Ecological Entomology (2004) 29, 327–335

Aerial dispersal and host selection by neonate ephemeraeformis (: Psychidae)

1 2 ROBERT G. MOORE andLAWRENCE M. HANKS 1United States Army Center for Health Promotion and Preventive Medicine, North, Attention: MCHB-AN Entomological Sciences Division, Maryland and 2Department of Entomology, University of Illinois at Urbana–Champaign, U.S.A.

Abstract. 1. Neonate evergreen bagworms, Thyridopteryx ephemeraeformis (Haworth) (Lepidoptera: Psychidae), disperse by dropping on a strand of , termed silking, and ballooning on the wind. Larvae construct silken bags with fragments of plant foliage. This species is highly polyphagous, feeding on more than 125 species of woody of 45 families. The larvae commonly infests (Juniperus spp.) and arborvitae ( spp.), but rarely feed on deciduous hosts such as . The hypothesis is proposed that polyphagy in T. ephemer- aeformis is maintained by variation among larvae in dispersal behaviour, and time constraints on the opportunity to disperse, but patterns of host species preference result from a predisposition for larvae to settle on arborvitae and juniper but disperse from other hosts. 2. Consistent with that hypothesis, laboratory experiments revealed: (a) starved larvae varied in their tendency to disperse from paper leaf models; (b) starved larvae readily silked only during their first day; (c) larvae became increasingly sedentary the longer they were exposed to plant foliage; (d) when provided with severalopportunities to silk,larvaebecame sedentary after exposure to arborvitae foliage, but repeatedly silked after exposure to (Acer species) foliage or paper; and (e) larvae were less inclined to silk from foliage of arborvitae than from maple. 3. Field experiments supported the hypothesis by demonstrating that: (a) neonates tended to disperse from maple leaves while larvae older than 1 day tended to settle and remain; and (b) neonates were less likely to disperse from arborvitae and juniper than from maples. Key words. Bagworm, ballooning, caterpillar, host plant location, plant– interaction

Introduction preordained by oviposition preference of the mother (see Rausher, 1983). For some dendrophagous species of several For phytophagous , location of a suitable host plant lepidopteran families, adult females are flightless and it is is obviously critical for survival and reproduction (Zalucki the young larvae that disperse and colonise new hosts et al., 2002). Larvalhosts of most lepidopterousspecies are (Barbosa et al., 1989). The larvae drop on a silken thread, termed silking, and balloon passively downwind where they may encounter new hosts (Mitchell, 1979; Ghent, 1999). Correspondence: L. M. Hanks, Department of Entomology, Aerial dispersal by caterpillars is usually restricted to University of Illinois at Urbana–Champaign, 320 Morrill Hall, 505 neonates (Stephens, 1962; Leonard, 1970; Mitchell, 1979; South Goodwin Ave., Urbana, IL 61801, U.S.A. E-mail: hanks@ Zalucki et al., 2002). Neonates of some species show an life.uiuc.edu innate predisposition to silk and balloon (Capinera &

