BEHAVIOR Facilitative Effects of Group Feeding on Performance of the Saddleback (: )

VICTORIA L. FIORENTINO,1 SHANNON M. MURPHY,2 TERESA M. STOEPLER,1,3 1,4 AND JOHN T. LILL

Environ. Entomol. 43(1): 131Ð138 (2014); DOI: http://dx.doi.org/10.1603/EN13144 ABSTRACT Gregarious feeding by herbivores is a widely observed, yet poorly understood, behavioral adaptation. Previous research has tested the importance of group feeding for predator deterrence, noting the ubiquity of among group-feeding , but few studies have examined the role of feeding facilitation for aggregates of insect herbivores. We tested the hypothesis that group feeding has facilitative effects on performance of the , stimulea Clemens, a generalist herbivore of deciduous trees. In an understory forest setting, we reared alone or in groups on two different plants, white (Quercus alba L.) and American beech (Fagus grandifolia Ehrlich), and recorded multiple measures of insect performance during regular Þeld censuses. As predicted, A. stimulea caterpillars feeding in groups on white oak had increased relative growth rates compared with caterpillars feeding alone, and the magnitude of this facilitative effect varied among censuses, conferring beneÞts both early and late in development. By contrast, no facilitative effects of group feeding were detected on beech, suggesting that the beneÞts of facilitative feeding may be host speciÞc. On both hosts, caterpillar development time was slightly faster for group-feeding cohorts compared with their solitary counterparts. Because early instar caterpillars are particularly vulnerable to predation and parasitism, even modest increases in growth rates and reductions in development time may decrease exposure time to enemies during these vulnerable stages. On both hosts, group feeding also reduced the trade-off between individual development time and cocoon mass, suggesting that feeding efÞciency is improved in group feeders relative to solitary caterpillars.

KEY WORDS facilitation, gregarious, group feeding, Limacodidae, plantÐinsect interaction

Gregariousness is a widespread phenomenon among and Bryant 1983). For example, in the saturniid cat- insect herbivores, and is commonly observed in tree- erpillar, Hemileuca oliviae Cockerell, aggregative hoppers, aphids, sawßies, and caterpillars (Costa and feeding is thought to discourage predator attacks by Pierce 1997). BeneÞts of gregariousness typically man- exaggerating the appearance of urticating spines ifest as increases in insect survival, growth rates, and (Capinera 1980). When basking in the sun, caterpillars body size (Stamp 1980, Hunter 2000). Within insects, in groups are better able to retain heat due to their gregarious feeding behavior is believed to have proximity to one another, as well as the convective evolved many times as an adaptation to a wide variety recycling of heat emanating from one individual to its of selective pressures (Bowers 1992, Costa and Pierce neighbors (Porter 1982, Benrey and Denno 1997). A 1997), including repellant defense against predators groupÕs control over the extent of its aggregation and (Fitzgerald 1993, Costa 1997, Hunter 2000, Allen the individual proximity of its members facilitates 2010), dilution of predation risk (Hunter 2000), in- thermoregulation, which can reduce water loss and creased feeding efÞciency via managing or overcom- thus increase growth rate (Bowers 1992, Klok and ing host plant defenses (Young and Moffett 1979, Tsu- Chown 1999). A variety of other largely anecdotal baki and Shiotsu 1982, Clark and Faeth 1997, Fordyce beneÞts to aggregation exist, such as vibrational com- and Agrawal 2001), microclimate control (Porter munication to track conspeciÞcs (Cocroft 2001) or to 1982, Bowers 1992, Klok and Chown 1999), and en- warn each other of nearby predators (Yack et al. hancement of aposematic signaling (Sillen-Tullberg 2001). In addition to gregariousness as a behavioral adaptation, it may also arise as a secondary outcome of 1 Department of Biological Sciences, George Washington Univer- -clustering, which is thought to increase fecundity sity, 2023 G Street NW, Suite 340, Washington, DC 20052. in insects facing a high likelihood of mortality from 2 Department of Biological Sciences, University of Denver, Mudd predation and adverse environments (Stamp 1980, Hall, Room 309, Denver, CO 80208. Courtney 1984, Faraji et al. 2002). 3 Present address: Agricultural Research and Extension Center, Virginia Tech, 595 Laurel Grove Rd., Winchester, VA 22602. The prevalence of group feeding generally de- 4 Corresponding author, e-mail: [email protected]. creases as insects mature, and in the case of caterpil-

