Due to economic and environmental constraints, alternatives to chemical management of Canada thistle (Cirsium arvense L.) are frequently sought, but adequate non-chemical suppression of this species remains elusive. Previous research has shown that Canada thistle biological control agents, such as the stem-mining weevil (Hadroplontus litura Fabricus), have limited efficacy, but integrating additional control tactics with biological control may enhance its effectiveness. Furthermore, soil resource levels can substantially influence impacts of and interactions between insect herbivores and plant competitors. We investigated effects of a biological control agent (H. litura, a stem-mining weevil) integrated with a native annual potential competitor (common sunflower, Helianthus annuus L.) on Canada thistle under two nitrogen, potassium and phosphorous regimes in outdoor microcosms during 2010 and 2011. Weevils caused modest reductions in Canada thistle height and flower number, but did not significantly affect two critical measures of Canada thistle reproductive capacity: final root biomass and number of side shoots. Exposure to common sunflower neighbors reduced Canada thistle height, final main shoot biomass, flower number, side shoot number, and final root biomass. Most measures of Canada thistle performance except root biomass declined with decreasing soil nutrient concentrations. Effects of weevil herbivory and common sunflower presence were additive rather than interactive. Our results suggest that integrating weevils with plant competition may place additional stress on Canada thistle compared to weevils alone, especially in situations where low soil nutrients inhibit Canada thistle performance.
Canada thistle (Cirsium arvense L.) is a problematic invasive weed in many croplands, rangelands, and recreational areas in cooler temperate regions of world, including the U.S. and Canada. This invasive weed thrives in disturbed or moist environments and can lower the quality of grazing lands, out-compete native plants, and negatively impact crop yield (McClay 2002; McLennan et al. 1991; O’Sullivan et al. 1982, 1985). Canada thistle is a clone forming perennial with a deep root system that can spread extensively (Donald 1994; McClay 2002) and give rise to adventitious shoots from root buds throughout the growing season (Tiley 2010). The widespread invasiveness of this weed is often attributed to these characteristics. Canada thistle’s persistence and vegetative spread has also been associated with the plants root carbohydrate reserves (Tworkoski 1992). In general, root carbohydrate levels are lowest in spring and early summer as a result of active shoot growth and begin to increase in late summer and fall in preparation for overwintering. Although environmental conditions principally influence Canada thistle root carbohydrate levels, they can also be impacted when insects feed upon foliar plant tissue (Hein and Wilson 2004).
Despite extensive research, managing Canada thistle remains challenging (Cripps et al. 2011; Tiley 2010). Numerous control tactics for suppression and management of Canada thistle have been investigated, including herbicides (reviewed by Donald 1990) and mechanical tactics such as frequent mowing (Lukashyk et al. 2008), hoeing (Graglia et al. 2006), and tillage (Pekrun and Wilhelm 2004); although these practices can be effective they are management intensive and often costly (Graglia et al. 2006). While individual management tactics such as herbicides and mechanical methods have been moderately successful (Liu et al. 2000), these tactics often don’t provide long-term results (Evans 1984; Travnicek et al. 2005), and therefore can be prohibitively expensive (Sciegienka et al. 2011; Tichich and Doll 2006). Overall, results from previous research suggest that integrated pest management (IPM) may provide longer-lasting Canada thistle suppression when compared to relying on a single chemical or mechanical control tactic (Ferrero-Serrano et al. 2008; Sciegienka et al. 2011).
Biological control is often an important component of IPM programs for invasive weed management. Biological control is an attractive option for many land managers because, if released agents successfully establish and persist, the expense and potential environmental concerns associated with repeated herbicide applications can be avoided (Liu et al. 2000). Although there are several other insects that are approved biological control agents (Winston et al. 2008), Hadroplontus (formerly Ceutorhynchus) litura Fabricius, a phytophagous stem-mining weevil (McClay 2002), is typically considered one of the most effective for Canada thistle in North America (Coombs et al. 2004). Adult H. litura overwinter in the soil and emerge in early spring in synchrony with Canada thistle emergence (Zwolfer and Harris 1966); in eastern North Dakota this typically occurs in late April or early May (E. Burns, unpublished data). Females lay eggs singly or in small groups (2-5) in round feeding cavities on the leaves of Canada thistle rosettes (Zwolfer and Harris 1966; E. Burns, unpublished data). Larvae emerge after 5 to 9 d and mine the mid-vein of the leaf, eventually tunneling into the stem (Zwolfer and Harris 1966). A single stem is often mined by several larvae (average of 3-6) and becomes discolored due to larval feeding and frass (Zwolfer and Harris 1966; Rees 1990; Burns 2012). Mature third instar larvae exit the plant and pupate in the soil (Zwolfer and Harris 1966), which is generally in late June to mid-July in eastern North Dakota when plants are at the pre-bud to bud stage (Burns 2012).