# 2004 The RoyalEntomologicalSociety 327 328 Robert G. Moore and Lawrence M. Hanks

Barbosa, 1976), but dispersalbehaviour can be modified by et al., 1960). Silking behaviour is not influenced by the order a variety of intrinsic and extrinsic factors (Leonard, 1970; in which larvae emerge from the mother’s bag, and is only Lance & Barbosa, 1981; Carrie` re, 1992; Diss et al., 1996; weakly influenced by maternal effects such as the maternal Rhainds et al., 1997, 2002). Neonates may be more likely to host (Ward et al., 1990; Moore, 2001). silk and balloon if they encounter hosts of low quality Thyridopteryx ephemeraeformis is a highly polyphagous (Ramachandran, 1987; Rhainds et al., 2002), non-preferred species (see Howard & Chittenden, 1908; Haseman, 1912; or unsuitable host species (van der Linde, 1971; Capinera & Neck, 1977; Johnson & Lyon, 1988), feeding on more than Barbosa, 1976; Lance & Barbosa, 1981; Futuyma et al., 125 species of woody plants of 45 families (Davis, 1964). 1984; Ramachandran, 1987), or when food is not available Despite its polyphagous nature, high-density populations (Leonard, 1970; van der Linde, 1971; Capinera & Barbosa, usually arise on the evergreen shrubs juniper or red cedar 1976). Dispersalbehaviour alsomay show dielperiodicity (Juniperus spp.) and arborvitae (Thuja spp.) of the Cupres- (Mitchell, 1979; Zlotina et al., 1999; Rhainds et al., 2002) saceae, but rarely on maples (Acer spp., Aceraceae) and and may be influenced by weather, particularly wind other deciduous trees (Jones & Parks, 1928; Johnson & speed, air temperature, and precipitation (Mitchell, 1979; Lyon, 1988). In the area of the studies (Champaign Co., McManus & Mason, 1983; Cox & Potter, 1986). Illinois), infestations most commonly arise on Juniperus Passive aerialdispersalis risky for phytophagous insects virginiana L., J. communis L., and Thuja occidentalis L., because they can not control flight direction or the plant including low-growing cultivars (Ghent, 1999; L. M. species to which they are carried, and consequently is asso- Hanks, pers. obs.). These species do not seem the most ciated with high mortality rates (e.g. Hanks & Denno, 1998; likely to intercept ballooning larvae, being neither the Zalucki et al., 2002). In fact, most aerially dispersing cater- most abundant of potentialhosts in urban habitats (maples pillars travel only short distances and many perish on the are dominant) nor the largest (sycamores, Platanus spp., ground (Mitchell, 1979; Weseloh, 1985, 1997; Cox & Potter, can be much taller and broader; L. M. Hanks, pers. obs.). 1986; Ghent, 1999; Rhainds et al., 2002). Of course, the Moreover, this pattern of dispersion apparently is not attri- odds of encountering a suitable host are improved greatly butable to variation in larval performance because T. ephe- if larvae are polyphagous (see Young, 1997). In that case, meraeformis can complete development on non-preferred the greatest proportion of ballooning neonates presumably hosts, and even unnaturalhosts such as sedges ( Carex would be intercepted by the host species that presents the spp.; Howard & Chittenden, 1908; Haseman, 1912; Jones largest target: those that are most abundant, tallest, and & Parks, 1928; Neal& Santamour, 1990; Ward et al., 1990, having the broadest canopies (Ghent, 1999). Ballooning 1991). caterpillars may achieve some degree of host selection by The hypothesis is proposed that polyphagy in T. ephemer- rejecting hosts and re-dispersing (Lance & Barbosa, 1981; aeformis is maintained by inherent variation among larvae Lance, 1983; Barbosa et al., 1989; Ward et al., 1990; in the tendency to disperse, and time constraints on disper- Rhainds et al., 2002; Zalucki et al., 2002), but this ability is sal, but that patterns in host species preference result from a temporally constrained, however, because small larvae suc- tendency in larvae to aerially disperse from non-preferred cumb quickly to starvation and desiccation (Capinera & hosts, but to settle on arborvitae and juniper. This hypoth- Barbosa, 1976; Stockoff, 1991; Reavey, 1993). esis was evaluated with experiments that tested the follow- In this article, new information on aerial dispersal by ing predictions: (a) neonates vary in their inherent tendency neonate caterpillars of the , Thyridop- to disperse; (b) the tendency to disperse declines with larval teryx ephemeraeformis (Haworth) (Lepidoptera: Psychidae) age; (c) the tendency to disperse declines with exposure to is presented, and the relationship between dispersal behav- host foliage (and the opportunity to construct a bag); and iour and host species preference is evaluated. This species (d) larvae will tend to disperse from non-preferred hosts but is native to North America and is univoltine. Larvae con- remain on preferred hosts. The research contributes much- struct a silken bag that they ornament with fragments of needed information on the behaviour and ecology of first- bark and foliage, but during this process do not consume instar caterpillars, rarely studied because of their small size plant materials (for general information on biology and (see Zalucki et al., 2002), and on the association between behaviour, see Haseman, 1912; Jones, 1927; Jones & aerialdispersaland host plantpreference (see Ward et al., Parks, 1928; Kaufmann, 1968; Leonhardt et al., 1983; Cox 1990). & Potter, 1986; Neal, 1986). Larvae never leave their bag, with only their head and thorax protruding, and enlarge it as they grow. Vermiform adult females fill their bags with as Materials and methods many as 1000 eggs. Eggs overwinter in the maternalbag and neonates (2 mm long) usually hatch in early June in the Sources of larvae area of the study (Champaign County, Illinois; Morden & Waldbauer, 1971). Thyridopteryx ephemeraeformis bags that contained eggs Neonate T. ephemeraeformis usually balloon in the morn- were collected from and arborvitae in late fall and ing (Cox & Potter, 1986) and may silk immediately upon early winter from areas in Champaign County, Illinois, emerging from the mother’s bag (Cox & Potter, 1986; including The Hoot Owl Christmas Farm, the campus Ghent, 1999), as is true for other psychid species (Gromysz of the University of Illinois at Urbana–Champaign, Mt

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 Aerial dispersal by neonate bagworms 329

Olive cemetery in Mayview, and the 4Es Tree Farm in seconds, and the few that fell without silking were elimin- Macon County, Illinois. Bags were stored in a 4 C refriger- ated from data sets (accounting for minor discrepancies in ator to suspend egg development, and emergence was sample sizes for some experiments). Bioassays were con- encouraged by bringing eggs to room temperature. ducted between 09.00 and 16.00 hours during Aprilto July Neonates usually emerged within 4 weeks. It was not pos- of 1999–2001. sible to discriminate between sexes of neonate T. ephemerae- formis and therefore sexualdifferences in dispersal behaviour could not be directly assessed. Evaluating phenotypic variation in dispersal behaviour

