Response of red alder (Alnus rubra) seedlings to
a woolly alder sawfly (Eriocampa ovata)
John H. Markham and C.P. Chanway
Abstract: We monitored the effect of an outbreak of Eriocampa ovata L.on experimental Alnus rubra Bong. seedlings duringthe year of the outbreak (1993) and the following growing season. Seedlings planted on low-elevation sites had significantly
more of their leaves damaged (>50% per tree) than plants on high-elevation sites (50% par arbre) que les plants situs sur des sites haute
target plant. The three high- and three low-elevation planting siteswere located within the University of British Columbia MalcolmKnapp Research Forest near Haney, B.C. All the sites had been domi-nated by coniferous forests and harvested. A bulldozer was used toclear all vegetation from the sites and remove the organic soil layer inearly July 1992. Plots were laid out using a 2-m spacing. Planting tookplace from July 21 to 23, 1992, with treatments randomly assigned tothe plots. Plants were approximately 4 cm tall at the time of planting.During the experiment the sites were weeded on up to a weekly basis.Height and diameter measurements were made on a monthly basisduring the growing seasons of 1993 and 1994 on all plants. The rootsand shoots of the plants were harvested in August 1994 and totalbiomass was determined from the plant mass dried at 65C. Themonthly census data were converted to total dry mass estimates foreach plant using a linear regression of height diameter2 versus massof harvested plants (r2 = 0.964). Relative growth rates (RGR) werecalculated on a monthly basis in 1993 and 1994. RGRs were deter-mined for each plant by taking the change in the log-transformedestimate of plant mass between census periods and dividing by thenumber of days in the period. Methods are more fully described else-where (Markham 1996).
The seedlings started showing signs of herbivore damage in earlyMay 1993, with damage peaking in late August, some trees beingtotally defoliated. On all but the most severely attacked trees, herbi-vore damage was confined to leaf tissue in the lower part of the crown.Where herbivore damage was heavy, the leaves in the top of the crownand soft stem tissue near the ends of branches were also eaten. Treesthat were defoliated produced new leaves that were generally free ofherbivore damage.
On August 17, 1993, and July 29, 1994, we quantified the herbi-vore damage on each tree in the experiment into the following sixclasses: (0) no damage, (1) 125% of leaves damaged, (2) 2650% ofleaves damaged, (3) 5175% of leaves damaged, (4) 76100% ofleaves damaged, and (5) complete removal of all leaf tissue. A pre-liminary sampling of wild red alder showed that these classes couldconsistently be distinguished on experimental trees. The herbivoredamage classes were used as a dependent variable to compare thedegree of herbivore damage between sites and as an independentvariable when examining the relationship between herbivore damageand plant growth.
The effect of herbivore damage on the growth of plants was com-pared by examining both the mass and growth of plants experiencingdifferent levels of herbivore damage. The effect of herbivore damageon plant mass and growth was analyzed using single-factor ANOVAswith log mass or RGR as the dependent variable and herbivore dam-age class as the independent variable for each date that mass andgrowth were estimated. Differences between herbivore damageclasses were determined using a Ryans Q test (Day and Quinn 1989).Mortality of plants (24%, with 50% of the total mortality occurring onone high-elevation site) and the differences in the numbers of plants
receiving different levels of herbivore damage meant that these analy-ses were performed using unequal sample sizes.
Feeding preferencesA feeding preference experiment was set up to determine if changesin herbivore damage between years were related to changes in thepalatability of previously defoliated trees. The experimental designand statistical analysis follow Peterson and Renauds (1989) recom-mendations of using replicated controls for changes in plant mass inthe absence of herbivores. On July 22, 1994, leaves and sawflies werecollected. Undamaged leaves from previously defoliated and undam-aged plants were collected from sites G and G40, the only sites withdefoliated trees in 1993. Although 10 trees on these sites had beendefoliated in 1993, only seven of these could provide undamagedleaves at the time of sampling. Sawflies were collected from thesesites but were not collected from the trees providing the leaf samples.
In the laboratory, leaves from a single defoliated tree were ran-domly matched with leaves from a single undamaged tree. Threefeeding preference dishes were made from each leaf pair by placingleaf sections of approximately the same fresh mass (0.335 0.115 g,mean 1SD) into petri dishes. Two of the dishes were used as repli-cate feeding preference trials with five sawflies placed in each dish.The remaining dish received no sawflies and was used as a control forchanges in leaf weight independent of consumption by sawflies. Thesawflies were allowed to feed for 16 h after which all leaf sectionswere weighed. The difference in the change in weight of the two leafsections was calculated as the percentage of the initial leaf weight.The mean difference of the replicate dishes was compared with thedifferences in weight change of leaves in the absence of sawflies usinga paired t-test.
