Budbreak Phenology and Natural Enemies Mediate Survival of First-Instar Forest Tent Caterpillar (Lepidoptera: Lasiocampidae)

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1 POPULATION EcoLOGY Budbreak Phenology and Natural Enemies Mediate Survival of First-Instar Forest Tent Caterpillar (Lepidoptera: Lasiocampidae) DYLAN PARRY,l.3 JOHN R. SPENCE,l AND W. JAN A. VOLNEy2 ABSTRACT Environ. Entomol. 27(6): (1998) Synchrony of egg hatch with budbreak has been proposed as an important component in the population dynamics of many spring feeding forest Lepidoptera. Here, we examine the consequences of phenological asynchrony with the budbreak of trembling aspen (Populus tremu loides Michaux) for cohorts of forest tent caterpillar, MalDcosoma disstria Hubner, larvae in north central Alberta, Canada. The timing of eclosure was adjusted through temperature exposure in the laboratory so that pairs of hatching egg bands were placed on trees belonging to a single aspen clone at intervals beginning 2 d before and at 2, 6, 10, and 18 d after budbreak. On each tree, 1 egg band was protected from predation with a sleeve cage and the other was left unprotected. Larvae from later hatching cohorts required significantly more calendar days and nearly 3 times as many degree-days to complete the 1st instar as did those hatching in synchrony with budbreak. Survivorship of later hatching cohorts was reduced drastically by invertebrate predation in unprotected groups but no change in overall survival was recorded for protected groups, suggesting that protracted development times caused by declining foliar quality enhanced the success of natural enemies. We hypothesize that a narrow phenological window in host quality after budbreak and its interaction with natural enemies has exerted strong selective pressure on larvae to emerge from eggs as early as possible in the spring and that this window is a potent force in determining the dynamics of low density populations of tent caterpillars. KEY WORDS MalDcosoma disstria, trembling aspen, asynchrony, tri-trophic interactions, invertebrate predation, phenological window AN INCREASINGLY LARGE body of evidence indicates that synchrony of egg hatch with budbreak in the spring is key to the success of many folivorous Lepidoptera in temperate forests (e.g., Feeny 1970, Mitter et al. 1979, Raupp et ai. 1988, Du Merle 1988, M.D. Hunter 1992, A. F. Hunter 1993, Quiring 1994, Stoyenoff et ai. 1994, Mattson et al. 1996, Lawrence et al. 1997). Larvae emerging more than a few days before budbreak may face starvation, whereas those emerging late must contend with decreasing foliar quality as the season progresses. Temporal reductions in foliar quality for herbivores have been linked to decreased nitrogen and water content, increased leaf toughness, and in some plants, elevated levels of secondary phytochemicals, all of which can have negative effects on growth rate, pupal mass, fecundity, and survival of tree feeding insects (Scriber 1977, Mattson 1980, Scriber and Slansky 1981, Krischik and Denno 1983). These factors alone or in combination are thought to be a major force in shaping the life history strategies of spring feeding caterpillars (Nothnagle and Schultz 1987, A. F. Hunter 1991). 1 Department of Entomology, University of Alberta, Edmonton, AB, Canada TSG 2E9 2 Natural Resources Canada, Canadian Forest Service, Northern Region, Edmonton, AB, Canada T6H Current address: Department of Entomology, Michigan State University, East Lansing, MI In addition to the direct effects on insect performance, temporal declines in foliar quality may also act indirectly through the 3rd trophic level (Price et ai. 1980). Extended development time caused by poor host plant quality may increase larval exposure to natural enemies (Feeny 1976; Moran and Hamilton 1980; Price et al. 1980; Raupp and Denno 1983; Schultz 1983,1988). Despite general acceptance of this idea, remarkably few studies have explicitly tested this "slow growth-high mortality hypothesis" (Clancy and Price 1987, Benrey and Denno 1997). Congruent with predictions of this theory, slow growing Pieris rapae (L) caterpillars suffered concomitant increases in parasitism relative to their faster growing siblings (Loader and Damman 1991, Benrey and Denno 1997). Similarly, larvae of the leaf beetle Plagiodera versicolora Laicharting grew more slowly and suffered higher mortality from coccinelid predators when feeding on leaves from previously defoliated trees than on higher quality leaves from undefoliated controls (Raupp and Denno 1984). However, the generality of these results is equivocal. In a review of pests feeding on resistant and susceptible varieties of cultivated crops, negative effects on predators and parasitoids occurred as often as synergistic effects in response to increased pest development time (Hare 1992). Benrey and Denno (1997) suggested that the outcome of interactions between development time and natural enemies may depend on whether or not X/98/ $02J)O/O 1998 Entomological Society of America