Prediction A, that neonate T. ephemeraeformis vary in Tree species their tendency to silk, was tested with laboratory experi- ment 1 over a 5-day period. Five bags from an infested In the experiments, T. ephemeraeformis larvae were pre- stand of juniper were collected and held individually in sented with juniper (J. virginiana or J. communis)andarbor- plastic Petri dishes to rear neonates. Neonates of unknown vitae (T. occidentalis) that are the common hosts (hence age were tested with the filter paper bioassay, recording referred to as preferred hosts), as well as maples which are how long they took to silk during a 0.5-h period (n ¼ 10 rarely infested (non-preferred hosts), including silver, sugar, siblings per trial, 12 trials). The study revealed that most and Norway maples (Acer saccharinum L., A. saccharum larvae that silked did so within 0.25 h (see Results), and Marshall, and A. platanoides L.; Aceraceae). Maples are this time limit was adopted in measuring dispersal rate in recorded hosts of T. ephemeraeformis (see Jones & Parks, subsequent bioassays. 1928; Davis, 1964; Johnson & Lyon, 1988), and larvae can complete development on them (Baerg, 1928; Barrows, 1974). In one study, tree of heaven [Ailanthus altissima (Miller), Evaluating the influence of larval age on dispersal behaviour Simaroubaceae] was included, which is not a host of T. ephe- meraeformis (see Davis, 1964; L. M. Hanks, pers. obs.). Two laboratory experiments and a field experiment were conducted to test prediction B, that the tendency to silk would decline with larval age. In laboratory experiment 2, Bioassay design dispersalrate was measured for the same individuallarvae every 24 h for 6 days (after which larvae began to die). Five Neonate T. ephemeraeformis continually produced a newly emerged neonates were collected from each of 10 strand of silk while walking that anchored them to the bags and cohorts were caged individually in cardboard substrate (gypsy larvae show the same behaviour; cups without food. Dispersalrate in 0.25-h filterpaper McManus & Mason, 1983). It was considered that silking, dropping bioassays was analysed by repeated-measures ANOVA with from the substrate on a silk line, constituted a dispersal time a fixed effect and maternalbag a random effect. behaviour and predisposed neonates to ballooning and aerial Because larvae readily silked only during the first day (see dispersal; larvae that were more inclined to silk would be Results), later experiments were conducted with neonates more likely to disperse from the host (see Reavey, 1993). that had emerged that morning. Because larvae could To study dispersalbehaviour, laboratorybioassays were construct bags from fibres and wax of cardboard cups, conducted in which larvae were transferred either to paper potentially influencing silking behaviour, neonates were or to foliage of host plants and the percentage that silked subsequently reared in plastic Petri dishes. during a specific time interval(dispersalrate) was recorded. In laboratory experiment 3, changes in silking behaviour Placing neonate caterpillars on paper leaf models provides over the course of the first day were evaluated, predicting a an assessment of the innate tendency and ability to disperse uniformly strong inclination to disperse. At 08.30 hours, while controlling for the influence of the substrate (see two bags were isolated in Petri dishes and five neonates Capinera & Barbosa, 1976; Ramachandran, 1987). The from each bag that had emerged during a 0.17-h period apparatus for the filter paper bioassays consisted of 10 were collected. The dispersal rate for each neonate was pieces of filter paper (halved disks, 11 cm in diameter; immediately measured with the filter paper bioassay, no. 1 qualitative, Whatman International Ltd, Kent, U.K.) neonates were transferred to individualPetri dishes, and attached 3 cm apart to a glass rod with binder clips, pos- re-tested at 2-h intervals for 6 h. Dispersal rate was analysed itioned at an angle of 20 above horizontaland 10 cm by repeated-measures ANOVA with time a fixed effect and above the bench top. Bioassays were conducted on a maternalbag a random effect. bench adjacent to north facing windows, under ambient Field experiment 1 was based on the observation in room conditions. Air vents were blocked to eliminate laboratory experiment 2 that silking behaviour declined breezes that might influence dispersal (wind speed was after 24 h, and tested prediction B on host trees, predicting undetectable with a hot wire anemometer). With a fine that newly emerged larvae would disperse from non- paintbrush, one neonate was transferred to the centre of preferred hosts more readily than older larvae. Larvae each paper. This handling did not appear to harm the larvae were reared from five bags in Petri dishes without food. in any way. Larvae could walk to the edge and silk within Neonates (<2 h old) or 1-day-old larvae were transferred