Stem-mining by H. litura larvae during the midsummer is thought to cause more damage to Canada thistle than the foliar chewing damage done by adult weevils in the spring and fall (Liu et al. 2000; Zwolfer and Harris 1966). Though larval mining stresses the plant, it is able to continue growth during and after attack because vascular bundles are not damaged by weevil feeding (Peschken and Wilkinson 1981). While H. litura herbivory does not kill shoots, larval feeding may lead to reduced overwinter survival (Rees 1990), reduction in early season root sugar (Peschken and Derby 1992) and starch content (Hein and Wilson 2004), and increased susceptibility to pathogens and/or adverse environmental conditions (Rees 1990). Overall, previous research results concerning H. litura efficacy are mixed and suggest that H. litura alone does not effectively control Canada thistle (Peschken and Derby 1992; Reed at al. 2006), but that combining additional management tactics might improve Canada thistle suppression (Bacher and Schwab 2000; Ferrero-Serrano et al. 2008; Friedli and Bacher 2001).
One potential option is seeding highly competitive native vegetation along with releasing biocontrol agents. Ferrero-Serrano et al. (2008) found that combining H. litura and a native cool season grass greatly reduced Canada thistle root biomass and hypothesized that H. litura had a positive indirect effect on the grass by decreasing the competitive ability of Canada thistle. Other plants, such as common sunflower (Helianthus annuus L.) may have even greater competitive abilities. Common sunflower is an annual dicot native to North America and found throughout the United States, Canada, and Mexico (Burke et al. 2002). It is similar to Canada thistle in several ways (i.e., it is fast growing and often thrives in disturbed areas) (Burke et al. 2002; Perry et al. 2009), which likely enhances its ability to compete against Canada thistle for sunlight and nutrients (especially nitrogen). As one example, Perry et al. (1990) reported that competition from common sunflower reduced Canada thistle above-ground biomass in greenhouse experiments.
Assuming that biological control and plant competitor impacts will be similar at all locations and under all conditions is naive (Shea et al. 2005). For instance, in North Dakota, anecdotal evidence suggests that H. litura releases have resulted in Canada thistle suppression in some geographical areas, but not in others (Gramig, personal observation). Environmental variability and differences among various Canada thistle biotypes in their response to H. litura are possible explanations for these observations. Successfully combining plant competition with biological control may require understanding how environmental variables, such as water or nutrient availability, mediate plant-plant and insect-plant interactions (Shea 2005). For example, a study that investigated interactive effects of soil nitrogen, plant competition, and various insect biological control agents found that a flower head weevil, Larinus minutus Gyllenhal, reduced spotted knapweed (Centaurea stobe L. subsp. micranthos [Gugler] Hayek) seed production most severely in low nitrogen soils and that reduced plant competition was associated with increased L. minutus numbers per flower (Knochel and Seastedt 2010). Conversely, soil nitrogen and plant competition did not significantly affect impacts of a root-feeding weevil, Cyphocleonus achates Fahr (Knochel and Seastedt 2010). These results demonstrate that soil resources regulate biological control impacts, but that generalizing about the impacts of soil resources on the impacts of insect herbivory or plant competition across species is problematic.
The goal of this study was to investigate the combined impact of H. litura and common sunflower on Canada thistle under different nitrogen, phosphorus and potassium (hereafter N, P and K) concentrations using field soil in outdoor microcosms. We focused on assessing impacts on plant parameters associated with vigor and reproductive potential, including root biomass, which is seldom investigated due to the difficulty of separating root tissue by species. We hypothesized that weevil attack and plant competition would reduce Canada thistle root biomass, in addition to reducing shoot height, shoot biomass, flower number, and number of side shoots. We further hypothesized that negative impacts of weevil attack and plant competition would be evident with low soil nutrients but not with high soil nutrients.
Experimental Design and Setting. Effects of H. litura, common sunflower presence, and soil nutrient content on Canada thistle growth and reproductive output were determined using outdoor microcosm experiments. During 2010 and 2011, experiments were conducted using a completely randomized design with four replications and three factorially combined treatments: 1) common sunflower present vs. absent, 2) H. litura weevil present vs. absent, and 3) high vs. low soil nutrient (N-P-K) content.
