Applications of survival analysis in botanical epidemiology

ABSTRACT Data on the occurrence and timing of discrete events such as spore germination, disease onset, or propagule death are recorded commonly in epidemiological studies. When analyzing such "time-to-event" data, survival analysis is superior to conventional statistical techniques because it can accommodate censored observations, i.e., cases in which the event has not occurred by the end of the study. Central to survival analysis are two mathematical functions, the survivor function, which describes the probability that an individual will "survive" (i.e., that the event will not occur) until a given point in time, and the hazard function, which gives the instantaneous risk that the event will occur at that time, given that it has not occurred previously. These functions can be compared among two or more groups using chi-square-based test statistics. The effects of discrete or continuous covariates on survival times can be quantified with two types of models, the accelerated failure time model and the proportional hazards model. When applied to longitudinal data on the timing of defoliation of individual blueberry leaves in the field, analysis with the accelerated failure time model revealed a significantly (P < 0.0001) increased defoliation risk due to Septoria leaf spot, caused by Septoria albopunctata. Defoliation occurred earlier for lower leaves than for upper leaves, but this effect was confounded in part with increased disease severity on lower leaves.     

Valdensia leaf blight of highbush blueberry caused by Valdensinia heterodoxa, a new fungal disease in Japan

In July 2003, a new disease occurred on leaves of highbush blueberry (Vaccinium corymbossum L.) in Iwate, Japan. Leaves initially had brownish spots, which subsequently developed into large lesions with concentric rings, resulting in premature defoliation. Teardrop-shaped conidia infecting leaves were visible by the naked eye as small protuberances in the center of lesions. Star-shaped conidia were sporadically produced on large lesions. The causal fungus was identified as Valdensinia heterodoxa, based on cultural, morphological and genetic studies. Inoculation tests showed that the fungus reproduced lesions on detached young leaves of highbush blueberry. A field survey in 2009 indicated that symptoms initially appeared on the lower leaves of basal shoots in late May, and the disease rapidly progressed on leaves of basal shoots, eventually spreading to lateral shoots from late June to late July. Removal of all basal shoots in late June significantly reduced disease incidence on lateral shoots in late July.     

Relationship between environmental factors,effects of fungicide applications,and premature defoliation of black locust trees (Robinia pseudoacacia L.)

From 1989 through to and including 1994 extensive premature defoliation of black locust ( Robinia pseudoacacia L.) was observed in a progeny test plantation in Greene County, in the Georgia Piedmont. During July 1991 and 1992, all observed trees suffered greater than 50% defoliation. Leaflets of black locust showing symptoms of leaf spotting began abscising as early as mid-June following wet springs. Onset and progress of defoliation was followed on 50 trees in two plots in 1993 and 1994. In both years, sample trees were cut at the base and allowed to regrow from sprouts. A protectant fungicide, chlorothalonil (Daconil WDG 1.5 g/l water) was applied to run-off weekly to one-half of the growing sprouts beginning 17 April through 22 August 1994 by backpack sprayer. Air temperature, relative humidity, rainfall, and leaf wetness were monitored. Abscission of unprotected leaflets in 1993, a dry, hot year, began in mid-July and averaged 36% by late August; abscission of unprotected leaflets in 1994, a wet, cool year, began in mid-June and averaged 80% by late August; whereas, abscission of protected leaflets in 1994 began in late June and averaged 70% by late August. The Gompertz model described the increase of leaflet abscission with time. The estimated rate of leaflet abscission for unprotected leaflets in 1993 was significantly slower ( k = 0.056/wk) compared to the rate of abscission of unprotected leaflets in 1994 ( k =0.070/wk). Estimated rates of leaflet abscission were not significantly different between protected ( k = 0.063/wk) and unprotected trees ( k =0.070/wk) in 1994. Cumulative hours of leaf wetness of 600 h were associated with initial leaf spotting and defoliation in 1993 and in 1994. Delay in leaflet abscission of protected trees indicates that fungal infection may have contributed to premature defoliation of black locust with onset related to moisture conditions favourable for infection.     

