they have been removed from the case, but they succumb in a few hours if kept in dirty or badly aerated water. Even in a natural state a fairly high proportion die, especially at the time of pupation, as an examination of a number of cases immediately after they have been taken from the brook will show.
LIFE-HISTORY OF THE PARASITE. The Egg. (Text-fig. 3.)
The habits of the imago when about to lay her eggs will be referred to later on.
Oviposition takes place during the latter part of April and in May. The egg is a long oval, 0.85 mm. x 0.17 mm., and the chorion is transparent, so that the developing embryo is visible through it. It is attached to the skin of the host by a flexible stalk 0.2 mm. in length, which rapidly darkens after ovi-
Text-figure 3.
,?%A
Larva of S. pallipes, with egg of A. awnatus attached.
position, and prevents the egg from being washed away by the respiratory movements of the host. Eggs which I removed from one host and placed upon another were invariably lost in this way. It is usual to find a single egg attached to the host in the region of the second abdominal segment, to one side of the median line ; but it is often placed elsewhere, and is occasionally laid through the end of the case, when it becomes fastened to one of the extremities, or even adheres to the inside of the case itself. A number of eggs are sometimes laid on a single host, and that this is not due to the abnormal conditions of the laboratory is shown by the instance of a larva of X. pallipes, which I took from the Hindhead brook, with six eggs on various parts of its body. Owing to an unfortunate stoppage of the water-supply, which had fatal results both to this host and to another with two eggs on it, I was unable to find out what would happen when the parasite larvae emerged. I have never found more than one individual of any of the later stages on a single host.
The Larva. (Text-figs. 4, 5, & 6.) The life-history of the larva is divided into three stages : the first, in which
i t finds its way from the egg to a suitable position on the host ; the second, which is spent entirely in feeding ; and the third, during which the cocoon and its band-like appendage are spun. Before pupation the larva remains in a quiescent pre-pupal state for some time, but although it is different in outline from the third stage proper, this is not a separate instar, as no ecdysis takes place.
ITS RELATIONS WITH ITS HOSTS. 455
When it first hatches from the egg, the larva exhibits many peculiar and interesting characteristics. The head is large and bluntly triangular, and bears upon its upper surface two stout curved horns directed backwards and a few minute scattered bristles. From the prothorax the segments gradually decrease in size to the 10th abdominal segment, which is bifurcate and bears two straight slender appendages which are strongly divergent and nearly as long as the whole of the rest of the insect. With the exception of the 10th abdominal, each segment has a transverse row of stout bristles of unequal
Text-figure 4.
Second-stage larva : side view.
length on its dorsal surface, a band of short set2 across each sternite, and one or two minute lateral bristles. Both upper and lower bands are interrupted medially in the hinder segments, and the bifurcate anal segment has only a single patch of short bristles on each side *. This first instar is the shortest, lasting not much more than a week, and during this time the larva finds its way from the egg to some spot on the under side of the thorax, where it will be able to feed undisturbed by the continual movements of the abdomen. When, as frequently happens, the host is in the pupal state, it takes up a position
* Clansen (2) gives two excellent figures of this stage in A. gradis , which seems to resemble A . amatus in all essential points.
456 MISS I(. FISREk : AGRtOTYPUS ARU!&7S ANB
beneath the wing-pads, and there commences to feed. Once it has settled it is very unwilling to move again, and if it is dislodged from its place seems to make no effort to regain it. Little increase in size takes place during this instar.
The head The second stage is very different in appearance from the first.
Text-figure 6.
;:: :I KJ. F.
Head of third-stage larva.
is more nearly square and is heavily chitinised, the mouth-parts being well developed and the mandibles being conspicuously toothed. The external armature of curved horns and bristles has disappeared, as have the dorsal and ventral series of set= so noticeable on the body-segments of the young larva. The greatest girth is now about the fourth and fifth abdominal segments, and the slender anal appendages have given place to two stout opposing hooks.
Test-figure 6.
Pre-pupa
i
There are no open spiracles, but the skin is transparent, and through i t the air-filled tracheal trunks, with dorsal and ventral branches in each segment, from the prothorax to the seventh abdominal, can be traced. In the eighth abdominal segment the main tracheal trunks divide into two branches which
ITS RELATIONS WITH ITS HOSTS. 457
diverge backwards through the remainder of the abdomen. The mid-gut is oval and, greatly distended with the yellow blood of the host, fills the main part of the body-cavity as far as the sixth abdominal segment. From here to the anus the hind-gut is faintly visible, but it is always empty, as evacuation of the faeces does not take place until immediately before pupation.
The third instar occurs when the host is almost consumed, and is very similar in appearance to the second. The head is large and quadrate (text- fig. 5), with dark eye-like patches of chitin on each side, and in some specimens minute antennae can be found. The mouth-parts, and especially the labium, are conspicuous, but the tail-hooks, having undergone no increase in size, are very small in comparison with the rest of the body. There is still no trace of open spiracles.