Experiments were conducted from June 2 to September 8, 2010 and June 4 to August 8, 2011 outdoors on the campus of North Dakota State University in Fargo, ND. Microcosms were established outdoors to take advantage of natural light and temperature fluctuations. Microcosms consisted of 18 kg of lightly compacted, finely sieved (3 mm [0.1 in] sieve) Ulen fine sandy loam (Sandy, mixed, frigid Aeric Calciaquolls) soil (hereafter field soil), placed in 19 L (5 gal) white plastic buckets with two drainage holes at the bottom and spaced 60 cm apart from adjacent microcosms.
Collection and Propagation of Plant Materials. In 2010, Canada thistle plants were propagated from vegetative root cuttings excavated from a small natural infestation on a south facing drainage ditch slope on the campus of North Dakota State University (Fargo, ND). Vegetative root cuttings were approximately 8 to10 cm in length and treated with 0.1% indole-3-butyric-acid powder (Bonide Products Inc., Oriskany, NY 13424) to promote rooting prior to planting. Root cuttings were grown in 8 cm wide by 9 cm deep plastic pots containing base soil. Plants were grown in the greenhouse (24 to 26 C [75 to 79 F], 16:8 light:dark h photoperiod) for 3 wk then transplanted on 6/1/10 and 6/2/11 into outdoor microcosms as small rosettes. Due to insufficient propagation in 2011, some Canada thistle plants were propagated as previously described while others were extracted as small rosettes directly from the field.
Common sunflower plants were grown from seed collected in the fall of 2009 and 2010 from wild plants on the campus of North Dakota State University in Fargo, ND. Approximately 5 seeds were planted 3 mm deep into 4.5 diam. x 4 cm plastic pots containing Sunshine Mix #1 (SunGo Horticulture Canada Ltd., Bellevue, WA 98008) on May 5 2010 and May 11 2011. After emergence (approximately 5 d after planting), sunflowers were transplanted into 8 diam. x 9 cm plastic pots containing field soil. Plants were grown in a greenhouse (24 to 26 C, 16:8 light:dark h photoperiod) until approximately the 4 leaf stage, when they were transplanted into microcosms on June 1 2012 and June 2 2011. When grown alone each Canada thistle plant was located in the center of the microcosm, and if grown with common sunflower each plant was 10 cm from the microcosm center. The 1:1 Canada thistle: common sunflower ratio is representative of a realistic ratio that might be observed in field settings (Burns, personal observation).
Hadroplontus Litura Treatment. Canada thistle and sunflower plants were allowed to establish for 1 d, after which they were subjected to H. litura weevils at a rate of 10 adults per microcosm. The average height of Canada thistle plants at this time was 7 cm, which is approximately the same height of plant that adult weevils have been observed to prefer in the field (Gramig, personal observation). Adult weevils field-collected on Canada thistle were purchased from a commercial source (Copeland Biological Inc., Bozeman, MT 59715) and shipped in containers along with Canada thistle foliage. Voucher specimens have been placed in the North Dakota State Insect Reference Collection (Fargo, ND). Before being placed in microcosms, weevils were stored in a refrigerator (4 C) with Canada thistle foliage for 23 d in 2010 and 12 d in 2011. Weevil gender was not assessed, but assuming equal sex ratios, the probability that all 10 insects would be the same sex is approximately 0.001 (Ferrero-Serrano et al. 2008). To prevent beetle migration, microcosms (including microcosms without weevils) were caged while adult weevils were present. Cages were constructed of 75 diam. x 150 cm nylon mesh sleeves draped over two overlapping 1.5 m (5 ft) metal wires embedded into the soil of each microcosm. Weevil adults and cages were removed 7 to 9 d after weevil release.
Soil Nutrient Treatment. The low soil nutrient treatment consisted of non-amended field soil with 60 kg ha-1 (53 lb ac-1N, 15 kg ha-1 P, and 132 kg ha-1 potassium, levels reflective of typical pastures (Burns unpublished data). The high soil nutrient treatment consisted of 142 kg ha-1 N, 55 kg ha-1 P, and 179 kg ha-1 K added to the field soil as ammonium nitrate (NH4NO3), potassium chloride (KCl), and triple superphosphate [Ca(H2PO4)2 • H2O]. Microcosms were watered periodically to field capacity, a water regime reflective of typical soil water conditions in many areas where Canada thistle is a problem (Gramig, personal observation).
