Behavioural Response of Blackfly Larvae (Simuliidae, Diptera) to Different Current Velocities

Limnologica 31 (2001) 179-183 LIMNOLOGICA http://www.urbanfischer.de/j ournals/limno © by Urban & Fischer Verlag

Institute for Nature Conservation and Environmental Education, University of Vechta, Vechta, Germany

ELLEN KIEL

With 3 Figures

Key words: Blackfly species, current velocity, looping activity

Abstract

Video equipment was used to record and to compare the behaviour of bend down to the substratum, apply new silk, release the grip different blackfly species at two flow velocities 0.25 m s-~ and of their abdominal hooks from the old silk pad and attach 1.35 m s 1. Simulium noelleri FRIEDERICHS,Simulium ornatum (com- themselves to the new one. Compared with their feeding po- plex) MEIGEN and Simulium variegatum MEIGEN were studied. Ef- sition, this so called 'looping behaviour' seems to be less fects of flow velocity on larval locomotive activities were analysed. streamlined and secure: video-studies have revealed that Looping activity and the time needed to attach for filter feeding again most larvae detach while looping (REIDELBACtt & KIEL were affectet to some extend, depending on species and flow velocity. While in S. ornatum no differences were recorded in locomotive 1990). activity, larvae of S. noelleri and S. variegatum were less active at This laboratory study was conducted in order to determine high flow velocities. Larvae of S. noelleri also moved over shorter whether current velocity affects larval locomotive behaviour. distances when exposed to high flow velocities. Consequences of the It was carried out in an artificial flume, and compared the be- differences in behavioural response to flow velocities are discussed havioural responses of larvae of three blackfly species. The with respect to drift and silk pad adhesion. species chosen for this comparison were Simulium noelleri FRIEDERICHS, Simulium ornatum (complex) MEIGEN and Simulium variegatum MEIGEN. Simulium noeIleri is a lake- Introduction outlet dwelling species. Larvae occur at enormous densities at the immediate outflow (WOTTON 1987), where flow veloc- According to VOGEL, life as a filter feeder in flowing water ity may vary considerably, sometimes exceeding 1.00 m s can be regarded as a compromise among conflicting factors: (KIEL et al. 2000). S. ornatum is a widespread species, tolerat- low flow right near the surface to facilitate attachment but ing a wide range of conditions (CROSSKEY 1990). Although high flow slightly farther away to provide ample supply of sometimes found in rapidly-flowing streams (SEITZ 1992; food (VOGEL 1994). Living as passive filter feeders atop WEANER 1993), this species usually occurs in streams where rocks or plant surfaces in rapid streams and rivers, blackfly water flows below 0.5 m -1 (REDELBACH 1994; ZHANG 1998; larvae seem to have achieved this compromise very well. pers. observations), and MALMQVIST 8z SACKMANN (1996) They attach by silk pads (BARR 1982; REIDELBACH & KmL recorded maximum feeding rates for S. ornatum at 0.19 m s -1 1990) and reduce drag coefficients by orienting their body and 0.36 m s-1. parallel to the current (CHANCE & CRAIG 1986). Although the S. variegatum, in contrast, appears to be adapted to com- cup shaped labral fans seem to cause comparatively high drag paratively high flow velocity regimes. Usually it is found in forces (EYMANN 1988), the streamlined position of the larva upland rivers and streams (SE~TZ 1992), where it is spaced appears to be an appropriate compromise with respect to fil- over the surfaces of stones. Concluding from laboratory stud- ter feeding. ies, PttILLIPSON(1957) mentioned that this species may toler- For a variety of reasons blackfly larvae are not able to ate velocities up to 2.5 m s 1. maintain this position permanently. They have to change In this study flow velocities of 0.25 m s-~ and 1.35 m s -~ their position frequently, which means that larvae have to were chosen for comparison in order to describe and also

