Observations on the ova and larvae of Netelia vinulae (N. cephalotes Holmgren) (lchneumonidae: Tryphoninae), a gregarious ectoparasitoid of the Puss moth caterpillar, Cerura vinula L.
Hymenopteran parasitoids may attack the ova, caterpillars or pupae of Lepidoptera. They may be solitary or gregarious, and feed inside the host's body (endoparasitic) or at the surface (ectoparasitic). An earlier article (Ellis, 1996) described the life-history of the braconid Microplitis ocellatae, a gregarious endoparasitoid of the Poplar hawk-moth caterpillar. In contrast, the present paper is concerned with the ichneumonid Netelia vinulae, which is a gregarious ectoparasitoid of the Puss moth caterpillar.
Parasitised Puss moth caterpillars
Over the years I have observed numerous Puss moth caterpillars, but it was not until 9th August 1995 that my attention was first drawn to the remarkable ova of this parasitoid, when I found seven Puss moth caterpillars feeding on willow near Hadston Scaurs, Druridge Bay, Northumberland (NU 278008). Most of these were immature, but one, in its final instar, had 18 shiny jet-black ova firmly fixed to the integument just behind the head. These were located dorsally and laterally in three rows with six ova in the intersegmental groove between the second and third abdominal segments and three between the first and second abdominal segments. Clearly the ova had been strategically placed out of reach of the caterpillar's mandibles (Plate1). None of the smaller immature caterpillars examined appeared to be parasitised. I revisited the location about a month later on 6th September and found six final instar Puss moth caterpillars, two of which had parasitoid ova attached to the thoracic region.
Plate 1 - Shiny black Netelia vinulae ova attached to the integument of a mature Puss moth caterpillar in the second/third thoracic and third/first abdominal inter-segmental grooves, 10th August 1995.
At the time, that only final instar caterpillars were affected seemed highly significant, since there were no further ecdyses possible to give the opportunity for the caterpillar to rid itself of the parasitoid ova along with the exuviae. But, as will be described later, sometimes immature caterpillars are attacked by the parasitoids and at least some ova, because of their special form of attachment, which are not removed by any subsequent ecdyses.
Fate of Puss moth caterpillar
I collected the initial affected caterpillar on 9th August 1995 and this continued to feed on willow leaves. Each ovum was firmly attached by a black thread-like structure which penetrated the integument and then re-emerged to terminate on the outside in an irregular enlargement. Thus a firm anchorage was effected as though each ovum had been sutured in place.
The parasitoid larvae commenced hatching on 12th August 1995. Hatching occurred at the site of a split at the free pole of the ovum and took several days when only the head and part of the segmented body of the larva projected (Plate 2). By the time the last larvae were emerging the earliest to hatch (from the groove between the second and third thoracic segments) were much enlarged and visibly green through the integument indicating they had been feeding on the caterpillar's haemolymph as an ectoparasitoid. The heads of the parasitoid larvae remained lighter in colour. After hatching the larvae remained clustered together on the thorax of the caterpillar reminiscent of piglets with their heads all "stuck in the feeding trough".
Plate 2 - Close up of anterior of Puss moth caterpillar showing hatched and hatching green Netilia vinulae larvae. Earliest larvae to emerge now enlarged. 16th August 1995. Dorso-lateral view, caterpillar's head to right.
By the 17th August the caterpillar had become an unusual brownish-red colour and had been making an unsuccessful attempt to form a cocoon. the parasitoid larvae continued to feed externally and increase in size, becoming greyish (Plate 3). By the 20th August the attempts to form a cocoon ceased and the moribund caterpillar lay on its side at the bottom of the cage, with the collection of larvae still feeding at the surface. commencing 20th August the parasitoid larvae began to leave the caterpillar. On 27th august the caterpillar was more or less dead, but still twitched if touched. The parasitoid larvae now appeared enlarged and swollen and measured l0mm to 12mm in length. By 13th September the caterpillar was empty and flat. the parasitoid larvae continued to wander around the cage ignoring twigs, leaves and a layer of peat-free compost provided for possible pupation sites. They became desiccated, more creamy coloured and most died. Clearly the conditions provided were unsuitable. On the assumption that pupation in the wild occurred within the puss moth cocoon, the few remaining larvae were placed in a small container, but these also died without pupating.
Plate 3 - Cluster of nearly mature Netelia vinulae larvae feeding externally on the moribund Puss moth caterpillar. Parasitoid larvae are now greyish and with a black mid-dorsal line and segmental patterning. 19th August 1995.
About this time I met Dr Ian Gauld at the British Association Meeting, that year held in Newcastle-upon-Tyne, and from what I was able to describe to him he suggested that the parasitoid was probably Netelia vinulae. Reference to Shaw & Askew (1976), revealed that N. cephalotes (= N. vinulae), a member of the subfamily Tryphoninae, is a well-recognised parasitoid of Cerura vinula and that the ova of Tryphoninae "are partially embedded in the integument of final instar larvae" and that "the eggs are usually placed on the thoracic segments or in some other position from which the host cannot easily dislodge them". It seems that the parasitoid N. vinulae is unique amongst the Netelia in being gregarious and that Tryphoninae are unique amongst ichneumonids in modification of their ova to provide an anchorage stalk (Gauld & Bolton, 1988). I have examined numerous Puss moth caterpillars throughout Northumberland, but have no further records of this parasitoid at other locations.