Text-figure 7.
Section of case containing pupa of Agriotypus. a. Inner envelope of cocoon. b. Fsoes and third larval skin.
During the early part of the instar the host is entirely consumed, and its chitinous remains are pushed back into the hinder part of the case, which is immediately cut off by a stout silken partition.
The whole of the rest of the case is then lined with layer after layer of coarse reddish-brown silk, which the larva spins irregularly backwards and forwards until a stout cocoon is formed. If a larva is taken from a caddis- case at this stage, and placed in one of the small glass tubes on damp cotton- wool, it is easy to observe the construction of this cocoon, although the fabric spun under these artificial conditions is not so thick as that found in nature, perhaps owing to the greater area to be covered. The front end of the case is then closed by means of another partition made by spinning round and round the mouth of the cocoon in a gradually thickening ring until the aperture disappears. The band-like appendage is now spun, and as it is made it is
458 MISS K. FIdHER : AOR~O'&PUfl &MATUS AN0
gradually pushed out through a slit in the side of the lid. This appendage consists of an outer layer of wet, closely woven silk, covering a mass of tangled dry silk, like cotton-wool in appearance, and the interstices in the band are in communication with the cocoon. Finally, the cocoon is lined with a very delicate white silk, which forms an inner envelope round the whole insect (text-fig. 7 , a ) . The larva then remains quiescent for a week or ten days, during which time the abdomen becomes more and more constricted about the second and third segments as the pupa forms within it (text-fig. 6) . This is the prepupal stage described by Klapalek (3). The contents of the gut become dark in colour and pass into the hind-gut, whence they are evacuated in a long chain surrounded by a peritrophic membrane just before pupation
The Pupa. (Text-fig. 3).
(text-fig. 7, b) .
During the last days of larval life the outline and eyes of the pupa are visible through the larval skin. Pupation takes place about the end of August. At first the pupa is white in colour everywhere except on the eyes and mandibles, but gradually it becomes darker until it assumes the jet black of the imago. The perfect insect emerges from the pupal skin at the end of Sepbember, but remains enclosed in the cocoon until the following spring.
Respiration while in the Caddis-case. During the first two stages of larval life respiration takes place through
the skin, which is very thin and delicate, and is washed by a continual current of water kept in motion through the case by the abdominal movements of the host.
From the prepupal stage onwards the parasite cocoon is fun of air which is in communication with the air-spaces in the band-like appendage. Through the wet surface of the latter osmosis takes place to keep the air in the cocoon fresh during the eight months the insect spends in the pupal and imaginal states beneath the water. That such an air-supply is necessary may be shown by removing the band-like appendage, in which case the insect dies in the course of a week or less, and also by the fact that when parasite cases are collected from which the appendage has bee6 removed by such accidents as the rubbing together of stones during freshets, the insects bhey contain are invariably dead. Control8 from which the band had been removed, but which were kept on damp cotton-wool instead of under water, sqvived, and emerged at a suitable temperature.
The full-grown parasite larva is much shorter than the host and also a good deal stouter, so that when the host-larva dies and the respiratory current ceases its body fills the whole of the lumen of the case. Between the death of the host-larva and the completion of the cocoon, gas appears in the case. It seems possible that this gas first arises as small bubbles of CO, exhaled from the skin and held hetween it and the walls of the case in such a position that it does not come into contact with the water, and so remains undissolved. When the watertight hind partition of the cocoon is constructed, this gas might pass behind the larva, so forming a gradually accumulating store which wouId eventually fill the cocoon. When the band-like appendage is finished, this CO, could get out of the cocoon entangled in the " cotton-wool " of the band, and, being then in contact with the water through the we6 surface-layer of the band, osmosis would take place to replace the CO, with oxygen.
ITS REUTIONS WTH ITS HOSTS. 459
Habits of the Adult. (Text-fig. 8.) Emergence of the adult insect begins about the second or third day in
April in the laboratory, probably slightly later in the field as it is greatly affected by heat, apparently ceasing when the temperature of the water falls below 13" C. The imago bites off the top of the cocoon and the silk ropes which hold the closing pebble in position on top of the caddis-case, and crawls out of the water by means of any objects which breaks through the surface-film. The females are about twice as numerous as the males, and exhibit considerably greater
Text-figure 8.
