Ecological Entomology (1992) 17, 299-302

The first parasitic Trichoptera A L I c E w E L L s Northern Territory Museum of Arts and Sciences, Darwin, NT, Australia

Abstract. 1. A parasitoid habit is confirmed in larvae of an Australian micro- caddisfly. Orthotrichia muscari Wells, being the first known incidence of this habil in the order Trichoptera.

2. Larvae of 0.muscari are non-specific parasites of pupae of other caddisfly species.

3. 0.muscari is in an Australian/New GuineadSE Asian species group in Orfhofrichia, all members of which probably share the habit. Their larvae and pupae have atypical features that are interpreted as adaptations to their uncharacteristic niche.

Key words. Trichoptera, Hydroptilidae, Orfhotrichia, parasitoid.

Introduction

Until now no parasitic Trichoptera were recognized. How- ever, cased pupae of members of the aberrans species group of the micro-caddis genus Orthotrichia (Family Hy- droptilidae) were often found within pupal shelters of other caddis species and raised suspicions that this group could be parasitic. Recently, final instar 0.muscari larvae of assorted sizes and pupae (indentities confirmed from mature pupae, i.e. pharate adults, and larval exuviae) were discovered inside the intact cased pupal cocoons of two hydropsychid caddises, Cheumatopsyche sp. and Asmi- cridea sp., together with the variously shrunken hydro- psychid pupae. Finally, the significance of many of the aberrans-group's peculiar larval and pupal features (Wells, 1985) became apparent. The background to the discovery, and evidence, albeit only circumstantial at present, for a parasitic life style in this caddisfly group, are outlined. The observations on 0.muscari were made on specimens collec- ted in Kakadu National Park, northern Australia, where geographic and climatic conditions mitigate against a con- trolled rearing programme.

Background

Atypical Orthotrichia larvae and pupae of SE Australian aberratis group (Wells, 1979, 1983, 1990, 1991) species were described in 1985 (Wells, 1985). Normally Orthotrichia immatures, while showing several unique features, con- form in general respects with other members of the family Hydroptilidae. This family, alone in the order, has what is known as a 'hypermetamorphosis'. Its larvae pass through

Correspondence: Dr Alice Wclls, Northern Territory Museum of Arts and Sciences, GPO Box 4646, Darwin, NT, Australia 0801.

four uncased instars as tiny spidery creatures before chang- ing form and (in all but one Neotropical genus (Flint, 1970)) constructing a case which is carried and enlarged during the final and major feeding instar until being modi- fied slightly for pupation.

In work on Australian micro-caddis larvae (Wells, 1985), a minute, flat larva (length about 1 mm) carrying a dorso- ventrally flattened case comprised of two unequal valves was identified as the early final instar form of a larva of grossly disproportionate dimensions occupying a more typical 'wheat seed' shaped case built of two equal valves joined by dorsal and ventral seams (Wells, 1985). Head, thorax and legs of both are indistinguishable in size and morphology, but the abdomen of the large larva is abnor- mally swollen. Pupal cases lack the typical dorsal ridges and bear no sign of attachment discs such as usually anchor these cases firmly to the substratum; in 0.corlferta Wells, one of the two valves of the dorso-ventrally flattened case is incorporated into each wall. A curious anterior beak- like projection occurs on the pupal head.

The parasite

In association with the parasitoid life style, the microcaddis life history appears to be modified in this aberrans group.

The form with the tiny flat case is an extra 'step' inserted at the start of the final larval instar. This is unknown in other Orthotrichia, and, as is apparent from the comparable size of head and thorax of the two forms, is not another instar (Wells, 1985). Circumstantial evidence suggests that the extra 'step' is the infective stage of parasitic aberruns- group Orthotrichia. In studies on south-eastern Australian streams (D. Cartwright and J. Dean, pers. comm.) these tiny larvae (probably 0.aberratzs Wells or 0.cotzferta) were netted, all with abdomens of similar size. Apparently,

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300 Alice Wells

Pc

Fig. 1. Pupal case of Cheumaropsyche sp. with side removed to show the pupal cocoon enclosing the Cheumatopsyche pupa and the parasitoid larva of Orrhotrichia muscari. Abbreviations: Hp, Cheumatopsyche pupa; 01, Orthotrichia muscari larva; Pc. Cheumatopsyche pupal case; Pcc; Cheumatopsyche pupal cocoon. Scale bar = 1 m.

then, they are free-living initially, although not feeding. Similar minute larvae of 0.rnuscari have been found inside the newly-made cased cocoon of prepupal hydropsychids. In 0.muscari the tiny early cases are rarely incorporated into the walls of the mature Orthotrichia cases as described above, but are usually found discarded alongside the dif- ferently cased parasitoid larvae or pupae within intact hydropsychid pupal cocoons. Since, when gathered care- fully, the hydropsychid cases bear no sign of any breach of the cocoon or surrounding tight sand shelter, the early final instar Orthotrichia larva must be sealed in by the prepupal host.