2 December 1998 PARRY ET AL.: A PHENOLOGICAL WINDOW FOR M. disstria 1369 the herbivore feeds freely or is concealed, and on features of the host plant which enhance or reduce natural enemy access. Clearly, further experimentation is needed to ascertain the true nature of such tri-trophic interactions, particularly with respect to forest ecosystems. Tent caterpillars, Malacosoma spp. (Lepidoptera: Lasiocampidae), are classic early season defoliators, overwintering as pharate larvae within eggs and emerging in synchrony with budbreak of their primary hosts. As with other spring feeding Lepidoptera, it is thought that they are constrained to early season feeding by phenological declines in host plant quality (Nothnagle and Schultz 1987, Fitzgerald 1995). However, Myers (1992) detected no effect of 3- to 6-wk delays in hatch after budbreak on the western tent caterpillar, Malacosoma califomicum (packard), and speculated that population declines of it and other Malacosoma spp. could not be explained by asynchrony with host plant phenology. Anecdotal evidence suggests that for the forest tent caterpillar, Malacosoma disstria Hubner, at least, asynchrony with host plant development does occur in nature and may have important ramifications for population dynamics (Hodson 1941, Blais et al. 1955, Fitzgerald and Costa 1986). Many studies on the effects of phenological asynchrony between herbivores and host plants are weakened by variation in the phenology and quality of trees used in the experiment (Stoyenoff et al. I994). Trembling aspen, the primary host of the forest tent caterpillar across its northern range, is clonal; all ramets within a single clone are virtually identical in the timing of budbreak and other morphological and physiological qualities (Barnes 1969, Chilcote et al. 1992), thus offering an ideal system to study the effects of varying hatch time on caterpillar performance. In our study, we used a single clone of trembling aspen to examine the effects of phenological asynchrony on the development time and survival of Ist-instar forest tent caterpillars. Materials and Methods Manipulation of Egg Hatch and Stocking. The study was conducted at George Lake in north central Alberta, Canada, in 1993 (see Parry et al. 1997a for site description). To remove intertree variability in the timing of budbreak as a source of error, we selected 75 trembling aspen trees that belonged to a single clone, established using morphological characteristics (see Barnes 1969). Study trees were "'15 yr old and ap proximately equal in height ("'4 m), aspect, and exposure to sunlight. We identified each tree with an aluminum tree tag and randomly assigned them to 5 treatment groups of 15. Preliminary studies in this aspen stand established that most predation on early instar forest tent caterpillars was caused by aerial and arboreal predators and that patchy mortality caused by terrestrial, ambulatory predators such as ants could be locally intense but was relatively unimportant overall (Parry et al. 1994). Therefore, we eliminated the potentially confounding effects of the clumped distribution of ants by placing a Tangletrap (Tanglefoot, Grand Rapids, MI) barrier at the base of each tree. Egg bands for the experiment were collected from an outbreak population near Cooking Lake, Alberta. To remove viable n!lclear polyhedrosis virus, egg bands were scraped With a razor blade to remove the spumaline covering before surface sterilization in a 5% sodium hypochlorite solution for 2 min, followed by a distilled water rinse for 1 h (procedure modified from Grisdale 1968). Egg bands were maintained in a controlled temperature chamber at 3 C until use. We used a subset of these egg bands to determine that hatching required 7 d at room temperature after removal from cold storage. Thus, to ensure that egg bands hatched on the day of placement in the field, groups of egg bands were removed from cold storage and placed at room temperature 7 d before each stocking. The phenology of the trees was monitored carefully using an aspen bud development classification scheme similar to that of Parry et al. (1997b). Single egg bands were attached with thin copper wire to the distal end of 2 dominant, lateral branches on each of 15 trees in the 1st group of trees when the buds were soft and the leaf tips were becoming visible (condition class 4, Parry et al. 1997b). Egg bands were placed on these trees as the larvae were beginning to chew through the chorion. Hatching is synchronous in forest tent caterpillar with >90% of the hatch complete within 4 d of 1st larval emergence (Raske 1974). To separate tree effects on survival from natural enemy effects, 1 egg band on each tree was protected with a fine mesh pollination sleeve (Fibe-Air, Kleen-Test Products, Brown Deer, WI) and the other was left fully exposed. At 4-d intervals, each of the subsequent groups of aspen received the same treatment. The final 15 aspen trees received egg bands on 25 May 1993, 8 d after the 4th group of egg bands was deployed. The first 2 stocking dates (5 and 9 May) bracketed the approximate natural hatching dates for forest tent caterpillar in the forest surrounding the experimental trees, established by placing egg bands on trees in the study area the previous fall and monitoring them for hatch. Insect Performance. To measure insect performance, we recorded development time and survivorship for each family group of larvae. Development time from hatch through the 1st molt was calculated in 2 ways. First, we recorded the number of calendar days required to complete the 1st instar. Second, to facilitate comparisons between groups of larvae from each of the 5 different hatch dates, the number of degree-days required to complete the 1st instar were calculated. Daily maximum and minimum temperatures were obtained from an Alberta Environment weather station at Sion, Alberta, km southwest of the field site. There were no significant bodies of water or orographic features between the study site and the weather station. The developmental threshold temperature has not been determined for forest tent caterpillar; therefore we used a 5 C threshold as recommended by Ives (1973). Because we were only interested in the relative degree-day accumulations

3 1370 ENVIRONMENTAL ENToMOLOGY Vol. 27, no. 6 between groups hatching on different days, beginning at the date of stocking, we estimated the degree-days accumulated by each family group of larvae by subtracting the threshold temperature from average daily temperature calculated as the midpoint of daily maximum and minimum and summed over the period of the experiment (e.g., Higley et al. 1986). At the end of the 1st instar, we collected and counted all surviving larvae from each family group. The number alive was then expressed as a proportion of the number that hatched to give an accurate estimate of the survivorship for each family group. The number of neonate larvae was determined by counting hatched eggs in each egg band under a dissecting microscope. Each hatched egg was marked with a fine tip felt pen as it was counted and every 5th egg band was recounted by a different observer to test the accuracy of the counts. Eclosed eggs are differentiated easily from the exit holes of egg parasitoids by the location, shape, and size of the emergence hole (Williams et al. 1996). Statistical Analyses. Hierarchical analysis of variance (ANOVA) (PROC GLM in SAS, SAS Institute 1992) with trees nested in hatch date was used to determine the effects of delayed hatch on both measures of development time. "Trees within hatch date" was used as the error term to test the effect of hatch date. Effects of caging treatment, trees within hatch date, and interactions were tested using the residual mean square as the error term. Graphical representation of the residuals suggested that variances were correlated with the means for both calendar days and degree-days. Thus, both variables were log transformed to improve homogeneity of variances (Sokal and Rohlf 1981). Analyses were performed on the transformed data, which was back-transformed for presentation. Pairwise t-tests (P = 0.05) (lsmeans statement, PDIFF option, PROC GLM) were used to separate main effect and interaction least-square means (SAS Institute 1992). The same ANOVA procedure as above was used to examine hatch date effects on survival. Before analysis, percentage survival data were arcsine square-root transformed to meet assumptions of normality (Sokal and Rohlf 1981). Transformed data were back-transformed to their original scale for presentation purposes. As above, pairwise t-tests on the least-square means were used to separate main effect and interaction means. Results The phenology of egg hatch had dramatic effects on development time. ANOVA of the log-transformed calendar days indicated that timing of hatch had significant effects on development time (F = ; df = 4, 70; P < 0.001). Pairwise t-tests on the least-square means suggested that caterpillars from later hatching egg bands required significantly longer to complete the 1st instar in both the sleeve cage protected and unprotected treatments (Fig. 1A). Caterpillars within sleeve cages developed faster than unprotected cat- C.. ca "0 C II) o A B Hatch Date Hatch Date D Sleeve Cage II Unprotected III Sleeve Cage II Unprotected Fig. 1. Mean number of calendar days (A) and degreedays (B) required to complete the 