The phoretic association of Nanocladius (Nanocladius) rectinewis (Kieffer) (Diptera: Chironomidae) on serricornis Say (: )

VYTENISGOTCEITAS' AND ROSEMARYJ. MACKAY Department of Zoology, University of Toronto, Toronto, Ont., Canada M5S 1Al Received June 26,1980

GOTCEITAS,V., and R. J. MACKAY.1980. The phoretic association of Nanocladius (Nanocla- dius) recrineruis (Kieffer) (Diptera: Chironomidae) on Nigronia serricornis Say (Megalop- tera: Corydalidae). Can. J. Zool. 58: 2260-2263. Nanocladius (Nanocladius) rectineruis larvae were discovered living phoretically on larval Nigronia serricornis in the Humber River, Ontario. No previous record of this association is known. Late-instar N.(N.) rectineruis appear to be host specific to N. serricornis. Nanocladius (N.) rectineruis larvae live in silken tubes attached to the mesothoracic venter of the host and feed on detrital material caught up in the body folds of the host. Overwintering occurs as late-instar larvae; pupation and emergence of the chironomid appears to precede the terrestrial pupation of the host. Phoresy seems to provide mobility, habitat stability, and protection for the chironomid. GOTCEITAS,V., et R. J. MACKAY.1980. The phoretic association of Nanocladius (Nanocla- dius) rectineruis (Kieffer) (Diptera: Chironomidae) on Nigronia serricornis Say (Megalop- tera: Corydalidae). Can. J. Zool. 58: 2260-2263. Des larves de Nanocladius (Nanocladius) recrineruis ont ete trouvees en association phoretique avec des larves de Nigronia serricornis de la riviere Humber, en Ontario. I1 n'y a pas d'antecedent a cette decouverte. Les N.(N.) rectineruis de stades avances semblent specifiques a N.serricornis. Les larves de Nanocladius (N.) rectineruis vivent dans des tubes de soie attaches au mesothorax ventral de I'hCite et se nourrissent des detritus qui restent accroches aux replis de I'hbte. Les larves de dernier stade passent I'hiver dans I'eau; la pupation et l'emergence du chironomide semblent prectder la pupation terrestre de I'h6te. L'association est benefique au chironomide puisqu'elle lui procure la mobilite, la stabilite d'habitat et la protection. [Traduit par le journal] Introduction The association between N. (N.) rectinervis and N. Chironomidae larvae have been found in various serricornis appears to be a new record. symbiotic associations with other aquatic inverte- brates (Steffan 1965a, 1967~).Whereas members of Methods the genus Symbiocladius are ectoparasitic on a Nigronia serricornis larvae were collected semi-monthly For personal use only. during October and November 1978, and sporadically between number of Ephemeroptera larvae (Wiens et al. December 1978 and July 1979, from a rifle area on the Humber 1975; Hynes 1976), phoretic associations appear River, Peel County, Ontario (43"56' N, 7Y50'W; site H2 of more common and have been described for a Mackay (1979)). At this site, bottom substrate is primarily boul- number of other Chironomidae species (Henson ders, cobbles, and gravel (as classified by Cummins 1%2), with accumulations of sand and (or) silt in slower reaches. Water 1957; Steffan 1965b, 19676; Hilsenhoff 1968; Hynes temperature during the fall sampling period (Oc- 1970; Benedict and Fisher 1972; Svensson 1976). tober-December 1978) ranged from 0-10°C; maximum summer While collecting larval Nigronia serricornis in temperature was 24°C. The mean depth of water was 24 cm. the Humber River, Ontario, we discovered Rocks were lifted from the stream bottom while a D-frame net Nanocladius (Nanocladius) rectineruis (Kieffer) (mesh: 0.5 mm) held downstream collected any dislodged in- vertebrates; still clinging to the rocks were picked off, larvae living phoretically on these corydalids. Lar- and all specimens were preserved in Kahle's solution. val Nanocladius (Plecopteracoluthus) downesi In the laboratory, N. serricornis larvae and other macroin- (Steffan) (Saether 1977) have been found on the vertebrates were examined for the presence of N. (N.) rectiner- larval corydalids Chauliodes pectinicornis L. and uis. The number per host and the location of each N. (N.) re- L. (Benedict and Fisher 1972), crineruis and found was recorded; larvae were then