Whatever the exact sequence at that juncture, the host pupates successfully: the second ‘stage’ final instar 0.muscat-i larvae have been found only with host pupae (Fig. 1) or their variously shrunken remains (Fig. 2).

The larva appears to feed on the pupal contents while, at least for some time, pupal development praceeds. When the larger Asmicridea is parasitized, the pupa advances further and more of it remains when the parasitoid pupates than Cheumatopsyche of which only the crumpled pupal exoskeleton is left.

Discussion

With hindsight, parasitism by larvae of this group seems selfevident: the disproportionately distended abdomen would inhibit free-ranging for feeding and would render the larva vulnerable to disturbance by currents or other animals. The characteristic labral tooth, normally serving the predatory habits (Wells, 1985) of Orthofrichia larvae,

Pc

The first purusitic Trichoptera 301

Fig. 2. A later stage in the development of the parasitoid larva of Orthofrichia muscari, showing the large larva with its tiny head and thorax and its discarded earlier larval case. Abbreviations: EOc, early final instar larval case of Orthotrichia muscari: Hp, Cheumutopsyche pupa; 01, Orthorrichia muscari larva; Pc, Cheumatopsyche pupal case; PCC, Cheurnatopsyche pupal cocoon. Scale bar = 1 nun.

would preadapt them for parasitism. At maturity, the larva seems to strengthen its thin case with a tightly spun lining, but, encased in the host’s pupal cocoon, makes no attachment discs. Case construction must be a gymnastic feat, and retention of the habit at all is curious when the pupa is already well protected. Perhaps, as is suspected for similarly taut cocoons of hydrobiosid and rhyacophilid caddisflies (Wiggins & Wichard, 1989). the case has some physiological function. Speculating further, the atypical anterior projection on the head of the uberruns-group pupae could be likened to the avian egg-tooth and, at emergence, may serve to aid escape of the pharate adult from the host’s robust sand pupal shelter.

Verification of several details is required, but the essence of a parasitic life is there. Choice of host appears to be facultative, with 0.rnuscuri parasitizing caddis species (both undescribed) in two hydropsychid genera, and also phil- opotamids (Chirnurru species). About half the numerous Cheurnatopsyche pupae collected at the beginning of the 1991 dry season from one small Kakadu stream were para- sitized, but only few Asrnicrideu from a larger stream nearby. Other uberruns-group pupae have been found in tasimiid pupal cases in northeastern Queensland (S. Bunn, pers. comm.).

Discovery of a parasitoid stage in these micro-caddisflies is significant as the first example of parasitism in the order Trichoptera, and represents the independent evolution of the habit in yet another insect group. It broadens the range of functional feeding groups (sensu Cummins, 1973) among Trichoptera. The Kakadu National Park locality of 0.rnuscuri is relatively inaccessible and difficulties with

transport and maintainance of lotic insects in a tropical climate present serious obstacles t o rearing this species in the laboratory. The problems raised here could be studied in temperate southeastern Australian members of the uber- runs-group.

Acknowledgments

1 am grateful R. 1. Sommerville, University of Adelaide, for comments on the manuscript, and to E . S. Nielsen and J . P. Green of CSlRO Division of Entomology, Canberra, for photographs. The work was funded by the Northern Territory Museum for the Arts and Sciences, and I thank staff for their help. A. Neboiss, J. Dean, D. Cartwright and S. Bunn assisted with material and encouragement.

References

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Wells, A. (1979) The Australian species of Orthotrichia Eaton (Trichoptera: Hydroptilidae). Australian Journul of Zoology,

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302 Alice Wells

Wells, A. (1985) Larvae and pupae of Australian Hydroptilidae (Trichoptera), with observations on general biology and re- lationships. Australian Journal of Zoology, Supplementary Series, 113, 1-69.

Wclls, A. (1990) The micro-caddisflies (Trichoptera: Hydroptilidae) of North Sulawesi. Invertebrate Taxonomy, 3, 363-406.

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linae). Invertebrate Taxonomy, 5,487-526. Wiggins, G.B. & Wichard, W. (1989) Phylogeny of pupation in

Trichoptera, with proposals on the origin and higher classification of the order. Journal of the North American Renthological Society, 8 , 260-276.

Accepted 3 January 1992