The year of the sawfly outbreak, herbivore damage class var-ied significantly both between planting elevations (p = 0.013)and among sites within elevations (p < 0.000 for both high- andlow-elevation sites) according to log-likelihood ratio analysis(Table 1). The mean of the mean herbivore damage class foreach site was 3.15 0.64 ( 1SD) on the low-elevation sitescompared with 0.867 0.69 on the high-elevation sites. Thehighest levels of damage occurred on sites G and G40, withplants having an average of greater than 50% of their leavesdamaged. One site (H110) had no evidence of damage on anyplant. Herbivore damage the following year (1994) was lessthan 25% of leaves per tree damaged on all but one site (G40).Mean plant mass at the end of the growing seasons variedsignificantly between sites, with plants on the low-elevationsite attaining a greater mass.
G (65) G40 (85) K (250) H30 (530) H90 (650) H110 (550)
ln mass 2.81.2a 1.71.0b 1.20.9c 1.00.8c 1.20.9c 0.20.3dDamage class 3.3 3.7 2.4 0.9 1.4 0.0
ln mass 5.11.3a 4.11.6b 3.11.4c 2.81.4c 3.41.5bc 1.61.7cDamage class 0.8 1.5 0.8 0.6 0.6 1.0
Note: Mass is given as ln-transformed values 1SD, with sites that are not significantly different followed by acommon letter. Elevation (m) of each site is given in parentheses.
Table 1.Mean plant mass at the end of the growing season and mean herbivore damage class in 1993 and1994 on each site.
Can. J. For. Res. Vol. 28, 1998592
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On high-elevation planting sites, where plants experiencedsignificantly lower levels of herbivory, there was no relation-ship between the level of herbivore damage and plant growthor size of plants. On low-elevation planting sites, plants withhigh levels of herbivore damage were significantly larger thanplants with low levels of herbivore damage at the end of thegrowing season (Fig. 1). By the end of the growing season,plants with no herbivore damage were significantly smallerthan plants with less than 50% of their leaves damaged. Thelargest plants were those with greater than 50% of their leavesdamaged. These differences were detected in May 1993 beforeany sawflies could be seen on the plants. The RGRs variedover the growing season for plants with different levels ofherbivore damage. From April until June 1993, there was apositive relationship between the degree of herbivore damageand RGR. By August, however, the relationship was negative,plants with all of their leaf tissue removed having significantlylower RGRs than all other plants. Plants with 50100% leafdamage had significantly lower RGRs than plants with lessthan 50% leaf damage. Plants with a high degree of herbivoredamage in 1993 remained significantly taller throughout the
1994 growing season. Herbivore damage in 1993 had no effecton RGRs in 1994.
Most trees in the study had a lower herbivore damage classin 1994 than in 1993 (Table 2). However, there was a positiverelationship between damage in 1993 and 1994 for plants ex-periencing high levels of herbivory in 1993. Eight of the nineplants that had greater than 50% damaged leaves in 1994 alsohad greater than 50% damaged leaves in 1993, even though
Fig. 1. Mean plant sizes and relative growth rates (RGR) for plants on low-elevation sites receiving different levels of herbivore damage in1993. +, no damage; , 125% leaves damaged; h, 2650% leaves damaged; e, 5175% leaves damaged; , 76100% leaves damaged; Y,complete leaf tissue removal. Vertical bars join plant damage classes that are not significantly different at p = 0.05 according to a Ryans Q test.
Class (1993) 0 1 2 3 4 5
0 14 19 3 1 0 0
1 8 9 3 0 0 0
2 9 6 0 0 0 0
3 14 23 2 0 1 0
4 0 24 1 4 1 0
5 1 3 3 1 1 0
Table 2.Frequency of plants in each herbivore damage class in1993 and 1994.
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only 55.2% of the plants sustained this level of damage in1993. This relationship was considered significant accordingto log-likelihood ratio analysis (p = 0.0240), although the lowcell frequencies render the test statistic biased (Zar 1984).