0046-225X/14/0131Ð0138$04.00/0 ᭧ 2014 Entomological Society of America 132 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 1 lars, later instars often mark distinct shifts in sociality (Inouye and Johnson 2005, Grant 2007). For example, both the eastern and western tent caterpillars (Mala- cosoma americanum F. and Malacosoma disstria Hu¨ b- ner, respectively) are highly social until they reach the ultimate instar, when caterpillars suddenly abandon their tents and leave the group (and often the host plant) to complete development and locate pupation sites (Fitzgerald 1995). In the gregarious caterpillar casta Scott (Limacodidae), caterpillars feed in groups of several 100 individuals for the Þrst several instars, after which group size decreases grad- ually until individuals reach the sixth and seventh instars, during which they mainly feed alone (Reader and Hochuli 2003). These ontogenetic shifts from gre- garious to solitary behavior may be inßuenced by a variety of factors, including a shift in the balance of costs and beneÞts of gregariousness (Reader and Hochuli 2003), an avoidance response to pathogens (Hochberg 1991), avoidance of food limitation, or the restricted proximity of adjacent caterpillars due to defensive armature, such as urticating spines (Capin- era 1980). Although the anti-predator and thermoregulatory beneÞts of group feeding have been well established, the direct, facilitative effects of group feeding on con- sumption and growth rates have received consider- ably less attention. Group feeding ideally enables herbivores to limit consumption of induced allelo- chemicals by quickly consuming an area of foliage Fig. 1. The saddleback caterpillar, Acharia stimulea (Li- before allelochemicals can be induced in damaged macodidae). (A) A late-instar caterpillar with typical color leaves (Krischik et al. 1991). Alternatively, group feed- patterning and stinging spines. (B) Early instar A. stimulea ing may permit insects to overcome physical plant caterpillars feeding in a group, with their previous feeding defenses such as trichomes and leaf toughness, which damage visible in the upper left corner. Photo credits: John are effective deterrents for solitary insects (Young and Lill and Doug McCaskill. Moffett 1979). Finally, group feeding may simply per- mit gregarious insects to increase consumption rates (Tsubaki and Shiotsu 1982, Rhoades 1985, Benrey and on its dorsum and protruding tubercles containing Denno 1997, Fordyce 2003). numerous urticating spines (Fig. 1; Dyar 1899, Epstein In this study, we designed an experiment to explic- 1996, Murphy et al. 2010). These caterpillars can be itly test for facilitative effects of group feeding in the found throughout eastern deciduous forests from Mas- saddleback caterpillar, Acharia stimulea Clemens sachusetts to and west to Missouri (Covell (Lepidoptera: Limacodidae). A. stimulea caterpillars 1984). Adult ßy in July and August, and cater- are well-known throughout the eastern United States pillars are generally found in the late summer (Wag- for their vivid coloring (Fig. 1A) and intensely urti- ner 2005, Murphy et al. 2011). Final-instar caterpillars cating spines, which are an effective defense against form a cocoon of calcium oxalate coated with urticat- an array of predators (Murphy et al. 2010). Early ing deciduous spines (Epstein 1996, Murphy et al. instars typically forage in sibling groups (Fig. 1B), but 2010). whether group feeding beneÞts them through facili- Like most species of Limacodidae, the caterpillars tative bottom-up effects is unknown. We recorded are polyphagous, and have been found feeding on a multiple measures of performance for A. stimulea cat- wide assortment of mostly woody host plants (Wagner erpillars foraging alone or in groups inside of predator 2005, Lill 2008, Murphy et al. 2011). In the vicinity of exclosures on two different host plants, which allowed our study site, common hosts include oak (Quercus us to assess the direct beneÞts of group feeding in the spp.), hickory (Carya spp.), American beech (Fagus absence of enemies. grandifolia Ehrlich), pawpaw (Asimina triloba L.), spicebush ( benzoin L.), black locust (Robinia pseudoacacia L.), and Eastern redbud (Cercis canaden- Materials and Methods sis L.). A. stimulea caterpillars are classiÞed as preso- Study System. A. stimulea, commonly known as the cial, having an intermediate level of sociality between saddleback caterpillar, is a temperate species of slug solitary insects, like the praying mantis, and eusocial caterpillar (Lepidoptera: Limacodidae) that has an insects, like ants and vespid wasps (Fitzgerald and aposematic, ßuorescent green, saddle-shaped pattern Peterson 1988, Costa 1997). February 2014 FIORENTINO ET AL.: FACILITATIVE EFFECTS OF GROUP FEEDING 133