Effect of foliar diseases of wheat on the physiological processes affecting yield under semi-arid conditions

The effects of Septoria leaf blotch (caused by Mycosphaerella graminicola) and leaf rust (caused by Puccinia recondita ) on the physiological processes affecting yield were studied under semi-arid conditions in Israel. In the absence of water stress, photosynthetic activity decreased as the rate of disease development increased. Transpirational activity was reduced in leaves infected by Septoria leaf blotch, but intensified in leaves with slight leaf rust infections (0.5-5% severity). When leaf rust seventy exceeded 5%, the transpirational water loss declined. Both diseases were associated with a decrease in the maximum rate of grain-weight accumulation, but did not affect the duration of weight accumulation. An inverse linear relationship between disease and final grain weight was observed. Under conditions of water stress, photosynthetic activity of leaves slightly infected by Septoria leaf blotch (1-5"., severity) was greater than that of uninfected leaves. Severely infected leaves (" 25% severity) photosynthesized the least. Both diseases were associated with a decrease in the maximum rate of grain weight accumulation, but the duration of accumulation was longer in tillers with a slow rate of disease development than in uninfected tillers. The relationship between disease and final grain weight in these cases was parabolic; yield was increased at low levels of infection. Theoretical explanations and practical implications of these phenomena are presented and discussed.     

Spatiotemporal Description of Epidemics Caused by Phoma ligulicola in Tasmanian Pyrethrum Fields

ABSTRACT Spatial and temporal patterns of foliar disease caused by Phoma ligulicola were quantified in naturally occurring epidemics in Tasmanian pyrethrum fields. Disease assessments (defoliation incidence, defoliation severity, incidence of stems with ray blight, and incidence of flowers with ray blight) were performed four times each year in 2002 and 2003. Spatial analyses based on distribution fitting, runs analysis, and spatial analysis by distance indices (SADIE) demonstrated aggregation in fields approaching their first harvest for all assessment times between September and December. In second-year harvest fields, however, the incidence of stems with ray blight was random for the first and last samplings, but aggregated between these times. Spatiotemporal analyses were conducted between the same disease intensity measures at subsequent assessment times with the association function of SADIE. In first-year harvest fields, the presence of steep spatial gradients was suggested, most likely from dispersal of conidia from foci within the field. The importance of exogenous inoculum sources, such as wind-dispersed ascospores, was suggested by the absence of significant association between defoliation intensity (incidence and severity) and incidence of stems with ray blight in second-year harvest fields. The logistic model provided the best temporal fit to the increase in defoliation severity in each of six first-year harvest fields in 2003. The logistic model also provided the best fit for the incidence of stems with ray blight and the incidence of flowers with ray blight in four of six and three of six fields, respectively, whereas the Gompertz model provided the best fit in the remaining fields. Fungicides applied prior to mid-October (early spring) significantly reduced the area under disease progress curve (P < 0.001) for defoliation severity, the incidence of stems with ray blight, and the incidence of flowers with ray blight for epidemics at all field locations. This study provides information concerning the epidemiology of foliar disease and ray blight epidemics in pyrethrum and offers insight on how to best manage these diseases.     

Barley yield losses due to defoliation of upper three leaves either healthy or infected at boot stage by <Emphasis Type="Italic">Pyrenophora teres</Emphasis> f. <Emphasis Type="Italic">teres</Emphasis>

This paper evaluates, in the greenhouse and under natural conditions, barley yield losses due to defoliation treatments of the upper three leaves either healthy or infected at the boot stage by Pyrenophora teres f. teres. Defoliation was assumed as a loss of a similar leaf area caused by net blotch disease severity of 100%. Contribution to grain yield was defined herein as a difference between defoliation treatments and a treatment where plants lost all their upper three leaves. In contrast, yield losses referred to differences in yield between defoliations and the control. In the greenhouse, removal of the antepenultimate leaf did not affect any yield component. For main stems, defoliating upper three leaves reduced grain yield by 30% and this was mainly due to flag leaf removal. These losses were similar to those induced by net blotch disease under natural conditions, but were of 42% for all tillers. Grain yield losses due to disease severity were not equivalent to the defoliation effect of a similar healthy leaf area. On the other hand and for a significant contribution to grain yield, flag leaf was dependent on the presence of the other two leaves. Inoculation and defoliation of 21 cultivars induced similar grain yield losses of 32%. However, biotic stress reduced by 40% the contribution of their upper three leaves. Under field conditions, yield losses were not significant until barley plants lost more than one upper leaf and flag leaf contribution was equivalent to that of the remaining leaves. Characteristic roots, defined as leaf coefficients for plant performance, were 0.13, 0.06 and 0.01 for the flag, penultimate and antepenultimate leaves, respectively. Because antepenultimate leaves become trivial at the boot stage, we propose that coefficients of the remaining leaves should be used when modelling yield losses due to barley foliar diseases.     