9 Adult female of A. asmatw.
activity. Both sexes descend beneath the surface of the water, crawling about on stones and the stems of water-plants. When submerged, they are covered with an air-film, and the antennae and wings are laid back over the body. This air-film probably assists in respiration under water, and is from time to time increased when the insect comes into contact with the small air-bubbles which abound on submerged stones and plants in the highly oxygenated water frequented by Agrio typs . If the amount of air in the film becomes great enough to render the insect so buoyant that walking is difficult, she will stop and squeeze 08 part of it with her hind legs. Every ten minutes or so she is obliged to come up to the surface for a fresh supply of air, and this is done by letting go all footholds and floating to the surface. Considerable diffculty is sometimes experienced in passing through the ourface-film, and I have once or twice observed individuals whose behaviour can most aptly be described as losing their temper with the surface-film, kicking and even
460 MISS K. FISHER : AGRIOTYPUS ARMATUS AN^)
biting it in their struggles to get through. This difficulty probably explains the rather high number of insects found floating and drowned on the underside of the film. Usually they run along the under surface cf the film until they find some stick or stem up which they are able to climb.
Out of the water they are rather sluggish in their habits, especially in cold weather. They do not fly about a t all readily; indeed, I kept a number of adults in a very large tank for over a month without ever shing them fly. A common method of locomotion is to skim over the surface of the water, with the legs outstretched like those of the pond skater, but with the wings in rapid motion to provide propelling power.
In each of three years during which I have observed this insect, the first individual to hatch has been a female, the first male to emerge appearing two or three days later. Mating takes place from a few hours to a couple of days after the emerg3nce of the male. There is no courting, and copulation only lasts for a few seconds, after which the male may immediately go to a second female. Indeed, the whole process is so quickly over that it is rather rarely observed.
About a week after emergence the female begins to take great interest in the cases of the host, and egg-laying commences. The cases appear to be found by means of sight, and are apparently visible to the parasite at a distance of an inch. When a suitable case has been found, the female inserts her ovi- positor into the small aperture a t the anal end of the case and gives the host a sharp poke. If the latter is in an active state it will immediately come out of the fore end of the case with a jerk, when the parasite will leave it for another. After several attempts the female finds a case containing a quiescent prepupa or pupa, and, piercing the case with her ovipositor, she lays an egg on the insect within. If she is unable to break through the case itself she will sometimes lay an egg through the hole a t the end, or between the strands which hold the " lid ') of the case in position.
The male and female are very similar in appearance, the latter being stouter, slightly larger, and having shorter antenna The wings in the female are also a little more cloudy than those of the male. Parasites reared from the cases of Goera are somewhat larger on the average than those from Xilo, but there are all stages in between, and the insects from the different hosts pair readily.
DISTRIBUTION. It has
been recorded from Scotland, Devon, Surrey, Berks, and Hants in this country, and from Bohemia, Sweden, Belgium, and Southern France (Mentone) on the Continent. Quite recently a new but olosely related species, Agriotypus gracilis (Waterston), has been found in Japan, which is particularly interesting inasmuch as it parasitises a lake-dwelling caddis instead of being restricted to brooks and small rivers, as is apparently the case with A . armatus. Further information is needed on the question of distribution, but it is likely that it may be found wherever suitable hosts exist.
I should like to take this opportunity of thanking Professor F. Balfour Browne for his kindness in assisting me in the preparation of this work for publication, and for his interest and advice during the period covered by my observations. My thanks are also due to E. M. E. Mosley for valuable information about the species of Trichoptera mentioned.
Agriotypus armatus appears to be local, but widely distributed.
fTS RaLATIONS W T H ITS HOSTS. 461
BIBLIOGRAPHY. 1. BROCHER. 2. CLAUSEN. (1931.) Biological Observations on Agriotypus. Proc. Ent. SOC. Wash. vol. xxxiii.
3. CURTIS. (1832.) Ayiiotypus ormatus. British Entomology, no. 389. 4. FITCH. (1884.) Review of Literature on A. armatus. The Entomologist, vol. xvii. June
5. HOLXGREN. 6. KLAPALEE. (1889.) Life History and Distribution. Ent. Monthly Mag., August 1889. 7. KOLLAR, V. (1857.) Beitrag zur Kenntnim iiber die Geographische Verbreitung de
8. MULLER. (1889.) Ueber A. aimatus. Zool. Jahrbuch Syst. 4 Bd. 9. MULLER. (1890.) Noch einnial A. armatus. Ebenda, 5 Bd. 1890.
L’Aquarium de Chambre, p. 404.
no. 2.
1884. (1858.) Oefvers. K. Vet.-Akad. Forhandl. t. xv. p. 354.
11. VON SIEBOLD. (1858.) Ueber A. armatua. Amtl. Bericht d. Versamml. d. Naturforsch. in
12. VON SIEBOLD. (1861.) Ueber A. armatus. Stettiner Ent. Zeitschrift, p. 189. 13. WALKER. (1835.) Entomological Magazine, 1835, vol. iii. p. 412. 14. WESTWOOD. Trans. Ent. SOC. Lond. ser. 3, vol. i. p. 170.