Our experiment took place at the Little Bennett with seven individuals (“small group”), and two bags Regional Park in northern Montgomery County, MD. with 14 individuals (“large group”). This resulted in 7 This 1,500-ha park is located in the Piedmont plateau solitary and 42 group caterpillars on each of the eight east of the Blue Ridge Mountains and consists of a mix trees, totaling to 392 caterpillars. Solitary caterpillars of upland hardwood forest and managed grasslands. within the same tree, as well as group caterpillars The second growth forest contains a mixed canopy of within the same exclosure bag, shared the same hatch , hickories, (Acer spp.), walnut (Juglans date. To homogenize potential genetic (i.e., family) nigra L.), and tulip poplar (Liriodendron tulipifera L.), effects, each of the eight trees included offspring from and an understory of saplings of the canopy species as no fewer than Þve females, and a minimum of three well as ßowering dogwood ( florida L.), iron- different females contributed to each group of mul- wood (Carpinus caroliniana Walter), black gum tiple caterpillars, as well as each treeÕs suite of solitary (Nyssa sylvatica Marshall), sassafras (Sassafras albi- individuals. dum [Nutt.] Nees), (Viburnum spp.), and The status (alive/dead/missing) and size of each black cherry (Prunus serotina Ehrlich). caterpillar were recorded weekly. Missing caterpillars Experimental Design. Our objective was to deter- were assumed to be dead. Body length of each cater- mine whether in the absence of predators, group feed- pillar (to the nearest 0.1 mm) was measured with dial ing facilitated growth and survival of saddleback cat- calipers on the Þrst day of Þeld exposure and weekly erpillars on each of two host plants: white oak thereafter for 5 wk, for six censuses in total over a span (Quercus alba) and American beech (Fagus grandifo- of 36 d (17 JulyÐ21 August). We used body length lia). To assess caterpillar performance, the growth rather than head capsule width because it is not pos- rate, survival, development time, and cocoon mass sible to measure head capsule widths in Limacodidae were recorded for caterpillars placed in mesh exclo- and standard curves relating body length to mass for sure bags in each of three densities: 1, 7, and 14 cat- A. stimulea have been generated previously (Murphy erpillars per bag (the Þrst density was the “solitary” et al. 2011). Bags and caterpillars were transferred to treatment and the latter two densities were our fresh branches as needed (weekly and more often as “group” treatments). We chose a group size of seven caterpillars grew larger) to avoid food limitation in the individuals as a “typical” group size, based on the mean largest group sizes; when bags had to be moved for one number of laid per cluster in A. stimulea (range, treatment, bags from all treatments were moved to 1Ð85 eggs per cluster; Murphy et al. 2011). The larger equalize handling time of larvae. At each census, we group size of 14 was chosen based on our estimate of also noted whether any of the caterpillars in the mul- how many caterpillars could reasonably be contained tiple-caterpillar exclosure bags were actively feeding in exclosures. together (i.e., clustered, feeding in proximity on the Experimental A. stimulea caterpillars originated same leaf). from a laboratory colony that we established using a Five days following the Þnal Þeld census, when the mix of locally caught caterpillars and adult moths, and most rapidly developing caterpillars were nearing pu- experimental caterpillars were derived from 20 differ- pation, all caterpillars were harvested and returned to ent female lineages that hatched between 25 and 28 the laboratory, keeping track of the tree, treatment, June 2008. White oak and beech are known to differ and bag they came from. Once in the laboratory, in host plant quality for A. stimulea caterpillars caterpillars were reared individually in 0.5-liter deli (S. M. M. and J. T. L., unpublished data), so we initially containers to complete their development. The con- reared all caterpillars on the same high-quality host tainers were provisioned with a moistened Þlter paper plant, Eastern redbud (Cercis canadensis: Fabaceae), disc and fresh excised leaves of their assigned host to minimize differences in caterpillar body size at the plant species collected from the Þeld site. The date start of the experiment. One week before beginning that each individual formed a cocoon was recorded the Þeld experiment, 500 early instar A. stimulea