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 330 Robert G. Moore and Lawrence M. Hanks to different leaves of four Norway maples trees in two trials, than from foliage of preferred hosts (arborvitae). Foliage on 1 July (n ¼ 5 larvae per age treatment and tree) and 6 July samples were taken from at least five trees per species in 2001 (n ¼ 10 larvae). On both days, weather conditions were urban landscapes and consisted of a single leaf (sugar suitable for aerial dispersal (see Cox & Potter, 1986; Ghent, maple), a compound leaf (tree of heaven), or a branchlet 1999): skies clear or partly cloudy, maximum temperatures with leaflets (arborvitae), that were 5 cm long but varied 25–30 C, average wind speed 2–2.7 m s1, peak gusts in leaf area across species. To maintain foliage turgor, sam- 4–9 m s1 (Illinois State Water Survey, Champaign, Illinois). ples were transported separately in wet plastic bags, then the The number of larvae that dispersed was determined at 2-h bases of cuttings were wrapped in damp paper towelling, and intervals for 8 h (dispersal also assessed after 24 h in first samples were used in experiments within 1 h. Ten foliage trialonly). Dispersalrate was tested by ANOVA with neonate samples of each species were clipped to aluminium rods, age and time as fixed effects and trialand tree as random randomising position. Neonates were placed individually on effects. Although larvae may have been removed by natural cuttings and dispersalrate was recorded during a 1-h period. enemies, it seemed unlikely that the probability of predation The experiment was replicated five times on five different would differ for neonates and 1-day-old larvae. days. Dispersalrate was tested by ANOVA with plant species and hour as fixed effects, and triala random effect. Field experiment 2 tested prediction D, that neonates Evaluating the influence of host species encountered by larvae would tend to disperse from foliage of non-preferred hosts on dispersal behaviour (one silver maple, and two sugar and Norway maples) than preferred hosts (five junipers and three arborvitae). Study To test prediction C, that dispersalbehaviour wouldbe trees were at Mt Hope cemetery, Champaign Co., Illinois, influenced by the host species encountered by young larvae and initially were free of bagworms. Five neonates (<2h (<4 h old), three laboratory experiments and a field experi- old) were placed on separate leaves of each tree at a height ment were conducted. Laboratory experiment 4 was of 1–2 m, and dispersalrate was recorded after 2, 4, 6, and intended to simulate variation in the amount of time larvae 24 h. It was also recorded whether larvae had bags. Disper- are exposed to a single host, and can construct a bag, due to salrate was tested by ANOVA with hour and tree species as weather conditions that inhibit ballooning (such as rainfall fixed effects. Data for the three maple species were com- and coolair temperatures). It was predicted that larvae bined because they did not differ significantly. The experi- would be most inclined to silk after being exposed to foliage ment was started at 09.00 hours on 27 June 2001, and of non-preferred hosts, but would become sedentary on weather conditions were suitable for ballooning (skies preferred hosts over time. Neonates that had emerged clear, maximum temperature 28.5 C, average wind speed within a 0.25-h period from five bags were individually 1ms1, peak gust 4.8 m s1). caged in Petri dishes with fresh foliage cuttings (branchlets with leaflets or single leaves) of either arborvitae, juniper, or sugar maple for periods of 1–7 h in 1-h increments (n ¼ 5 Data analysis larvae per time period/host treatment). The experiment was replicated twice on different days. Dispersal rate was ANOVA was used to test differences between treatment measured with the filter paper bioassay and tested by means (PROC MIXED; SAS Institute, 2001). Original ANOVA with hour a covariate, plant species a fixed effect, data were log transformed (linear measurements) or angular and triala random effect. It was alsorecorded whether transformed (percentages) as necessary to meet ANOVA larvae had constructed bags to evaluate their influence on assumptions. Differences between means were tested with silking behaviour. full ANOVA models, but insignificant interactions and ran- Laboratory experiment 5 was similar in design to experi- dom effects were eliminated in a stepwise fashion, starting ment 4 (above), but larvae were provided with multiple with highest order interactions, leaving only significant opportunities to silk over the course of a day, and thus terms (see Milliken & Johnson, 1984). Pre-planned compar- simulated conditions that favoured ballooning. It was pre- isons of means were conducted using t-tests ( SAS Institute, dicted that larvae exposed to foliage of a non-preferred host 2001). In a few instances the G goodness-of-fit test (Sokal& (maple) would disperse readily and repeatedly, but those Rohlf, 1995) was used to test differences between single exposed to foliage of a preferred host (arborvitae) would be percentages and values expected from null hypotheses. more sedentary. Neonates were caged individually in Petri Untransformed means 1 standard error are presented dishes with filter paper or fresh foliage of either arborvitae or throughout except where stated otherwise. sugar maple (n ¼ 5 larvae per each of four replicates per treatment), and dispersalrate was measured with the filter paper bioassay after 0, 1, 3, and 5 h. The experiment was Results replicated on two different days, and data were analysed as in laboratory experiment 4, but as a repeated-measures ANOVA. Evaluating phenotypic variation in dispersal behaviour Laboratory experiment 6 tested prediction D, that young larvae would be more likely to silk from foliage of non- As predicted, dispersalbehaviour of T. ephemeraeformis preferred hosts (sugar maple) and non-hosts (tree of heaven) larvae varied considerably in laboratory experiment 1. Even