0075-9511/01/31/03-179 $ 15.00/0 179 compare the locomotive behaviour of larvae under quite dif- abdominal hooks and started filtering once again. Analysis was fo- ferent flow velocities. We hypothesised that the locomotive cused on those looping activities initiated by the larvae themselves; activity at least of those of blackfly species living in fast further activities - e.g. loopings caused by competitive interactions - flowing streams should be comparatively low, thus to prevent were excluded. the risk of detachment. From their natural flow preferences it was assumed that S. variegatum will be more active at 0.25 m ~ than at 1.35 m -1 Results while larvae of S. ornatum should show higher locomotive Locomotive activity: activity at 1.35 m -~ than at 0.25 m -~. S. noelleri is known to number of loops per larva have a great tolerance to low current velocities (WOTTON 1985:0.04 m -~) but also occurred at sluices and dams with up In S. noelleri, the number of loops differed significantly be- to 0.95 m -1 (EBHARDT 1994) or even 1.20 m s -1 (KIEL, pers. tween high and low velocities (Fig. 1). Whereas larvae shift- observ.). Therefore, S. noelleri was expected to be indiffer- ed to new feeding sites on average 8.6 times at 0.25 m s ent, i.e. larvae were thought to show similar activity pattern at (n = 209) activity was significantly reduced to about 50% of both flow velocities. this level at high velocities, i.e. larvae shifted to new attachment sites 4.5 times only at 1.35 m s ~ (n = 122; p < 0.01, Mann & Whitney U-test). Materials and Methods In S. ornatum, the average number of loops did not differ significantly at high and at low velocities. On average, larvae The experiments were carried out in a re-circulating flume at the shifted to another silk pad 3.9 times at 0.25 m s -j (n = 103) Swiss Federal Institute for Environmental Science and Technology and 4.2 times at 1.35 m s -~ (n = 123). (EAWAG). The behaviour of the blackfly larvae was recorded at high The locomotive activity of larvae of S. variegatum was (1.35 m s-~) and at low (0.25 m s-~) water flow. Flow was measured 1 cm above the substratum which is little above larval head fans. The similar to that of S. oJ~atum when flow velocity was low flume was a transparent PVC channel, 3 m long, and 10 x 10 cm in (4.3 loops/larva at 0.25 m s -~, n = 73), but activity was signif- cross-section, giving homogenous flow conditions over a compara- icantly lower at high velocities: 1.6 loops/larva at 1.35 m s -1 tively long distance. Mirrors mounted below the transparent bottom (n = 37; p < 0.05, Mann & Withney U-test). at a 45 ° angle allowed the study of larval behaviour from below, i.e. Comparing species at similar flow velocity, it is evident from the point of attachment. Recording larval activity from this per- that larvae of S. noelleri are most active at 0.25 m s -~. They spective is necessary if locomotive activity is to be analysed (for a moved more than twice as much (8.6 loops/larva) as larvae of detailed description of the flume, see KIEL • FRUTIGER1997). S. ornatum (3.9 loops/larva) and S. variegatum (3.7 loops/ The day before a new experiment was started, larvae were collect- larva) [(p< 0.05, Kruskal-Wallis H-test; for details concern- ed from the field. They were rinsed into the flume and allowed to at- ing this test, see LOZAN (1992)]. tach to the ground at 0.50 m s-~. After 12 hours, about 50-100 larvae were randomly chosen for the study. Only undamaged, medium-aged At 1.35 m s <, S. noelleri and S. ornatum showed similar larvae were analysed. Larvae ready to pupate, small larvae (first in- activity (4.5 and 4.2 loops/larva) respectively, whereas stars), and larvae that had not settled in the typical way were re- S. variegatum was significantly less active than the others, moved before the experiments were started. with only 1.6 loops/larva (p < 0.05, Kruskal-Wallis H-test). Prior to the start of our video-recordings, flow velocity was slow- ly raised or lowered to the experimental flow velocity. Video-recording was started about 10 minutes after the study velocity was reached Locomotive activity: and lasted for 10 hours. number of loops per looping sequence During the 10-hour experiments, temperature was maintained at The number of loops per looping sequence was affected by 14 °C. Oxygen was always around 100% saturation. Food supply was achieved by mixing about 2/3 tap water and about 1/3 of stream flow velocity in S. noelleri only (Fig. 2). Whereas larvae of water. Previous experiments had shown this food supply to be suffi- S. noelleri carried out about 6.6 loops per looping sequence at cient to rear larvae until pupation. The experiments were run with 0.25 m s -1 (n --- 151) looping sequences were significantly constant cold light illumination. Evaluation of the experiments was shorter (3.0 loops per looping sequence; n -- 75) at 1.35 m s -1 performed by playing back the videotapes in slow motion and (p < 0.05, Mann-Withney U-test). In contrast, the length of analysing larval behaviour individually. By marking larval silk pads looping sequences did not differ significantly in on the TV monitor, any further activity could be recorded. S. variegatum and S. ornatum between the two flow veloci- To characterise locomotive activity patterns, the 'number of loops ties. Larvae of S. ornatum carried out 5.0 or 5.1 loops/looping per larva ', the 'number of loops per looping sequence', and 'time sequence respectively until they fixed themselves again for needed to attach for feeding again' were recorded. 'Looping se- filter feeding (25 m s-l: n = 171; 135 m s-l: n = 87), and quence' was defined as the number of new silk pads that were applied to the substratum between leaving an old feeding site and pro- S. variegatum carried out 4.3 loops/looping sequence at ceeding to feed at the new attachment site. The 'time needed to attach 0.25 m s ~ (n = 40) and 3 loops/looping sequence at for feeding again' was determined by the start of application of new 1.35 m s -1 (n = 5). In S. variegatum, the length of looping se- silk until the moment a larva had shifted to this new silk pad, fixed its quences varied markedly between individuals at high speed.