Dr Mark Shaw confirmed the identity of the parasitoid from photographs I sent to him in March 1996 and explained that although the female parasitoid generally only oviposits onto final instar host caterpillars, this was not invariable. Penultimate instar caterpillars could rarely be affected, when the method of anchorage of the parasitoid ova was sufficiently strong as to prevent their loss with the exuviae. However Dr Shaw related to the possible subsequent survival time of the caterpillar so that was sufficient for it to be able to form a cocoon before succumbing to the attentions of the parasitoid larvae. My caterpillar specimen died before it constructed a cocoon and the parasitoid larvae subsequently wandered off and died. Given ideal circumstances the timing of events would permit the formation of a cocoon by the caterpillar within the confines and protection of which the parasitoid larvae construct their own cocoons. Left in the open the parasitoid larvae soon desiccate and fail to form their cocoons, as I observed in the present case. My attempt to initiate cocoon formation by confining the few parasitoid larvae in a small container was unsuccessful - presumably I tried too late or the container did not simulate the required conditions. Presumably it is essential that there is a cocoon with a moribund caterpillar to provide the correct textural or chemical stimuli to initiate cocoon formation by the parasitoid larvae. This particular Puss moth caterpillar was heavily parasitised with 18 ova attached and possibly was overwhelmed by the large number of parasitoid larvae feeding on it before it could construct its cocoon.
Parasitisation of immature caterpillars
The following year I revisited the locality on 17th August 1996 and found three parasitised Puss moth caterpillars at the original site plus a further six at a nearby clump of willows. The nine caterpillars carried a total of 46 ova. Eight of the caterpillars had only four or five ova attached to the thoracic region. On the ninth caterpillar, which was mature, there were 11 ova attached to the thoracic region and to the intersegmental groove between ' the first and second abdominal segments. Interestingly, five of the nine caterpillars were immature and awaiting the penultimate or final ecdysis. I observed one immature caterpillar with four attached ova undergo ecdysis over the period 17th to 18th August and all of the ova remained attached.
Dr Mark Shaw required some living adult N. vinulae to undertake experiments to determine the possible effects of venom on the host caterpillar and all of the collected parasitised caterpillars were sent to him on l9th August for that purpose. I was thus unable to study the life-cycle further. However Dr Shaw later informed me that the resultant adult parasitoids commenced emerging the following year in mid-June 1997 and that he was able to carry out a number of experiments, the results of which will be reported elsewhere. Suffice to note that as described here the anchored ova were able to survive the caterpillar's ecdyses.
Netelia cephalotes seems an appropriate name for this parasitoid, cephalotes referring to the large head of the species which is related to the considerable musculature required for the adult to chew its way out of the very tough cocoon of the Puss moth. However, it seems that Netelia vinulae is the current correct appellation.
Effect of parasitoid on the Puss moth population
This is difficult to assess. The number of parasitised caterpillars found at one time does not give an accurate indication of the degree of parasitisation. My experience suggests that N. vinulae is an infrequent and localised species here in the north-east. Nevertheless, where it occurs it must have some effect on the density of the local Puss moth population. Since the parasitoid is host specific, then for the long-term survival of both species there must be some overall balance between parasitoid and host numbers.
N. vinulae is a gregarious ectoparasitoid which is host specific for Puss moth caterpillars with synchronised univoltine life-cycles. The parasitoid is remarkable for its egg-laying dual strategy. Firstly, ova are deposited on the anterior (mainly thoracic) segments of the caterpillar out of reach of the caterpillar's mandibles, and secondly, each ovum is provided with a suture-like extension which firmly anchors it in position, thus preventing it being cast off with the exuviae during ecdysis. Observations indicate that the host caterpillar has to be able to survive long enough for the feeding parasitoid larvae to reach maturity, and to be able to form its cocoon, within the protection of which the parasitoid larvae can form their own cocoons and pupate. The feeding demands of an excessive number of parasitoid larvae may overwhelm the caterpillar before it is able to form the necessary cocoon.
I am indebted to Dr Mark Shaw, the Royal Museum, Edinburgh for his continued help and encouragement and for the determination of the parasitoid Netelia vinulae.
Ellis, H.A. (1996). Observations on Microplitis ocellatae Bouche (Braconidae: Microgastrinae), a gregarious endoparasitoid of the Poplar hawk-moth caterpillar, Laothoe populi Linn. Bull. Amat. Ent, Soc. 55: 199-202.
Gauld, I.D. & Bolton, B. (1988). The Hymenoptera. British Museum (Natural History). Oxford University Press, London. p. 201.
Shaw, M.R. & Askew. R.R. (1976). Parasites. In: The Moths and Butterflies of Great Britain and Ireland. Vol. 1 pp. 240-56. Ed. J. Heath, Harley Books, Essex.Originally published in the Volume 57 of the Bulletin of the Amateur Entomologists' Society.
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