1st instar for forest tent caterpillar cohorts eclosing on 5 different dates. Analyses were performed on log-transformed data that were backtransformed for presentation. Error bars are 95% CI because standard errors have no meaning for log-transformed data (Sokal and Rohlf (1981). Same letters on each bar indicate no significant difference (preplanned pairwise t-tests, P > 0.05) among means within treatments (sleeve cage or unprotected) and between treatments on the same date. erpillars (F = 17.67; df = 1,61; P < 0.001), presumably because of the slightly warmer temperatures within the sleeve. There was no interaction between caging treatment and hatch day (F = 1.38; df = 4, 61; P = 0.252). As with calendar days, an ANOVA using logtransformed degree-days suggested that development time varied significantly with hatch date (F = ; df = 4, 70; P < 0.001). Comparisons among the least-

4 December 1998 PARRY Er AL.: A PHENOLOGICAL WINDOW FOR M. disstria C 50 :;, (/) 25 o Hatch Date Fig. 2. Survival (mean ± SE) from hatch to 1st molt for forest tent caterpillar cohorts eclosing on 5 different dates. Analysis was performed on arcsine square-root transformed data that were back-transformed for presentation. Same letters on each bar indicate no significant difference (preplanned pairwise t-tests, P > 0.05) among means within a treatment (sleeve cage or unprotected) and between treatments on the same date. square means showed that caterpillars from later hatching groups required significantly more degreeday accumulation to complete the 1st instar (Fig. IB). There was no interaction between caging treatment and hatch date (F = 1.95; df = 4, 61; P = 0.114); although as with calendar days, caged and uncaged treatments were significantly different (F = 16.81; df = 1,61; P < 0.001). A nested ANOV A indicated that hatch date had significant effects on survivorship (F = 10.39; df = 4, 70; P < 0.001) and that survival differed significantly between larvae in sleeve cages and those unprotected (F = 29.94; 1,57; P < 0.001). In addition, there was a significant hatch date X caging treatment interaction (F = 3.53; df = 4, 57; P = ). Pairwise comparisons between the least-square means indicated that there was no difference in survival among hatch dates in the sleeve cage treatment, whereas larvae in later hatching groups within the unprotected treatment suffered increasingly higher mortality as hatch became more asynchronous with budbreak (Fig. 2). Most of the mortality in the unprotected treatment appeared to be caused by the pentatomid bug, Podisus brevispinus (Phillips), formerly P. modestus UhI. Observations indicated that pentatomids did not become active in the plots until 14 May. By this time, naturally hatching forest tent caterpillars in the area were already well into the 2nd instar (see Parry et al. 1997a for forest tent caterpillar phenology at the George Lake study site). Thus, the 1st cohort and most of the 2nd cohort hatched before pentatomids became prevalent, whereas caterpillars from the 3rd and later stockings hatched with pentatomids already present. Pentatomids were observed frequently on the experimental trees, feeding on larvae, foraging, or resting nearby. There were often 2 or 3 P. brevispinus in close proximity to experimental larvae, sometimes standing within a colony, with.caterpillars seemingly oblivious to both the bug and e disappearance of their siblings. Feeding pentatomids left the shriveled carcasses of their victims stuck to the silk resting mats spun by forest tent caterpillar, which aided in our ability to determine causes of mortality. Subsequent feeding trials showed that individual bugs denied food for 24 h consumed 36.6 ± 4.02 (mean ± SE) (n = 10) 1st instar forest tent caterpillars in the following 24 h, which was significantly higher (I-way ANOVA: F= 28.31; df = 1, 18; P < 0.001) than for 2nd instar caterpillars (14.4 ± 1.13, n = 10). Given that the average colony in our experiment consisted of ± 3.14 first instars, our data show that pentatomids could exact a significant toll once forest tent caterpillar colonies were discovered. In addition to pentatomids, salticid spiders were observed on several occasions consuming caterpillars. The sudden disappearance of entire colonies without any trace occurred several times particularly in the latest hatching group. Because early instars rarely abandon their natal tree and extensive searches of the surrounding trees did not reveal the missing colonies, we suspect that birds may have been responsible for the disappearance of these larvae. We also note that no larvae were ever found stuck to the tanglefoot barriers at the tree bases nor were any observed spinning from the tree on silk threads. Discussion Both development time and survival of forest tent caterpillars were affected significantly