Can. J. Zool. Downloaded from www.nrcresearchpress.com by Texas A&M University on 07/18/17 removed from the host and their head capsule width measured and N. serricornis (Hisenhoff 1968), as well as on a dorsally across the eyes, using an ocular micrometer. number of Perlidae (Plecoptera) nymphs (Steffan In January 1979 several N. serricornis larvae carrying larval 1965b; Hilsenhoff 1968; Benedict and Fisher 1972). N. (N.) rectineruis were collected and brought back to the lab- oratory alive. Hosts and symbionts were placed in containers of 'Present address: Department of Zoology, University of Al- aerated, circulating water (water temperature: 18-20°C) and berta, Edmonton, Alta., Canada T6G 2E9. reared to confirm the symbiont's identification. Larvae, pupae, 0008-43011801 122260-04$0 1 .W/O @ 1980 National Research Council of Canada/Conseil national de recherches du Canada GOTCEITAS AND MACKAY

I (106%) I (1.6%) 51 (83-8%)

3 (4.9%) (dorsal)

5 (8.1%) For personal use only.

FIG. 1. Ventral view of Nigronia serricornis larva showing total number of Nanocladius (N.)rectinervis collected from various sites on 63 Nigronia larvae. Inset is an enlarged view of the seventh abdominal sternite. Can. J. Zool. Downloaded from www.nrcresearchpress.com by Texas A&M University on 07/18/17 and adults of Nanocladius were identified using Saether's (1977) rectineruis larvae (mean: 1.04 per host). Additional keys. collecting between December 1978 and July 1979 Results produced 19 N. serricornis larvae, 11 (59%) carry- Fall collections yielded 142 N. serricornis larvae, ing N. (N.)rectinervis larvae (mean: 1.06 per host). 52 (37%) of which were found carrying N. (N.) Nanocladius (N.)rectinervis larvae were not found CAN. J. ZOOL. VOL. 58. 1980 For personal use only.

FIG.2. Dorsal view of Nigronia serricornis larva with pupal Nanocladius (N.)rectinervis attached. in association with any other macroinvertebrates out of either end of its tube and bend to apply its present in the Humber River, nor were any other mouthparts and anterior prolegs to the detrital symbiotic chironomids collected. material. Larvae were able to turn around while Although N. (N.) rectinervis larvae were found remaining within their tube. on various parts of the host's body (Fig. l), the Nanocladius (N.) rectinervis pupae were found venter of the mesothorax, between the second and in cases that were quite distinct from the larval third pair of legs, was most favoured (83.8%). tubes although apparently made of similar mate- Chironomid larvae observed in the laboratory did rials. All of the 12 specimens of Nigronia found not change their site of attachment on their hosts. carrying N. (N.) rectinervis pupae had the pupal Can. J. Zool. Downloaded from www.nrcresearchpress.com by Texas A&M University on 07/18/17 All larvae were in tubes open at both ends and fixed case attached laterally on the left side of the to the host's body. Although presumably made of mesothorax, anterior to the second leg. The pupa silk, the tubes were gelatinous in appearance. was oriented with its head directed away from the In the laboratory N. (N.) rectinervis larvae were host's body (Fig. 2). At the time of emergence, the observed feeding on pockets of detrital material pharate adult breaks out of the posterior end of the accumulated in numerous body folds of the host. pupal case and rises to the water's surface where The larva would extend its body up to half its length eclosion occurs. GOTCEITAS AND MACKAY 2263