cat- and cocoons were weighed to the nearest 0.01 mg with erpillars that had been reared since hatching on red- a microbalance within 30 d of cocoon formation. Co- bud were transferred to either white oak or beech coons were overwintered in environmental chambers leaves (n ϭ 250 on each) to allow them time to ha- and their emergence success and sex were recorded bituate to their assigned host plants. the following spring. Eight large trees (four white oak and four beech) Data Analysis. All statistical analyses were con- located across a single hillside at the Þeld site were ducted using SAS 9.1 or JMP Pro 9 (SAS Institute Inc., haphazardly chosen for use in the experiment. On 17 Cary, NC). In preliminary analyses, there were no July 2008, caterpillars were placed onto foliage in differences between the small- and large-group treat- green zippered 20- by 40-cm Þne-mesh insect-rearing ments (N ϭ 7 or 14 per bag), so we combined these sleeves (BioQuip, Rancho Dominguez, CA; referred two treatments into a single category (group feeding) to as “exclosure bags” hereafter) so that larvae could for Þnal analyses. To test whether the initial size of be relocated, larval groups would remain associated, caterpillars in the density treatments was similar, we and predators would be excluded. Exclosure bags conducted t-tests on initial lengths of caterpillars in were tied onto one of the lower branches of each of the two treatments (solitary vs. group) on each host the eight trees after removing resident . plant separately. To obtain measurements of relative Each of the eight trees contained 11 exclosure bags; growth rate (RGR, hereafter), we converted Þeld seven bags with one individual (“solitary”), two bags measures of caterpillar body size (body length in mm) 134 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 1 to biomass (mg) using a standard curve developed for A. stimulea reared on each host plant, as described in ϭ Murphy et al. (2011): white oak: log10(mass) ϫ Ϫ ϭ log10(length) 3.133 1.400; beech: log10(mass) ϫ Ϫ log10(length) 3.245 1.568. The RGR of each solitary caterpillar was then estimated as: RGR ϭ (ln- Ϫ Ϫ [masstϩ1] ln[masst])/(t2 t1). For caterpillar groups (density of 7 or 14), the RGRs of individuals could not be calculated due to our inability to track individuals across censuses; instead, we calculated the RGR for each group using the mean mass/bag/census, which also avoided problems with nonindependence of caterpillars within bags. In sum, all analyses were conducted using the “bag” as the unit of replication. Density effects on RGR were analyzed using PROC Mixed (Littell et al. 1996) with tree as a random block effect and density (solitary or group) and census as Þxed effects; the two host plants were tested separately. The REML option was used to estimate random effects and compound symmetry was used in structuring the covariance matrix (Lit- tell et al. 1996). To test for relative differences in caterpillar perfor- mance between density treatments within each tree, we conducted paired t-tests comparing the mean val- ues for the response variables cocoon mass and de- velopment time (days from egg hatch to cocoon for- mation), for each density treatment (averaged across bags) on each tree (N ϭ eight pairs). Preliminary Fig. 2. Percent survival of A. stimulea experimental cat- analyses showed that responses differed between host erpillars in both density treatments, solitary (one individual plants, but there was no evidence of host plant ϫ per exclosure bag) and group (seven or 14 individuals per density treatment interactions for either variable, al- exclosure bag), on two host plants, (A) white oak and (B) lowing us to examine the relative differences in per- American beech, at four time points: the Þrst day of the Þeld formance for the combined set of eight trees. In experiment (Census 1 [C1]), the last day of the Þeld exper- addition, we examined the relationship between in- iment (Census 6 [C6]), after cocoon formation in the lab- oratory (Cocoon), and after emergence the following dividual development time and cocoon mass using spring (Moth). linear regression and used t-tests to compare the re- gression coefÞcients between density treatments for each host plant (Zar 1999). Survival of caterpillars in lars feeding in the largest group size (14 caterpillars each density treatment during the Þeld portion of the per exclosure bag) may have experienced short-term experiment was compared using the YatesÕ corrected food limitation before moving them to a fresh branch. ␹2 test (Zar 1999). We note, however, that any incidental food limitation To test for potential effects of unequal