Resistance to Leptosphaeria maculans (phoma stem canker) in Brassica napus (oilseed rape) induced by L. biglobosa and chemical defence activators in field and controlled environments

Effects of pretreatment of Brassica napus leaves with ascospores of Leptosphaeria biglobosa or chemical defence activators [acibenzolar- S -methyl (ASM) or menadione sodium bisulphite (MSB)] on infection by ascospores of Leptosphaeria maculans (phoma stem canker) and development of disease were studied in controlled-environment (phoma leaf spot) and field (phoma leaf spot and stem canker) experiments. In controlled-environment experiments, pretreatment of oilseed rape leaves (cv. Madrigal) with L. biglobosa , ASM or MSB delayed the appearance of L. maculans phoma leaf spot lesions. These pretreatments also decreased the phoma leaf spot lesion area in both pretreated leaves (local effect) and untreated leaves (systemic effect). In winter oilseed rape field experiments in the 2002/03 and 2003/04 growing seasons, pretreatment with L. biglobosa or ASM in October/November decreased not only the number of phoma leaf spot lesions per leaf caused by L. maculans in autumn/winter, but also the severity of phoma stem canker in the subsequent spring/summer. Effects were greater in 2002/03 (when natural L. maculans ascospore release began in September 2002) than in 2003/04 (when ascospore release began in December following a period of dry weather in August/September 2003). These results suggest that pretreatment with biological or chemical defence activators can induce local and systemic resistance to L. maculans , with both short-term effects on the development of phoma leaf spotting and long-term effects on the development of stem canker 8 months later.     

The reliability of visual estimates of disease severity on cereal leaves

Visual estimates of wheat disease severity were compared with actual severities determined using image analysis of tracings of diseased leaves. Septoria tritici , leaf senescence and Erysiphe graminis were studied. Observer estimates were widely scattered about the actual severities (i.e. they were imprecise), differed substantially from the actual severities even after averaging (i.e. they were inacctirate), and varied considerably over short time-scales. Relative bias decreased with increasing disease severity. In a comparison of three seed treatments to control powdery mildew on winter barley, visual assessment errors altered the conclusions of the experiment. Two treatments were statistically indistinguishable on the basis of visual severity estimates, while estimates obtained by image analysis showed that one seed treatment was twice as effective as the other.     

Heterogeneity of peach rust disease progress within the tree canopy

Peach rust (Tranzschelia discolor) is a major foliar disease of peach that can cause severe defoliation. Few epidemiological studies have been conducted on peach rust, and there is no information concerning the spatial distribution of the disease within the canopy. This study aimed to characterise the onset and temporal progress of peach rust in three height strata in peach trees grown in two different orchards: one treated with fungicide and the second non-treated. Evaluations were conducted fortnightly between November and April for two consecutive years. Positional information for the disease within the canopy was obtained by assessing the incidence and severity of peach rust on leaves in both orchards. A linear mixed model with the position of shoots as the fixed effect and cultivars and blocks as random effects was adopted for the data analysis over both seasons, in the fungicide-treated orchard incidence and severity ranged from 60 to 90 % and 0.5 to 2 %, respectively, while in the non-treated orchard incidence and severity ranged from 90 to 100 % and 10 to 15 %, respectively. The area under the disease progress curve was greater for the upper shoots compared to the lower shoots, but the disease progress rates were similar. The logistic and exponential models best fitted the incidence and severity data, respectively. Urediniospores were detected by traps within the experimental area between late winter and early spring. Predominance of autoinfection or alloinfection is discussed.     