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 Aerial dispersal by neonate bagworms 331 though the paper provided neither food nor substrate with 100 which to construct a bag, some apparently healthy and a active larvae wandered, encountering the margin of the 80 paper several times, but avoided silking. Of 109 larvae, 93 (85%) silked from paper within 0.5 h (Fig. 1), and times to 60 dispersalaveraged 8.5 5.9 min (mean SD). Because the primary sex ratio of T. ephemeraeformis approximates 1:1

% silking 40 (Barrows, 1974), it is unlikely that the 16 larvae that did not b silk were of a different sex than the 93 larvae that did b 20 b (G-test, P > 0.5). A significant difference between the sexes b in silking behaviour also may have resulted in a bimodal b frequency distribution which was not evident in Fig. 1. 0 123456 Age of larvae (days)

Fig. 2. Relationship between the percentage of Thyridopteryx Evaluating the influence of larval age on dispersal behaviour ephemeraeformis larvae that silked during filter paper bioassays and their age (laboratory experiment 2). n ¼ 50 larvae. Means SE Laboratory experiment 2 confirmed the prediction that with different letters are significantly different (t-tests; P < 0.05). dispersal behaviour would decline with larval age; most larvae silked from paper when tested on the first day, but constructed bags with maple foliage by the end of the day by the second day were much less inclined to do so (Fig. 2; (>90% in both age groups). All larvae in the first trial that overall ANOVA F15,58 ¼ 26.4, P < 0.0001; day effect was the remained on hosts for 8 h (age groups combined) still were only significant term). present after 24 h. In laboratory experiment 3, larvae showed a consistent and strong tendency to silk over the course of the day, as predicted. All larvae silked every time they were tested during the 6-h study (overall ANOVA for dispersalrate Evaluating the influence of host species encountered by larvae P ¼ 1). The strong tendency to disperse during the first on dispersal behaviour day was consistent with laboratory experiment 2 (above). Field experiment 1 confirmed the prediction that younger Laboratory experiment 4, in which larvae were exposed larvae would be more likely to disperse from non-preferred to tree foliage for varying periods of time, confirmed the hosts than older larvae. Among neonates (<2 h old at the prediction that dispersal rate would decline with exposure onset of the experiment), 83.8 8% dispersed before hour 2, time (Fig. 3; overall ANOVA F3,41 ¼ 23.5, P < 0.0001; hour and 87.8 5.6% by hour 8, while percentages of older lar- covariate F1,41 ¼ 68.8, P < 0.0001), but did not show the vae (>24 h) that had dispersed by hours 2 and 8 were expected host species effect (F2,31 ¼ 0.91, P ¼ 0.42). It was 48.1 6.9 and 61.9 10.6% respectively (overall ANOVA concluded from this study that larvae that do not have an F5,63 ¼ 7.33, P < 0.0001; age effect F1,63 ¼ 33.8, P < 0.0001; opportunity to disperse will become increasingly sedentary other effects not significant). Thus, most larvae that dis- over time regardless of their host species. persed did so during the first two hours, regardless of their age. Of the few larvae that did not disperse, most had Arborvitae Juniper Maple 100 25 80 20 60 15 40 % silking 10

% of larvae 20

5 0 1234567 0 Exposure time (h) 0246810121416 18 20 22 24 26 28 30 Time to silking (min) Fig. 3. Relationship between the percentage of Thyridopteryx ephemeraeformis larvae that silked during filter paper bioassays Fig. 1. Frequency distribution for time to silking for 93 neonate and the amount of time they had been exposed to plant foliage of Thyridopteryx ephemeraeformis larvae released on paper leaf three tree species in Petri dishes (laboratory experiment 4). n ¼ 10 models (laboratory experiment 1). Arrow indicates mean. larvae per time period/host treatment. Means SE are presented.