by phenological asynchrony with budbreak of trembling aspen (Figs. 1 and 2). There is anecdotal evidence that the effects we describe are significant and do occur in nature. The collapse of a large population of forest tent caterpillar in Ontario and adjacent Manitoba in 1953 was attributed partially to a cool spring decoupling the synchrony between the developing larvae and trembling aspen (Blais et al. 1955). Fitzgerald and Costa (1986) reported a similar temperature driven asynchrony between forest tent caterpillar and another host species, sugar maple, Acer saccharum (Marsh.). In both cases, greatly protracted development of larvae was associated with population reductions. The authors of these studies suggested that in years characterized by cool springs, host trees may develop faster relative to forest tent caterpillar growth, forcing caterpillars to eat foliage that is more mature than that nonnally consumed. In our study, increased development time of late hatching forest tent caterpillar larvae was likely the result of changes in aspen foliar quality. Foliar nitrogen and water content in trembling aspen leaves decreases rapidly after budbreak (James and Smith 1978, Hunter and Lechowicz 1992, Lindroth and Hwang

5 1372 ENVIRONMENTAL ENToMOLOGY Vol. 27, no ). The reduction in water content may exacerbate the decline in nitrogen available to caterpillars (Scriber and Slansky 1981). In addition to the seasonal decline in the nutritive value of leaves, secondary chemicals, in particular phenolic glycosides, may have played a role in the delayed development of later hatching larvae. In conjunction with lowered nitrogen levels, constitutive levels of phenolic glycosides have been shown to have significant negative effects on larval performance of several aspen folivores including forest tent caterpillar (Bryant et al. 1987, Lindroth and Bloomer 1991, Lindroth and Hwang 1996). These effects are likely to have greater impact on young caterpillars because of the reduced sensitivity of older instars to dietary quality changes (Lindroth and Bloomer 1991). In addition, the highly mobile late instars typically abandon their natal tree and feed extensively on species other than aspen (D.P. and }.R.S., unpublished data), thus avoiding any reduction in aspen foliar quality. The results of our study are in marked contrast to those of Myers (1992) who found that western tent caterpillar feeding on red alder, Ainus rubra (Bong), experienced no change in survivorship despite delays in hatching as long as 6 wk after budbreak. The study did not assess survival directly; instead, Myers (1992) estimated it from correlates with tent size done in unmanipulated populations, although these correlations explained as little as 50% of the variance in population density. Furthermore, no quantitative measures of development time or other estimates of insect performance were provided. Myers (1992) did note that the egg masses of caterpillars experiencing late hatching conditions were smaller than those hatching synchronously with budbreak. Female pupal mass is strongly correlated with fecundity in forest tent caterpillar (y = (SE = ) x ,?- = 0.81, n = 70, P < 0.001; D.P., unpublished data), indicating that phenological asynchrony may have affected the fecundity of insects used by Myers (1992) through reductions in pupal mass. Studies using other species of tent caterpillars such as M. americanum (F.), M. califomicum, and the palearctic species, M. nell strium (Moschulansky) have shown that they are susceptible to phenological changes in foliage quality and perform poorly on mature leaves (see Fitzgerald 1995 and references therein), supporting the generality of our findings with forest tent caterpillar. Although many studies have addressed the direct consequences of phenological asynchrony on spring feeding Lepidoptera, ours is among the few to document an important indirect effect of phenological mismatches. The increase in development time allowed a relatively minor predator of forest tent caterpillar (see Parry et al. 1997a) to play a much more important role, apparently by altering spatial and temporal components of a predator-prey relationship. We found that although P. brevispinus was capable of preying on later instar forest tent caterpillar, it had its greatest impact on 1st instars. Similarly, for eastern tent caterpillars, Evans (1983) found that once through the early instars, vigorous defensive behaviors employed by older larvae dissuaded most Podisus spp. attacks. Thus, in our experiment, phenological asynchrony served to hold larvae in a vulnerable instar for a protracted period. Second, the extended time frame when 1st instars were available allowed P. brevispinus a much longer period in which to locate the experimental colonies. Once a colony was discovered, individuals