sex ratios would tend to bias against detecting feeding facilita- among treatments, we conducted two-sample t-tests tion, making our results conservative. We observed to compare the cocoon mass, and development times evidence of active group-feeding in the exclosure bags of solitary vs. group feeding caterpillars separately by during 73% of the white oak censuses and 59% of the sex for the subset of individuals in each treatment beech censuses. group that survived to cocoon formation and emerged Initial Lengths of Experimental Caterpillars. The as moths the following spring (white oak: solitary ϭ initial lengths of caterpillars in the two density treat- 71% of original experimental caterpillars, group ϭ 63%; ments (solitary and group) did not differ (white oak: ϭ ϭ ϭ ϭ ϭ ϭ beech: solitary 68%, group 57%). t188 0.77, P 0.44; beech: t189 0.82, P 0.41). However, initial sizes of caterpillars did differ among host plants; on average, caterpillars reared on white Results oak for 1 wk before Þeld placement measured 0.4 mm, Overall, Þeld survival of the bagged caterpillars or 10% greater body length than caterpillars reared on ϭ Ͻ (through Census 6) was high (96% vs. 89% for solitary beech (t379 4.76, P 0.0001). and gregarious caterpillars, respectively) but did not Density Effects on RGRs. The RGR of A. stimulea differ among the two density treatments on either host caterpillars feeding on both host plants varied over the (white oak: YatesÕ corrected ␹2 ϭ 0.68, P ϭ 0.41; beech: course of development (census effect on white oak: ␹2 ϭ ϭ ϭ Ͻ ϭ Ͻ YatesÕ corrected 0.70, P 0.40; Fig. 2). Cater- F4, 202 63.53, P 0.0001; beech: F4, 202 24.43, P pillars never entirely consumed the food in their bags, 0.0001; Fig. 3). On white oak, the average RGR for but there were two or three instances when caterpil- cohorts of caterpillars feeding in groups was higher February 2014 FIORENTINO ET AL.: FACILITATIVE EFFECTS OF GROUP FEEDING 135

Density Effects on Caterpillar Development Time. All caterpillars experienced 41 d of Þeld exposure, which was, on average, 54% of their total development time (the remainder of their development occurred in the laboratory, both before and following the Þeld experiment). Development time was reduced by Ϸ2d for group-feeding compared with solitary caterpillars ϭ ϭ (one-tailed paired t7 2.25, P 0.03), which repre- sents a modest (3%) reduction for these slow-devel- oping caterpillars. The mean caterpillar development time of females was signiÞcantly longer than that of ϭ Ͻ males on both white oak (t112 4.50, P 0.0001) and ϭ Յ beech (t110 3.91, P 0.0001). Development time and cocoon mass were positively correlated for caterpillars on both host plants (white oak, solitary: r2 ϭ 0.33, df ϭ 27, P ϭ 0.0017; white oak, group: r2 ϭ 0.18, df ϭ 138 , P Ͻ 0.0001; beech, solitary: r2 ϭ 0.27, df ϭ 26, P ϭ 0.0061 [outlier excluded from regression]; beech, group: r2 ϭ 0.16, df ϭ 147, P Ͻ 0.0001; Fig. 4AÐD). In comparing the slopes of the relationship between de- velopment time and cocoon mass between density treatments, we found that for both white oak and beech, the slope of the relationship (␤) was reduced for the group-feeding caterpillars compared with sol- itary caterpillars (␤ Ϯ 1 SE for white oak, group ϭ 11.12 Ϯ 2.06; white oak, solitary ϭ 20.41 Ϯ 5.80; beech, group ϭ 6.46 Ϯ 1.22; beech, solitary ϭ 10.10 Ϯ 3.36; Fig. 4AÐD). While t-tests comparing the slopes be- Fig. 3. Relative growth rate (LSM ϩ 1 SE; mg ϫ dayϪ1) tween density treatments were not statistically differ- ϭ of A. stimulea caterpillars in solitary (one caterpillar per ent, there was a strong trend (white oak: t161 1.35, ϭ ϭ ϭ exclosure bag) and group (7 or 14 caterpillars per exclosure P 0.09; beech: t169 1.13, P 0.13). bag) treatments on (A) white oak and (B) American beech over the course of Þve intercensus intervals in the Þeld. Asterisks denote censuses where treatment differences were Discussion signiÞcant according to post hoc tests (TukeyÕs honestly We found that A. stimulea caterpillars feeding in signiÞcant difference tests). groups had increased RGRs compared with those feeding alone on white oak, which supports the hy- pothesis that in at least certain ecological contexts, ϭ ϭ than for caterpillars feeding alone (F1, 202 14.81, P group feeding can facilitate individual growth. How- 0.0002), but the magnitude of this effect varied among ever, the beneÞts of group feeding varied over the ϫ ϭ censuses (census density interaction: F4, 202 2.85, course of development, as indicated by the signiÞcant ϭ P 0.025), appearing both early and late in develop- treatment ϫ census interaction on white oak, with ment (Fig. 3A). In contrast