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 332 Robert G. Moore and Lawrence M. Hanks

In the same experiment, the percentage of larvae that had foliage (filter paper), readily and repeatedly silked in filter constructed bags with leaf fragments increased rapidly paper bioassays (Fig. 5), even after 5 h, but larvae exposed (Fig. 4a; overall ANOVA F3,41 ¼ 13.8, P < 0.0001; hour covari- to arborvitae foliage showed a sharp decline in dispersal ate F1,41 ¼ 50.0, P < 0.0001; host and trialeffects not rate (overall ANOVA F6,23 ¼ 10.2, P < 0.0001; hour covariate significant). Larvae that had bags showed a sharp decline F1,23 ¼ 10.6, P ¼ 0.0046; host effect F2,23 ¼ 17.5, P < 0.0001; in dispersal rate with exposure period (solid line in Fig. 4b; host hour effect F2,23 ¼ 6.7, P ¼ 0.007; trialeffect not ANOVA F3,35 ¼ 3.2, P ¼ 0.027; hour covariate F1,35 ¼ 9.94, significant). These findings suggest that, under conditions P ¼ 0.0036; other terms not significant), but larvae that that favour ballooning, larvae will repeatedly reject non- did not have bags showed a consistently stronger tendency preferred or unsuitable hosts and re-disperse, but would to silk (dotted line in Fig. 4b; overall ANOVA P > 0.05; sam- tend to remain on preferred hosts. ple size not sufficient for analysis after day 4). These find- In the same experiment, sedentary behaviour again was ings suggest that larvae vary in their tendency to make bags, associated with construction of a bag, consistent with and that bag construction is associated with increasing laboratory experiment 4. None of the larvae exposed to sedentariness over time. filter paper produced bags, and all showed uniformly high The results of laboratory experiment 5, in which larvae dispersal rates. High rates of silking in the maple foliage were repeatedly provided with an opportunity to silk, were treatment, compared to the arborvitae treatment, also were more consistent with the prediction that dispersalwouldbe associated with absence of bags; in the maple treatment, 0, strongly influenced by host species. Larvae exposed to foli- 32.5 7.5, and 45.0 5.0% of larvae had bags by hours 1, 3, age of the non-preferred host (maple), or in the absence of and 5 respectively, while 47.5 28 of larvae on arborvitae had begun constructing bags within 1 h and 100% had bags by the third hour. In fact, most of the larvae that silked did (a) not have bags, regardless of host species (78 and 80% of 100 larvae that silked in maple and arborvitae treatments respectively). 80 Laboratory experiment 6, in which larvae were placed on foliage, confirmed the prediction that larvae would tend to 60 silk from non-hosts and non-preferred hosts, but remain on preferred hosts. Nearly all larvae silked from the non-host 40 tree of heaven during the 1-h trial(Fig. 6), and dispersal rates were high for sugar maple, but significantly lower 20 (<40%) for arborvitae (means significantly different, over- % of larvae having bags % of larvae having all ANOVA F2,14 ¼ 9.4, P ¼ 0.0034; host species was the only 0 significant term). Of the four larvae remaining on tree of 1234567 heaven, only one constructed a bag, while 93% or more of Exposure time (h)

(b) With bags Without bags Arborvitae Juniper Paper 100 a a a 80 100 a a 80 60

60

% silking 40

% silking 40 20 b b b 20 b 0 b 1234567 0 Exposure time (h) 031 5 Exposure time (h) Fig. 4. Relationship between (a) the percentage of Thyridopteryx ephemeraeformis larvae that had constructed bags when exposed to Fig. 5. Relationship between the percentage of Thyridopteryx foliage of three tree species (see Fig. 3) and (b) the percentage of ephemeraeformis larvae that silked during filter paper bioassays larvae with bags and without bags that silked during filter paper and the amount of time they had been exposed to plant foliage or bioassays, and the amount of time that larvae were exposed to paper in Petri dishes (the same individuals were tested repeatedly; foliage of three tree species in Petri dishes (laboratory experi- laboratory experiment 5). n ¼ 40 larvae per time period/host ment 4). n ¼ 30 larvae per time period. Means SE with different treatment. Means SE with different letters are significantly letters are significantly different (t-tests; P < 0.05). different (t-tests; P < 0.05).

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 Aerial dispersal by neonate bagworms 333

Discussion 100 a Laboratory experiment 1 confirmed prediction A, that larvae 80 a vary in their tendency to silk, as is true for aerially dispersing caterpillars of other species (Capinera & Barbosa, 1976; 60 Lance & Barbosa, 1981; Ramachandran, 1987). Some bag- worm larvae avoided silking from filter paper, a completely b