不同植物秸秆对番茄及南方根结线虫的影响

为有效防治南方根结线虫,本试验研究了添加不同剂量的玉米秸秆(8.32、4.16、2.08g/kg)、辣椒秸秆(4.16、2.08、1.04g/kg)和茵陈蒿秸秆(4.16、2.08、1.04g/kg)对温室大棚番茄及根结线虫的影响。结果显示,在根结线虫侵染的土壤中添加植物秸秆后30d,玉米秸秆(4.16、2.08g/kg)对番茄株高有显著影响,辣椒(4.16、1.04g/kg)和茵陈蒿(4.16、2.08g/kg)秸秆对番茄茎粗影响显著;60d时经茵陈蒿处理的番茄植株比对照生长发育良好,对形态指标的影响程度依次为茎粗开花分枝;120d时番茄的茎粗、分枝和果实重量均显著高于对照。末次接种后20d调查,每种作物秸秆处理以高剂量对根结线虫的防治效果最好,防治效果依次为:茵陈蒿秸秆辣椒秸秆玉米秸秆,分别为79.60%、71.32%、68.89%,表明茵陈蒿秸秆处理既可降低根结线虫危害程度,又可提高番茄产量。本研究为温室大棚有效防治根结线虫提供了依据。     

Relating plant and pathogen development to optimise fungicide control of phoma stem canker (<Emphasis Type="Italic">Leptosphaeria maculans</Emphasis>) on winter oilseed rape (<Emphasis Type="Italic">Brassica</Emphasis><Emphasis Type="Italic">napus</Emphasis>)

In winter oilseed rape experiments at Rothamsted in 2000/01 to 2002/03 growing seasons, the severity of phoma stem canker epidemics in summer depended on the timing of phoma leaf spot epidemics in the previous autumn, and hence on the timing of Leptosphaeria maculans ascospore release. The first major release of L. maculans ascospores was earlier in 2000 (26 September) and 2001 (18 September) than in 2002 (21 October). Consequently, the autumn phoma leaf spot epidemic was also earlier in 2000 and 2001 than in 2002. The resulting stem canker epidemics were severe by harvest (July) in 2001 and 2002 but not in 2003. No correlation was found between the severity or duration of phoma leaf spotting (lesion days or lesion °C-days) and the subsequent severity of phoma stem canker epidemics. Rates of leaf production and loss were similar in the three growing seasons. Out of ca. 25 leaves produced on plants during each season, leaf numbers 10–14 generally remained on plants for the longest. Treatment with flusilazole + carbendazim in autumn decreased the severity of phoma leaf spotting for several weeks after treatment, decreased the severity of stem canker the following summer and increased yield significantly in 2001 and 2002 but not in 2003. The most effective timings for flusilazole + carbendazim application were when leaves 7–11 were present on most plants and at least 10% of plants were affected by phoma leaf spot. Two half-dose applications of fungicide reduced phoma stem canker and increased yield more than a single full dose application when phoma leaf spot epidemics were early (<800 °C-days after sowing).     

梨叶部病害与梨叶早衰脱落相关性分析

为明确南方梨产区造成梨早衰落叶的原因,本研究对梨叶部病害的发生与早期落叶间的关系进行了调查分析。结果显示:4种叶部病害(梨斑点病、褐斑病、黑斑病和黄脉病)中,除黄脉病外,不同年份间其余3种病害的发生程度与早期落叶率均呈显著正相关;不同品种、果园和时段间这3种病害均呈极显著正相关;7-9月间梨早衰脱落叶片斑点病发病率均达到100%,显著高于其他3种病害;病害防控对减少梨叶部病害发生和降低早期落叶率具有同效性,由此认为防治以斑点病为重点的叶部病害,是控制梨树落叶早衰问题的关键。     

Factors influencing infection of eucalypts by Cylindrocladium pteridis

The pattern of Cylindrocladium pteridis adhesion, germination and penetration in eucalypt leaves was assessed using scanning electron microscopy. The effects of inoculum concentration, leaf wetness period, plant age and branch position of cylindrocladium leaf blight and defoliation severity were assessed in greenhouse studies using two Eucalyptus grandis × E. urophylla hybrid clones. Penetration occurred through stomata, and there was no difference in the number of penetrations between young and old leaves. Percentage leaf area with lesions and defoliation increased with the increase in inoculum concentration (1 × 10² to 10⁵ conidia mL⁻¹), duration of leaf wetness period (6 to 48 h) and plant age (60 to 180 days). Branch position in plants also significantly affected the percentage leaf area with lesions and defoliation, the latter variable being significantly higher at the stem base. The highest values of lesion area were also observed on leaves at the stem base in both clones. The Pearson correlation between defoliation and leaf area with lesions was significant in all experiments ( r  > 0·9) indicating a high association between these two variables.     