180 Limnologica 31 (2001) 3 When exposed to low velocity, larvae of 10 S. noelleri were able to carry out the longest looping activity looping sequences, whereas there were no dif- 9-- 4 -- ferences between the looping sequences of the 8 0.25 m ,¢~ other species (Kruskal-Wallis H-test). 1,35 rn s~ 7 At high velocity, there were no significant differences among species with respect to the 6 p

again, but the opposite effect was evident in S. I X 0.25 m s~ ornatum. In S. noelleri and S. variegatum, lar- o 6' 1.35 rn s~ vae were ready to feed again 74 - 81 s after starting their locomotive activity (S. noelleri: n = 154; S. variegatum: n = 33), while S. orna- q- turn finished silk pad application significantly •~ p

Discussion Fig. 2. Looping activity of medium aged larvae of S. noelleri, S. ornatum and S. variegatum at different current velocities. Number of loops per looping sequence during Since drag forces are proportional to approxi- 1Oh records (average and standard error). mately the cube of velocity (VOGEL 1994) and are also higher if the larval body is bent down time to attach for filter feeding to the substratum (EYMANN 1988), the risk to 105- blackfly larvae of detaching should increase 0.25 m sl 90" p

Limnologica 31 (2001) 3 181 activity and the time spent preparing new silk pads were af- son of silk pads used by feeding and by looping larvae also fected significantly by flow velocity. The total number of shows that the time needed to produce silk pads is correlated loops per larva was significantly lower and the time spent with the amount of silk applied to the substratum: whereas preparing new silk pads was significantly longer at high than looping silk pads, which are prepared within seconds, are at low velocities. Since larvae stretch out to their maximum very indistinct and thin, larvae usually need more than a length when looping (REIDELBACH& KIEL 1990), the number minute to finish a silk pad used for filtering, which is much of loops also gives an indirect measurement of the distances thicker (BARR 1982; KmL et al. 1989). the larvae have moved. Therefore, it is concluded that in S. Clearly, this hypothesis needs further research but, but it is noelleri and S. variegatum larvae also move over shorter dis- assumed that the time needed to apply silk is correlated with tances at high than at low flow velocities. In S. ornatum, on the amount of silk, and thus to better adhesion. Indeed, our the other hand, the total number of loops per larva as well as results indicate that S. noelleri and S. variegatum are able to the number of loops per looping sequences remained con- respond to higher drag forces not only by different feeding stant at both velocities. This means that larvae continue mov- positions (CHANCE & CRAIG 1986; CRAIG & GALLOWAY ing over the same distances and with the same intensity al- 1987) or different looping direction (WOTTON 1985), but also though the risk of detachment will be increased. by improved silk pads. In contrast, S. ornatum seems not to The differences in response to current velocity found in be able to react adequately at this flow velocity. Silk pads are S. ornatum and S. noelleri, does not agree with other studies. applied comparatively quickly and thus should result in poor- MALMQVIST et al. (1999) recorded that blackfly larvae with er adhesion. In contrast to S. variegatum and S. noeIleri, similar labral fan metrics prefer similar velocity regimes. which are able to reduce activity and increase adhesion, the Since S. noelIeri and S. ornatum have similar fan areas, they constant activity pattern and reduced adhesion in S. ornatum should have similar current preference in the range of moder- should cause a higher risk of dislodgement. ately to fast flowing streams. Further investigations are need- Despite the otherwise broad ecological tolerance of S. or- ed to test whether or not these differences refer to the experi- nature (CRoSSKEY 1990), inadequate adhesion and locomo- mental design. Especially in S. noelleri, the dense crowding tive activity might be another reasons for its restriction to of larvae often found under natural conditions (WOTTON special types of streams and rivers (SEITZ 1992) with low to 1992) might cause 'skimming flow' (JUMARS & NOWELL medium current velocities. 