% silking 40 unacceptable host, even though they were starved. In nature, such variation in dispersal behaviour would result in larvae 20 settling to feed on a diversity of host species. Prediction B, that the tendency to disperse would decline 0 with larval age, also was supported. Larvae readily silked Arborvitae Sugar maple Tree of heaven from paper during their first day, and would do so repeat- Plant species edly, but subsequently were much less willing to silk even though they had no food and eventually died (laboratory Fig. 6. Influence of plant species on percentage of neonate experiments 2 and 3). These findings suggest that sedentary Thyridopteryx ephemeraeformis that silked from foliage samples individuals in laboratory experiment 1 may have been older (laboratory experiment 6). n ¼ 50 larvae per host species. Means than those that actively dispersed. with different letters are significantly different (t-tests; P < 0.05). Field experiment 1 demonstrated that larvae would be much more likely to remain on a non-preferred host after larvae that remained on foliage of the other host species at their first day of life. A greater tendency to disperse in least had begun constructing bags by the end of the experi- neonates compared to 1-day-old larvae also has been ment. reported for the tortricid Choristoneura rosaceana (Harris) Field experiment 2 further confirmed the predictions that (Carrie` re, 1992). young larvae would be more inclined to disperse from non- Experiments to test prediction C, that the tendency to preferred maple hosts than preferred hosts. Within 4 h disperse would decline with exposure to foliage of hosts, almost all of the neonates dispersed from maple leaves, yielded some unexpected results. Young larvae confined to but very few dispersed from juniper and arborvitae (Fig. 7; foliage for varying periods of time in laboratory experi- overall ANOVA: F6,64 ¼ 16.5, P < 0.0001; species effect: ment 4 showed a declining tendency to silk regardless of F2,64 ¼ 41.4, P < 0.0001; time effect: F4,64 ¼ 3.96, host species, even when caged with paper. When larvae P ¼ 0.0066). More larvae dispersed from arborvitae and were provided several opportunities to silk in laboratory juniper in late afternoon, but after 24 h more than 30% of experiment 5, however, they soon became sedentary after larvae were still present on these hosts. Regardless of host exposure to foliage of arborvitae, and showed a strong and species, almost all of the neonates that did not disperse consistent tendency to silk after being exposed to maple (95.4%) were making bags by the second hour. foliage or paper. These findings suggest that larvae will repeatedly disperse from non-preferred hosts when there is an opportunity to do so, but if ballooning is hindered for even a few hours, larvae will become sedentary on any host. Arborvitae Juniper Maple Experiments also supported prediction D, that larvae would tend to disperse from non-preferred hosts and a a a 100 a remain on preferred hosts. Most larvae silked from foliage a of the non-preferred host maple in laboratory experiment 6, but tended to remain on arborvitae. Similarly, almost all the 80 b b larvae dispersed from maple in field experiment 2, but many remained on juniper and arborvitae. 60 b b In nearly all of the experiments in which larvae had access b to materials with which to make a bag, sedentary behaviour 40 was associated with bag construction. In field experiment 1, the few young larvae that did not disperse from maple had Accumulated % dispersing Accumulated 20 constructed bags. When larvae were caged with foliage in 246824laboratory experiment 4, sedentary individuals tended to be Time (h) those that had bags. In laboratory experiment 5, a decline in dispersalrate on arborvitae was associated with bag con- Fig. 7. Relationship between the accumulated percentage of Thyridopteryx ephemeraeformis larvae that dispersed and the time struction. Finally, in field experiment 2, larvae that did not since they had been released on foliage of three tree species (field disperse from either preferred or non-preferred hosts con- experiment 2). n ¼ 15 larvae for the arborvitae treatment and 25 structed bags. Despite the consistent association between larvae per juniper and maple treatment. Means SE with different sedentary behaviour and bag construction, a small propor- letters are significantly different (t-tests; P < 0.05). tion of larvae that had bags nevertheless silked in both