Data Collection. Adult weevil damage to Canada thistle foliage was qualitatively assessed by visually inspecting plants after insect attack. At the end of the growing season, Canada thistle main stem shoot height, number of flowers (including developing buds), and number of side shoots were quantified. Microcosms were then moved to a greenhouse on 9/8/10 and 8/3/11(24 to 26 C, 16:8 light:dark h photoperiod) and allowed to desiccate until plants visibly wilted, approximately 10 to 14 d, to aid root dyeing (Murakami et al. 2006). At the time of harvest, 13 and 10 wk after weevil removal in 2010 and 2011 respectively, all Canada thistle plants were mature and had begun to senesce. Then, Canada thistle main stem shoots were cut 5 cm above the soil surface, split open using a scalpel, and assessed for weevil larval damage using a qualitative scale: 1 = undamaged (stem pith fleshy and 100% white/green), 2 = lightly damaged (stem pith mostly white with <25% stem damaged with thin, light brown mines), 3 = moderate damage (25-50% stem pith mined and discolored brown), and 4 = severe damage (>50% stem pith severely mined and blackened). Side shoots were harvested at the same time. Shoot material was placed in paper bags and dried at 70 C to a constant mass. After harvesting aboveground plant parts, we followed a root dyeing procedure developed by Murakami et al. (2006) to aid in separating roots by species. After separating by species, roots were dried to a constant mass at 70 C.
Statistical Analysis. For all plant response variable data, Levene’s test was performed to assess homogeneity of residual variance and normality was assessed via the Shapiro-Wilk test (Proc Univariate in SAS Version 9.2 (2008). Data for all response variables met the assumptions of ANOVA and were not transformed but were analyzed separately using Proc Mixed in SAS Version 9.2 (2008). Initial Canada thistle height was included as a covariate in all analyses. Weevil attack (W), common sunflower presence (CS), and soil nutrient level (SN) were modeled as fixed effects and year as a random effect. Significant differences among treatment means were determined using Tukey’s HSD post-hoc tests (95% confidence level).
Potential effects of common sunflower presence and soil nutrients on the frequency of larval weevil damage to Canada thistle plants in weevil addition treatments were analyzed using frequency tables and Pearson’s chi-square statistic (SYSTAT 2007). Differences in the intensity of larval damage among treatments receiving weevils were assessed using factorial ANOVA, with year, common sunflower presence, and soil nutrient level as the independent variables and larval damage rating as the explanatory variable.
The foliage of all Canada thistle plants in weevil addition treatments sustained similar amounts of heavy feeding damage by adult weevils (i.e., windowpaning damage to upper and lower leaf surfaces; Zwolfer and Harris 1966; Prischmann-Voldseth et al. 2012). The majority of Canada thistle plants in weevil addition treatments sustained some larval damage (main stem damaged = 72%, not damaged = 28%), and the incidence of larval weevil presence was statistically similar among treatments (PC x SN, P = 0.858; PC, P = 0.739; SN, P = 0.096). On average, experimental plants sustained relatively light levels of larval damage. Plants in a field setting experience variable levels of larval pressure (Rees 1990; Liu et al. 2000; Burns 2012); in ND a late-summer survey of 192 weevil infested Canada thistle stems at 46 sites where weevils were released revealed that 43% were lightly damaged (rating of 2) while 58% had moderate or severe damage ratings (unpublished data). Larval damage ratings from Canada thistle plants grown with low levels of soil nutrients (mean ± SE = 1.75 ± 0.21) were lower than plants grown with high levels of soil nutrients (2.44 ± 0.24; Year x PC x SN, P = 0.569; Year x SN, P = 0.191; PC x SN, P = 0.346; Year, P = 0.191; SN, P = 0.045), although larval damage was similar when common sunflower was present (2.00 ± 0.24) or not (2.19 ± 0.25; Year x PC, P = 0.569; PC, P = 0.569). The development and performance of herbivorous insects is often linked to plant quality, and endophagous insects (e.g. stem-miners, gall makers) often do better on vigorous plants growing in resource rich environments (Price 1991, 1997; De Bruyn et al. 2002). Additionally, second generation adult weevils were not observed at the end of the experiment, so late season adult feeding did not impact our results.
Canada Thistle Size.
Canada Thistle Height. Canada thistle main stem height was affected by weevil herbivory, common sunflower presence, and soil nutrients, but interactions among treatments were absent (Table 1). Canada thistle plants exposed to weevils produced main stems that were 15% shorter than plants not exposed to weevils (Figure1A). This is a slight height difference that was not accompanied by a corresponding decline in shoot biomass (Figure 2A). A field study that quantified Canada thistle height as affected by several insect biological control agents including H. litura determined that plants were often, but not always, shorter at the control site than at release sites (Liu et al. 2000). The authors concluded that environmental differences among sampling times may have been responsible for these inconsistent results. They also speculated that insect damage may have stimulated an elongation response. Another study found that stem mining by H. litura did not affect Canada thistle stem height (Peschken and Wilkinson 1981). However, both of these studies were conducted in the field, where differences in soil nutrients or other herbivorous insects could have influenced the results.