Feeding preferencesAfter being exposed to sawflies for 16 h, most leaves fromboth damaged and undamaged trees showed visual signs ofherbivory. Leaf sections from undamaged trees lost approxi-mately two times more mass in the presence of sawflies thandid leaf sections from damaged trees, while there was no dif-ference in the absence of sawflies (Table 3). Mass loss fromleaves of defoliated and undamaged trees ranged from 6.96 to46.8% and from 1.73 to 77.6%, respectively. A paired t-test onthe differences in mass loss between the two leaf types incontainers with and without sawflies revealed a greater differ-ence in mass loss when sawflies were present (p = 0.020),indicating that the sawflies preferred leaves from previouslyundamaged plants.
Although herbivory did result in plant growth reduction late inthe growing season, plants with a high level of herbivore dam-age were larger at the end of the growing season due to higherRGRs early in the growing season. Since herbivory was notcontrolled, the total reduction in plant yield due to herbivory isdifficult to quantify. The selection of fast-growing plants bysawflies prevents an estimation of the RGR of these plants, inthe absence of herbivory, late in the growing season. Red alder,like other Betulaceae, tends to lose leaves in midsummer(Kikuzawa 1982; Markham 1996), and summer drought con-ditions in the region tend to retard growth (Harrington et al.1994). Leaf loss by all plants due to a summer drought maytherefore limit the relative effects of reduced growth due toherbivory on attacked trees. Variation in plant growth in thisstudy was accounted for by differences in site conditions andthe specific alder/Frankia combination (Markham 1996). Dif-ferences in plant performance due to these treatments weredetectable in 1992, before the herbivore outbreak. Althoughherbivory reduced differences in plant performance betweentreatments, it did not alter the relative ranking of the treatmenteffects on plant growth. A higher incidence of herbivory onfaster growing individuals, similar to what we found, is pre-dicted by a number of hypotheses. Plants growing under con-ditions of low resource availability are predicted to make moreof an investment in defensive structures either through selec-tion for defense of long-lived tissues (Loehle 1987; Coley et al.1985) and (or) allocating more carbon to the production ofsecondary metabolites (Herms and Mattson 1992). An in-creased incidence of herbivory with increased productivity hasbeen found in another alder species, European black alder (Al-
nus glutinosa (L.) Gaertn.), but there was no relationship be-tween or within other alder species tested (Hendrickson et al.1991).
The feeding preference experiment and the general reduc-tion in damage in 1994 support the hypothesis of induced re-sistance, although other factors may have resulted in lowerherbivore populations throughout the region. However, the ob-servation that plants with greater than 50% of their leaves dam-aged in 1994 were likely to have greater than 50% of theirleaves damaged in 1993 does not support the induced defensehypothesis. This may have resulted from the overwinteringbehaviour of the sawflies. In the fall, sawflies drop to theground and overwinter under the host tree (Mackay and Wel-lington 1977). In the spring, emerging adults would likely en-counter and lay eggs on the same host plant, even though morepalatable individuals may exist. Myers and Williams (1987)found that while the quality of leaves from red alder trees thatwere repeatedly attacked by western tent caterpillar decreased,in terms of their effect on larval development, the caterpillarscontinued to feed on these trees. Also, in a wild cotton (Go-sypium thurberi) population, leaf miner damage late in theseason was positively correlated with leaf miner damage earlyin the season, even though the plants showed an inducibledefense response (Karban and Adler 1996). Induced chemicaldefenses in plants may therefore have little effect on the dis-persal of adults or larvae and therefore may only reduce her-bivore damage by decreasing the fitness of herbivorepopulations and not an individuals feeding behaviour.
Overall, these data show that even under conditions of com-plete leaf tissue removal, if herbivores select fast-growing in-dividuals the reduction in growth due to herbivory may notreduce subsequent plant size to match that of slower growing,uneaten plants. This then suggests that periodic outbreaks ofherbivores that select the fastest growing individuals in a popu-lation may exert little selective pressure in terms of the plantsability to compete with slower growing, chemically defendedplants in the same population.
We would like to thank Laura Lazo and Masahiro Shishido forhelp with the field work. This study formed part of thePh.D. requirements for J.H.M., and we would like to thank PhilBurton, Brian Holl, Peter Jolliffe, Ellen MacDonald, RoyTurkington, Bart van der Kamp, and the staff at the Universityof British Columbia Malcolm Knapp Research Forest for theirhelp and advice. Two anonymous reviewers also made valu-able comments on a previous version of this manuscript. Thisstudy was funded by a NSERC op...