Occurrence and development of Colletotrichum acutatum on symptomless blueberry bushes

The anthracnose fungus Colletotrichum acutatum was detected in symptomless blueberry bushes ( Vaccinium spp.) in a Japanese blueberry field. Naturally diseased bushes and their apparently healthy neighbours were selected, and C. acutatum was isolated from the symptomless tissues of each bush from February 2000 to January 2002. Analysis of the diseased bushes during the dormant period revealed that the fungus was able to survive on symptomless tissues, such as shoot bark and bud scales. Furthermore, C. acutatum was consistently isolated from symptomless leaves and shoots of several surrounding symptomless bushes. Arbitrarily primed PCR (ap-PCR) analyses of the fungal isolates obtained from the diseased and symptomless bushes revealed that most C. acutatum isolates were genotypically identical, regardless of their origins. Inoculation tests using leaves of various blueberry cultivars suggested that the presence or absence of symptoms on each bush can not always be explained by differences in cultivar susceptibility, and other factors may be associated with the appearance of symptoms.     

Coincidence of maximum severity of powdery mildew on grape leaves and the carbohydrate sink‐to‐source transition

Grapevine leaves infected with powdery mildew are a source of inoculum for fruit infection. Leaves emerging on a single primary shoot of Vitis vinifera cv. Cabernet Sauvignon were exposed to average glasshouse temperatures of 18°C (0·23 leaves emerging/day) or 25°C (0·54 leaves emerging/day). All leaves on 8–10 shoots with approximately 20 leaves each were inoculated with Erysiphe necator conidia to assess disease severity after 14 days in the 25°C glasshouse. Two photosynthetic ‘source’ leaves per shoot on the remaining 8–10 shoots were treated with ¹⁴CO₂ to identify, by autoradiography, the leaf position completing the carbohydrate sink‐to‐source transition. There was a clear association between the mean modal leaf position for maximum severity of powdery mildew (position 3·7 for 18°C; position 4·4 for 25°C) and the mean position of the leaf completing the sink‐to‐source transition (position 3·8 for 18°C; position 4·7 for 25°C). The mean modal leaf position for the maximum percentage of conidia germinating to form secondary hyphae was 4·2 for additional plants grown in the 25°C glasshouse. A higher rate of leaf emergence resulted in a greater proportion of diseased leaves per shoot. A Bayesian model, consisting of component models for disease severity and leaf ontogenic resistance, had parameters representing the rate and magnitude of pathogen colonization that differed for shoots developing in different preinoculation environments. The results support the hypothesis that the population of leaves in a vineyard capable of supporting substantial pathogen colonization will vary according to conditions for shoot development.     

Phenotypic,molecular and pathogenic characterization of Phlyctema vagabunda,causal agent of olive leprosy

Olive leprosy, caused by the fungus Phlyctema vagabunda, is a classic fruit rot disease widespread in the Mediterranean basin. From 2009 to 2013, new disease symptoms consisting of small circular necrotic leaf lesions, coin branch canker and shoot dieback were observed in Spanish and Portuguese olive orchards showing intense defoliation. Phlyctema‐like anamorphs were consistently isolated from leaves and shoots with symptoms. Representative isolates from affected leaves, shoots and fruits were characterized based on morphology of colonies and conidia, optimum growth temperature and comparison of DNA sequence data from four regions: ITS, tub2, MIT and rpb2. In addition, pathogenicity tests were performed on apple and olive fruits, and on branches and leaves of olive trees. Maximum mycelial growth rate ranged between 0.54 and 0.73 mm per day. Conidia produced on inoculated apple fruits showed slight differences in morphology among the representative fungal isolates evaluated. Phylogenetic analysis clustered all of the Phlyctema‐like isolates in the same clade, identifying them as Phlyctema vagabunda. On fruits, influence of wounding, ripening and cultivar resistance was studied, with cv. Blanqueta being the most susceptible cultivar. On branches, a mycelial‐plug inoculation method reproduced olive leprosy symptoms and caused shoot dieback. On leaves, Koch's postulates were fulfilled and the pathogen caused characteristic necrotic spots and plant defoliation. This is the first time that the pathogenicity of P. vagabunda in olive leaves has been demonstrated.     