of P. brevispinus would remain in the vicinity, often eliminating all the larvae through their feeding activity. This foraging pattern led to a bimodal distribution of survivorship, with undiscovered colonies enjoying generally high survival, whereas discovered colonies were drastically reduced or eliminated. Across the northern portion of its range, forest tent caterpillar are among the earliest emerging forest Lepidoptera, and inclement weather at budbreak and during the early feeding period can cause significant mortality (Blais et al. 1955, Witter 1979). Forest tent caterpillar hatch appears to coincide with budbreak of the earlier flushing aspen clones in a stand. This suggests that optimizing host plant quality is not the only selective factor operating on forest tent caterpillar; if that were the case, considerable risk from inclement weather could be mitigated if hatch was instead timed to coincide with budbreak in later flushing clones, which may occur as much as 2-3 wk later. The emergence of other species of aspen feeding lepidopterans such as the large aspen tortrix, Choristoneura con jlictana (Walker), also coincides with budbreak in early flushing clones (Witter and Waisenen 1978, Witter 1983, Parry et al. 199Th). We suggest that forest tent caterpillar and other early emerging aspen folivores have evolved a life-history strategy that risks the consequences of occasional poor springs to exploit the narrow phenological window when host plant quality is optimal and pressure from natural enemies is low. Hatching of forest tent caterpillar often commences several days before aspen budbreak. This appears to cause no ill effects because neonate forest tent caterpillar larvae are resistant to starvation for as long as 9 d at temperatures commonly encountered in early spring in the prairie provinces of Canada (Smith and Raske 1968). This behavior suggests that early emergence may be preferable to late eclosure. Studies with some spring feeding Lepidoptera such as winter moth, Opherophtera brumata (L), have shown that hatch may be tied to individual tree phenology (e.g., Van Dongen et al. 1997). This aspect of phenological synchrony has not been investigated for forest tent caterpillar but we suggest that the high degree of starvation resistance inherent to neonates is an adaptation to variable budbreak, precluding tight relationships at the level of individual trees. In addition, gravid female forest tent caterpillar moths are highly mobile, and unlikely to be patch restricted in contrast to species exhibiting a high degree of tree fidelity. It is unknown if forest tent caterpillar females can differentiate between early and late flushing clones or if egg hatch is controlled partially by factors such as cues released by developing buds or swelling branchlets that could increase synchrony with the host plant. These would be fruitful areas of additional research.

6 December 1998 PARRY gr AL.: A PHENOLOGICAL WINDOW FOR M. disstria 1373 Although Myers (1992) speculated about the role of phenological asynchronies in the collapse of outbreaks, asynchrony may have much greater significance for low density populations between outbreaks. In low density populations where forest tent caterpillar already suffers heavy mortality from predators and to a lesser extent parasitoids (Parry 1995, Parry et al a), small increases in development time caused by phenological asynchrony and the concomitant reduction in survival caused by predation could have a significant negative impact on populations. These events would only need to occur occasionally for populations to be maintained at low levels and could even be a mechanism whereby regional populations are synchronized. Ives (1973) found that early, warm springs preceded outbreaks by 2-4 yr in the prairie provinces. Warm conditions provide optimal opportunity for synchronous development of aspen and forest tent caterpillar, and rapid caterpillar growth under these conditions may allow escape in time from natural enemies. Research on the phenology of forest tent caterpillar egg hatch relative to tree development under natural conditions when populations are at low levels could provide further insight on the initiation of incipient outbreaks. Acknowledgments We are grateful to T. N. Kutash (University of Alberta) for sewing the sleeve cages and A. R. Meyer (University of Alberta) for technical assistance. We thank R. Weingardt (Department of Animal Science, University of Alberta) for statistical advice and are grateful for the identification of Podisus brevispinus provided by D. Shpeley (Strickland Museum, University of Alberta). We thank A. F. Hunter (University of Massachusetts) for comments and suggestions that improved an earlier version of the manuscript. 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