to caterpillars feeding on beneÞts accruing both early and, somewhat surpris- white oak, group feeding did not inßuence RGR for ingly, later in development. ϭ caterpillars feeding on beech (density: F1, 202 0.48, Many species of gregarious caterpillars feed in ϭ ϫ ϭ ϭ P 0.49; census density: F4, 202 1.65, P 0.162) groups earlier in their development and their behavior (Fig. 3B). often becomes more solitary as they near pupation Density Effects on Cocoon Mass. Within a tree, the (Hochberg 1991, Reader and Hochuli 2003, Inouye cocoon mass obtained by caterpillars reared in groups and Johnson 2005, Grant 2007). When adjusted for ϭ ϭ vs. alone did not differ (paired t-test: t7 0.50, P body size, RGRs and foliar consumption are typically 0.63). However, the mean cocoon mass obtained by highest in early instars and decline as insects grow, as caterpillars reared on white oak was 20% greater than was seen here on both host plants. Very early in de- those reared on beech (across density treatments; t14 velopment, A. stimulea caterpillars (and Limacodidae ϭ 3.59, P ϭ 0.003). Female cocoons were signiÞcantly more generally) feed by skeletonizing foliage, scrap- heavier than male cocoons on both host plants (48 and ing small epidermal patches with their mandibles (Ep- 38% heavier on white oak and beech, respectively). stein 1996). It is generally thought that such feeding When examined separately by sex, cocoon mass com- behaviors in neonate caterpillars result from an in- parisons between solitary and group treatments (av- ability to generate sufÞcient mandibular force to chew eraged within trees) did not differ on white oak (fe- through leaf veins and/or cuticles and may promote ϭ ϭ ϭ ϭ male: paired t7 1.18, P 0.33; male: t7 0.87, P higher rates of assimilation due to the greater selec- ϭ ϭ 0.44) or on beech (female: t7 0.33, P 0.76; male: tivity of tissues (i.e., consuming less Þber; Godfrey et ϭ ϭ t7 0.56, P 0.61). al. 1989, Hochuli 2001). However, around the third 136 ENVIRONMENTAL ENTOMOLOGY Vol. 43, no. 1

Fig. 4. Regression of caterpillar development time vs. cocoon mass (mg) of individual A. stimulea caterpillars in the (A) white oak solitary treatment, (B) white oak group treatment, (C) American beech solitary treatment, and (D) American beech group treatment. The outlier in “C” was excluded from the regression (development time 100 d). Note the reduced slopes of the regression in the group treatments relative to the solitary treatments. instar, A. stimulea caterpillars begin group “edge-feed- to explain. If anything, larger instars of A. stimulea ing,” and have been observed to spin silken pads on the might be expected to have decreased RGR in groups leaf surfaces, which likely aid in adhesion. The cater- due to possible food limitation inside the exclosure pillars used in this experiment were all in the edge- bags. However, we have observed wild late-instar cat- feeding stage by the time they were placed in the Þeld, erpillars feeding gregariously, which suggests that ag- and it may have been easier for those in groups to gregation late in development is likely to be beneÞcial overcome the physical barriers of these relatively for A. stimulea in nature. One possible explanation is tough, late-season oak and beech leaves. Our Þnding that group feeding may generate a nutritional sink, of signiÞcant facilitative effects of group feeding on resulting in increased plant quality (Karban and white oak but not beech may in part reßect differences Agrawal 2002). This may be especially important for in physical characteristics of the foliage; on average, late instars that feed late in the season, when plant beech foliage is tougher, has more Þber, and has less quality is declining. In addition to bottom-up facilita- water content than white oak (Ricklefs and Matthew tive effects, group feeding may serve to deter preda- 1982), making it a low-quality host, which is reßected tion by amplifying the aposematic signal of these in reduced performance measures of A. stimulea. bright, spiny caterpillars. Group feeding may also be inhibited in some way on Gregarious feeding may also facilitate faster con- beech, perhaps due to the smaller leaf size and biomass sumption, often of more nutritious tissue. For in- compared with white oak, and was reßected in the stance, aggregation might enable caterpillars to feed lower incidence of observed group feeding on beech on highly nutritious and thus highly protected apical vs. white oak (59 vs. 73% of censuses). portions of leaf tissue (Fordyce and Agrawal 2001, Density treatment effects on RGR later in the de- Fordyce 2003). The removal or consumption of velopment of A. stimulea