Modeling of Relationships Between Weather and Septoria tritici Epidemics on Winter Wheat: A Critical Approach

ABSTRACT Two models for predicting Septoria tritici on winter wheat (cv. Riband) were developed using a program based on an iterative search of correlations between disease severity and weather. Data from four consecutive cropping seasons (1993/94 until 1996/97) at nine sites throughout England were used. A qualitative model predicted the presence or absence of Septoria tritici (at a 5% severity threshold within the top three leaf layers) using winter temperature (January/February) and wind speed to about the first node detectable growth stage. For sites above the disease threshold, a quantitative model predicted severity of Septoria tritici using rainfall during stem elongation. A test statistic was derived to test the validity of the iterative search used to obtain both models. This statistic was used in combination with bootstrap analyses in which the search program was rerun using weather data from previous years, therefore uncorrelated with the disease data, to investigate how likely correlations such as the ones found in our models would have been in the absence of genuine relationships.     

The response of different celery genotypes to infection by septoria apiicola

A rapid and useful method of disease assessment, based on a visual key, was developed for leaf spot of celery, caused by Septoria apiicola . Details were provided by an assessment of percentage infection, number and type of lesions per plant and number of pycnidia per lesion. The lesion response was graded from 0 (resistant with no lesions) to 3 (susceptible with grey lesions, leaf chlorosis and numerous pycnidia). Assessments were performed on leaves attached to the plants as well as on detached leaves incubated in sealed Petri dishes, after inoculation with a standard spore suspension. Tests were carried out on currently popular celery varieties, lines of wild celery, hybrids of celery × wild celery and celery × parsley. Lesion response 0 was found on some lines of wild celery, lovage and parsley; response 1 on lines of wild celery; response 2 on hybrid celery × wild celery and on the commercial celery Giant Red; and response 3 on all of the remaining celery varieties tested (Monarch, Fenlander, Tall Utah and Galaxy). Detached leaves from the individual genotypes showed responses in an order similar to that of the attached leaves but the onset of the response in detached leaves was always more rapid, with fewer lesions and pycnidia. Analysis of leaf chlorophyll content from the different sources was made to establish any relationship between chlorophyll and resistance but none was found.     

Epidemiological Characteristics of Angular Leaf Spot of Bean: A Systems Analysis

In this review, available knowledge on angular leaf spot (ALS) of bean, caused by Phaeoisariopsis griseola, is analysed and synthesised. This is done through a systems-analytical approach, and successive flowcharts of the system, in order to identify knowledge gaps and guide further research. Six connected sub-models of the ALS monocycle are used as a framework: lesion establishment, lesion extension, defoliation, sporulation, spore liberation, and spore deposition. Each of the sub-models enables the linking of processes to various effects of environmental (physical and host) factors. Disease-induced defoliation is one feature of the pathosystem, leading to a depletion of infectious tissues from the canopy, which are transferred to the ground. Consequences of defoliation may include: strong reductions of the amount of inoculum and of vacant sites in the canopy, limited maximum disease severity, and progressive accumulation of inoculum below the canopy, which may become important a later stage of disease epidemics. These elements are hypothesised to explain the typical behaviour of ALS epidemics in the field, especially late onset, high apparent rate of disease increase, and low level of terminal disease severity in the standing canopy. Epidemiological consequences of lesion expansion, sporulation, and survival of spores deposited onto the canopy are other knowledge gaps in this pathosystem.     

Foliar lifespan,phenology and seasonal dynamics of the invasive shrub Schinus terebinthifolia

Schinus terebinthifolia is a dioecious tree native to South America that has become an invasive weed in Florida, southern California, southern Arizona, Texas and Hawaii and has been naturalised in over 20 countries. Biological control is considered a viable long-term control option for S. terebinthifolia because release from natural enemies appears to be at least partly responsible for its success in Florida. We examined leaf phenology of S. terebinthifolia over a period of 15 months at five sites in central and southern Florida to provide information that may help in predicting the impacts of potential biocontrol agents for this weed. We documented leaf lifespan, the seasonality of leaf development and abscission and the survivorship of leaves that emerged during either spring, summer or autumn. Average leaf lifespan was >4.5 months at all sites, and leaf phenology followed the seasons closely. Although S. terebinthifolia possesses leaves throughout the year, leaf production was greatest from April to September, and most leaves were abscised in February and March. Spring- and summer-emerging leaves were also longer-lived than leaves produced during autumn. These results suggest that leaves of S. terebinthifolia would be most vulnerable to herbivory during the spring and summer months when newly growing leaf tissue is most plentiful. Biocontrol agents capable of damaging these tissues during spring/summer might be an effective means of controlling this invasive weed.