# 2004 The RoyalEntomologicalSociety, Ecological Entomology, 29, 327–335 334 Robert G. Moore and Lawrence M. Hanks laboratory and field experiments (laboratory experiments 4 is based upon work supported by the Cooperative State and 5, field experiments 1 and 2). In contrast, earlier studies Research, Education, and Extension Service, U.S. Depart- have reported that 36–75% of aerially dispersing larvae ment of Agriculture, under Agreement nos 99-35316-7850 had at least partially constructed bags (Cox & Potter, 1986; and 2001-35316-11275. Ghent, 1999). Cox and Potter (1986) also report, however, that all neonates silked immediately after emergence, but those not carried away by wind later constructed bags. It therefore seems likely that the proportion of neonates that References balloon without bags is determined by weather conditions; under conditions favourable for ballooning, most dispersers Baerg, W.J. (1928) Three shade tree insects. University of Arkansas will not have bags. Agricultural Experiment Station Bulletin, 224, 1–25. The findings in the work reported here support the Barbosa, P., Krischik, V. & Lance, D. (1989) Life-history traits of forest-inhabiting flightless Lepidoptera. American Midland hypothesis that polyphagy in T. ephemeraeformis is main- Naturalist, 122, 262–274. tained by variation among larvae in the tendency to disperse Barrows, E.M. (1974) Some factors affecting population size of the and the limited time available for dispersal, but that relative bagworm, Thyridopteryx ephemeraeformis (Lepidoptera: Psychi- preference for plant species is determined by the inclination dae). Environmental Entomology, 3, 929–932. to disperse. The ability to complete development on a vari- Capinera, J.L. & Barbosa, P. (1976) Dispersalof first-instar ety of host species is obviously adaptive in an insect that has gypsy moth larvae in relation to population quality. Oecologia, limited opportunity to move between hosts as a neonate, 26, 53–64. and subsequently becomes even more sedentary. In fact, Carrie` re, Y. (1992) Larvaldispersalfrom potentialhosts within a there is a strong association between flightlessness and population of a generalist herbivore, Choristoneura rosaceana. polyphagy in other families of Lepidoptera (reviewed by Entomologia Experimentalis et Applicata, 65, 11–19. Cox, L.C. & Potter, D. (1986) Aerialdispersalbehavior of larval Barbosa et al., 1989). bagworms, Thyridopteryx ephemeraeformis (Lepidoptera: This study provides insight into factors responsible for Psychidae). Canadian Entomologist, 118, 525–536. the patchy distribution of T. ephemeraeformis in urban Davis, D.R. (1964) Bagworm of the western hemisphere. habitats. Sedentary behaviour on preferred hosts juniper Bulletin of the United States National Museum, 244, 1–217. and arborvitae would result in an accumulation of larvae Diss, A.L., Kunkel, J.G., Montgomery, M.E. & Leonard, D.E. and high-density populations where regulation by natural (1996) Effects of maternalnutrition and egg provisioning on enemies is not effective. Larvae are strongly inclined to silk parameters of larval hatch, survival, and dispersal in the gypsy from the non-preferred host maple, and neonates emerging moth, Lymantria dispar (L.). Oecologia, 106, 470–477. on such hosts therefore would be likely to disperse, and Futuyma, D.J., Cort, R.P. & van Noordwijk, I. (1984) Adaptation aerially dispersing larvae are more likely to reject them to host plants in the fall cankerworm (Alsophila pometaria) and its bearing on the evolution of host affiliation in phytophagous and re-disperse (see Ward et al., 1990). Nevertheless, larvae insects. American Naturalist, 123, 287–296. of the same age showed variation in their innate tendency to Ghent, A.W. (1999) Studies of ballooning and resulting patterns of silk, the extreme case being the one that constructed a locally contagious distribution of the bagworm Thyridopteryx bag with foliage of tree of heaven. As a result, a few neo- ephemeraeformis (Haworth) (Lepidoptera: Psychidae). American nates emerging on non-preferred hosts may not disperse, Midland Naturalist, 142, 291–313. and some ballooning larvae inevitably would become Gromysz, K., Kalkowski, W. & Wojtusiak, R.J. (1960) Experimental stranded on non-preferred hosts at the end of their first investigations on innate behavior, when building its bag, of the day when they become sedentary. These larvae then will caterpillar Psyche viciella Schiff. in its ontogenic development. construct a bag, take up permanent residence, and may Folia Biologica, 8,14–268. complete development. The interacting influences of the Hanks, L.M. & Denno, R.F. (1998) Dispersaland adaptive deme formation in sedentary coccoid insects. Genetic Structure and host plant and innate variation in dispersal behaviours of Local Adaptation in Natural Insect Populations: Effects of larvae therefore result in higher population densities on Ecology, Life History, and Behavior (ed. by S. Mopper and S. juniper and arborvitae, but also assure the persistence of a Y. Strauss), pp. 239–262. Chapman & Hall, New York. broad host range. Haseman, L. (1912) The evergreen bagworm. University of Missouri Agricultural Experiment Station Bulletin, 104, 308–330. Howard, L.O. & Chittenden, F.H. (1908) The bagworm (Thyr- Acknowledgements idopteryx ephemeraeformis Haw.). USDA Bureau of Entomology Circular, 97, 1–10. We gratefully acknowledge advice provided by J. A. Ellis in Johnson, W.T. & Lyon, H.H. (1988) Insects That Feed on Trees and rearing bagworms, and her assistance in collecting insects Shrubs. Cornell University Press, Ithaca, New York. Jones, F.M. (1927) The mating of the Psychidae (Lepidoptera). for experiments while the first author was in active military Transactions of the American Entomological Society, 53, service in Kuwait. We also appreciate helpful comments on 293–314. the manuscript by M. D. Ginzel, J. F. Tooker, two Jones, F.M. & Parks, H.B. (1928) The bagworms of Texas. Texas anonymous reviewers, and editor M. D. E. Fellowes. This Agricultural Experiment Station Bulletin, 382, 1–36. work was in partial fulfilment of a MS degree for R.G.M. Kaufmann, T. (1968) Observations on the biology and behavior of from the University of Illinois at Urbana–Champaign and the evergreen , Thyridopteryx ephemeraeformis

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