are somewhat more difÞcult trichomes, or other defensive structures, can increase February 2014 FIORENTINO ET AL.: FACILITATIVE EFFECTS OF GROUP FEEDING 137 the speed of locomotion (Young and Moffett 1979, pillars need more time to consume the necessary nu- Fordyce and Agrawal 2001). An increase in the speed trition, which may place them at greater risk in the of locomotion may increase total consumption, short-term. We found that cocoon mass and develop- thereby increasing growth rate and reducing devel- ment time are positively correlated, yet A. stimulea opment time, with possible indirect effects on survival caterpillars feeding in groups enjoy a slightly shorter when exposed to natural enemies. development time, and thus a likely reduction in pre- After just 1 wk of feeding on the two host plants dation risk, while suffering less of a reduction in co- before Þeld exposure, caterpillars fed on white oak coon mass, as evidenced by the trend of reduced were signiÞcantly larger than those fed on beech, most slopes of development time vs. cocoon mass for cat- likely due to the nutritional advantage of white oak erpillars in the group vs. solitary treatments. Facilita- leaves. However, because there were no differences in tive effects of this type may be subtle and likely re- mean initial size for caterpillars in the two density quire large Þeld experiments to uncover. treatments within a host plant, differences in RGR Our study on the gregarious feeding behavior of A. detected in the Þeld represented real treatment ef- stimulea demonstrates that there is moderate evidence fects. White oak has higher foliar nitrogen content to support the hypothesis that feeding in groups en- than beech (2.32 vs. 2.16%) and slightly higher water hances caterpillar Þtness by increasing growth rates content (59 vs. 57%; J. T. L. and S. M. M., unpublished and reducing development time, which may indirectly data). This superior nutrition resulted in larger cocoon affect Þtness by reducing exposure to natural enemies. masses for caterpillars developing on white oak com- Because placing caterpillars together in exclosure bags pared with beech, but was not evident in either growth does not ensure that all individuals feed gregariously rates or total development time. (although many certainly did in this experiment), the In addition to overcoming physical defenses, group facilitative beneÞts of group feeding observed here are feeding of caterpillars can also enhance its membersÕ likely to be underestimates because not all caterpillars nutritional intake by preventing or limiting the inges- in the group-feeding treatment fed gregariously for tion of harmful host plant allelochemicals. Because the the entire experiment. Future experiments that ex- sheer number of caterpillars in a group causes the amine the beneÞts of group feeding in A. stimulea in group to progress rapidly across leaf tissue while feed- both the presence and absence of enemies are needed ing as compared with the speed of a solitary caterpil- for a more complete understanding of this behavioral larÕs feeding, groups can consume tissue before in- phenomenon. duced defensive allelochemicals reach the area (Rhoades 1985, Tallamy and Raupp 1991, Fordyce 2003). Under this scenario, group feeding enables cat- Acknowledgments erpillars to escape consumption of allelochemicals in- We thank Wendy Hanley and the staff at the Little Ben- duced by their herbivory, thus reducing their negative nett Regional Park for use of the Þeld site and logistical effects, while still exploiting the maximum amount of support. Funding for this project was provided by a Howard host plant tissue (Tsubaki and Shiotsu 1982). Benrey Hughes Medical Institute grant for Undergraduate Science and DennoÕs (1997) study supports the idea of alle- Education to V.L.F. and an NSF grant (DEB-0642438) to lochemical avoidance because they found a lack of J.T.L. We thank L. Power, R. Liebson, and J. Moore for help nutritional beneÞt for laboratory-reared groups of cat- in the Þeld and laboratory. We also thank the DC-PlantÐ erpillars fed on leaves detached from trees before Insect Group (DC-PIG) and the University of Denver Ecol- feeding. However, this type of rapid allelochemical ogy and Evolution reading group for helpful comments on the manuscript. induction has not been described for plants in the family Fagaceae, for example, white oak and beech, both of which mainly contain high-molecular-weight References Cited phenolics characterized by slow turnover (Coley et al. 1985), so are not likely to explain the facilitation ob- Allen, P. E. 2010. 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