1984; VOGEL 1994). At these dense aggregations, distances between larvae are much less than their height above the substratum, thus protecting the individual larva from the main Acknowledgements: I am grateful to the Deutsche Forschungs- flow, which moves over them as if they were a solid object. gemeinschaft, the Swiss Federal Institute for Environmental Science Though in our experiments larvae of S. noeIleri also crowed and Technology (EAWAG), and the Johanna & Fritz-Buch-Gedficht- nisstiftung who financially supported parts of this study. I am also together, forming lines across the current as it is reported in very grateful to Dr. ANDREAS FRUTIGER: He constructed the high literature (WOTTON 1992), mean densities were too low speed flume, which was the basic technical requirement for this (< 50 ind. cm -2) to cause 'skimming flow'. study, and gave many helpful comments on an earlier version of this It remains uncertain if the differences in time larvae need paper. to attach in new silk pads do also reflect differences in adhesion. Since the application of silk by S. noelleri and S. variegatum lasts much longer at high flow velocities, this could mean that larvae apply larger or thicker silk pads. However, this may also reflect the more difficult situation and increased References hydrological stress at higher flow velocity. Two results from BARR, W. B. (1982) Attachment and silk of Simulium vittatum other studies might be worth further attention: PMNE & LEVIN ZETTERSTEDT (Diptera: Simuliidae). M. Sc.-Thesis, Department of (1981) have shown that agitation of waves increases byssus Entomology, Edmonton, Alberta. thread formation by MytiIus caIifornianus, and studies by CHANCE, M. M. & CRAIG, D.A. (1986): Hydrodynamics and be- WITMAN & SUCHANEK (1984) have revealed that the strength haviour of Simuliidae larvae (Diptera). Canadian Journ. Zool. 64: of attachment is higher where Mytilus californianus and 1295-1309. M. edulis live exposed to higher mechanical stress. In black- CRAIG, D. A. & GALLOWAY,M.M. (1987): Hydrodynamics of larval flies, a similar correlation seems to exist. BARR (1982) com- black flies. In: K~M, K. C. & MERRITr, R. W. (eds.), Black Flies - pared larval silk pads sampled in a stream, with a flow of ecology, population management, and annotated world list, pp. 171-185. University Park and London, Pennsylvania State Uni- 0.20-0.45 m s 1, and silk pads applied to artificial substrates versity. in the laboratory at velocities < 0.07 m s -1. Histological stain- CROSSI~Y, R. W. (1990): The natural history of blackflies. John ing of the silk suggests that larvae respond to higher veloci- Wiley & Sons, London, pp. 611. ties by the application of more silk: silk pads prepared under EBHARDT, D. (1994): Analyse zur Drift von Simuliidae (Diptera) low flow conditions are much thinner than silk pads of the nnter besonderer Berticksichtignng yon S. noelleri FRIEDERICHS same species produced in the field. Additionally, a compari- 1920. M. Sc. Thesis, Univ. Hamburg.

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- & KIEL, E. (1990): Observations on the behavioural sequences of Author's address: Prof. Dr. ELLEN KIEL, Hochschule Vechta, Insti- looping and drifting by blackfly larvae (Diptera: Simuliidae). tut far Naturschutz und Umweltbildung, Driverstr. 22, D - 49377 Aquatic Insects 12: 49-60. Vechta, Germany; e-mail: [email protected]

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