Adults of larvae collected in January 1979 (water carnivorous hosts may be a disadvantage during the temperature at collection site: 0°C) emerged in the process of attachment because of possible preda- laboratory in March 1979. The first evidence of tion by the host; however he offered no explanation pupation in the field was 16 April 1979, when three for the association of N. (P.) downesi exclusively N. serricornis larvae harbouring pupae were col- on predators. We propose that once N. (P.) dow- lected. These observations suggest that pupation is nesi or N. (N.) reitineruis larvae are successfuIly triggered in part by rising water temperatures. established, the host's position as a higher predator The mean head capsule width of all the N. (N.) in the trophic structure of the community confers a rectinervis larvae collected was 0.22 mm (range: degree ofprotection for the chironomids from pre- 0.19-0.24 mm). As this size class of larvae under- dation by other organisms. went pupation in the laboratory, it must include Acknowledgements final and perhaps also penultimate instars. No early instars were collected. As N. (N.) rectinervis lar- We thank Jan J. H. Ciborowski for helpful sug- vae were found on various instars of N. serricornis, gestions and criticisms during preparation of the no definitive correlation between instars of the host manuscript; Dr. W. L. Hilsenhoff for specimens of and symbiont were apparent in this study. phoretic Nanocladius and collection records from Wisconsin, and Dr. D. R. Oliver for assistance in Discussion chironomid identification. The research was sup- Late instar N. (N.) rectinervis appear host ported by the Natural Sciences and Engineering specific to N. serricornis larvae, as other potential Research Council of Canada. host organisms recognized from other studies BENEDICT,P. R., and G. T. FISHER.1972. Commensalistic relationships between Plecopteracoluthus downesi (Diptera: (Steffan 1967b; Hilsenhoff 1968; Benedict and Chironomidae) and Chauliodes pectinicornis (Megaloptera: Fisher 1972) were not used in spite of their presence Corydalidae). Ann. Entomol. Soc. Am. 65: 109-1 11. in the Humber River. CUMMINS,K. W. 1962. An evaluation of some techniques for Steffan (1%7b) observed Nnnvclndi~ts1P.)dow- the collection and analysis of benthic samples with special ncsi larvae coping with moulting in their host by emphasis on lotic waters. Am. Midl. Nat. 67: 477-504. HENSON,H. 1957. The larva, pupa and imago of Hydrobaenus leaving as moulting commenced and reattaching to ephemerae Kief. (Chironomidae: Diptera). Hydrobiologia, 9: the next instar, but assumed that N. (P.1 Ifnwnesi 25-37. had to synchronize its aquatic period with that of its HILSENHOFF,W. L. 1968. Phoresy by Plecopreracolurhus dow- host. This assumption and our own observations nesi on larvae of Nigronia serricornis. Ann. Entomol. Soc. Am. 61: 1622-1623. lead us to conclude that N. (N.)rectineruis larvae HYNES,H. B. N. 1970. The ecology of running waters. Univer- attached to final instar N. serricornis appear com- sity of Toronto Press, Toronto. mitted to completing their life cycle in time for the 1976. Symbiocladius aurifodinae sp.nov. (Diptera: spring or early summer terrestrial pupation of their Chironomidae), a parasite of nymphs of Australian Lep- tophlebiidae (Ephemeroptera). Mem. Nat. Mus. Victoria,

For personal use only. host. Melbourne, 37: 47-52. The ectoparasitic association in larval Sym- MACKAY,R. J. 1979. Life history patterns of some species of biocladius spp. is obviously one of nutrient acqui- Hydropsyche (Trichoptera: Hydropsychidae) in southern sition (Wiens et al. 1975; Hynes 1976). The advan- Ontario. Can. J. Zool. 57: 963-975. tage of a phoretic association in various other SAETHER,0. A. 1977. Taxonomic studies on Chironomidae: Nanocladius, Pseudochironomus and the Harnischia com- Chironomidae larvae is less obvious. Possible ad- plex. Bull. Fish. Res. Board Can. 1%: 1-143. vantages for the symbiont include stability in rela- STEFFAN,A. W. 1965a. On the epizoic associations of tive]y fast currents (Steffan 1967b), a food supply Chironomidae (Diptera) and their phyletic relationships. Pro- (Steffan 1967b3, and a possible refuge from com- ceedings of the XI1 International Congress of Entomology, petitive interacrions (Svensson 1976). In using its London, 1964,l: 77-78. - 19656. Plecopteracoluthus downesi gen. et sp.nov. host as a substrate for habitation and food ac- (Diptera: Chironomidae) a species whose larvae live phoreti- cumulation, N. (N.) rectinervis could be viewed as cally on larvae ofPlecoptera.Can. Entomol. 97: 1323-1344. successfully avercoming any competition for space -1967~. Ectosymbiosis in aquatic . In Symbiosis. and lor) food which may exist. or may have existed. Vol. 2. Chap. 4. Editedby M. S. Henry. Academic Press, New in York. pp. 207-289. Can. J. Zool. Downloaded from www.nrcresearchpress.com by Texas A&M University on 07/18/17 its habitat. Simultaneously, N. (N.) recrineruis 1%7b. Larval phoresis of Chironomidae on Perlidae. gains added stability, mobility. and protection Nature (London), 213: 846-847. through the habits and biology of its host. For SVEMS~ON,B. t976. The association between Epoicacladius example. because N. serricorhis larvae exhibit ephemerae Kieffer {Diptera: Chironomidae) and Eph~tnern danicrr Miiller(Ephemeroptera). Arch. Hydrobiol. 77: 22-36. both morphological and behavioural adaptations to D. cope with relatively strong currents, they provide a WIENS. A. P., M. ROSENBERG. and K. W. EVANS.1975. Symbinclcrdirrs eqlritans (Diprera: Chironomidae). an ec- ' mobile yet secure habitat. Steffan (19676) recog- toparasite of Ephernemptera in the Martin River, Northwest nized that the association of N. (P.) downesi with Territories. Canada. Entomol. German. 2: 1 13-120.