Canada thistle plants grown alongside common sunflower produced main stem shoots that were 28% shorter than shoots produced by plants grown without common sunflower neighbors (Figure 1B). This reduction in Canada thistle plant height associated with competition is not mirrored by other studies that measured Canada thistle height as affected by plant competition and may perhaps be attributed to functional differences in the plant competitors used in the various studies. Bacher and Schwab (2000) used an herbaceous seed mix and Cripps et al. (2010) chose a mixture of perennial ryegrass (Lolium perenne L.) and white clover (Trifolium repens L.). Both studies reported no difference in height between Canada thistle plants grown with and without plant competitors (Bacher and Schwab 2000; Cripps et al. 2010).
Common sunflower has a fast growth rate, which gives the plant the ability to quickly shade plant neighbors, thus reducing the neighboring plant’s growth (Perry et al. 2009). Previous research has reported negative impacts of shading on Canada thistle growth (Evans 1984); these results may help to explain the above results. Although common sunflower presence had a negative impact on Canada thistle height in our study, competition can also lead to height increase in response to shading (Aarssen 1995; Jaremo et al. 1996). Common sunflower presence may have exerted competition for light above ground and competition for soil resources below ground. The reduction of soil nutrients imposed by common sunflower competition could be primarily responsible for the reduction in Canada thistle height.
Canada thistle plants grown in low nutrient soil produced main stem shoots that were 30% shorter than shoot produced by plants growing in high nutrient soil (Figure 1C). Most previous results regarding Canada thistle growth responses to nutrients are from studies that focused on only the effect of nitrogen. One previous study (McIntyre and Hunter 1975) found that Canada thistle shoot length was reduced by 53% when plants were grown with 31.5 kg ha-1 N compared to plants grown with 315 kg ha-1 N (the N levels in this study were 142 and 60 kg ha-1, for comparison).
Canada Thistle Main Stem Shoot Biomass. Our experiment did not detect an impact of H. litura weevil presence on Canada thistle main stem shoot dry biomass (Table 1, Figure 2A). These findings are similar to those reported by Collier et al. (2007) and Ferrero-Serrano et al. (2008), who both reported no effect of weevil attack on Canada thistle shoot biomass. Conversely, Sciegienka et al. (2011) reported that H. litura herbivory negatively impacted Canada thistle shoot biomass in greenhouse experiments. The differences in reported impacts of H. litura on Canada thistle shoot biomass could be attributed to genetic differences among the weevils, differences in attack severity, and also impacts of differential environmental conditions on biological control agent performance (Menalled et al. 2004). In our study, while adult feeding damage was heavy on all rosettes, larval damage was light overall, and this may be a potential reason why weevil presence did not affect main stem shoot biomass.
Canada thistle plants grown with common sunflower neighbors or in low soil nutrients produced less main stem shoot biomass (64 and 74 % less biomass, respectively) than Canada thistle plants grown in high soil nutrients or without common sunflowers (Table 1; Figure 3). Perry et al. (2009) found that common sunflower competition resulted in reduced Canada thistle shoot biomass under controlled greenhouse conditions. Friedli and Bacher (2001), who grew Canada thistle in competition with perennial ryegrass, Italian ryegrass (Lolium perenne L. ssp. multiflorum (Lam.) Husnot), and orchardgrass (Dactylis glomerata L.) also found that competition reduced shoot biomass. In contrast, Canada thistle biomass was not affected when it was grown with alkali sacaton (Sporobolus airoides (Torr.) Torr.) and needle and thread grass (Hesperostipa comata (Trin. & Rupr.) Barkworth) (Ferrero-Serrano et al. 2008). Differences among studies may perhaps be attributed to the physiological and morphological differences in the specific plant competitors used in experiments or to experimental differences such as pot size, water or nutrient levels, and planting density. Furthermore, our study was performed outdoors and subject to variable weather conditions whereas the previous studies were conducted in highly controlled greenhouse environments. The natural weather fluctuations in our study may have played a large role in the results. Additionally, Ferrero-Serrano et al. (2008) and Sciegienka et al. (2011) studies were conducted in 7.6 L plastic containers whereas in our study, microcosms were 19 L plastic containers. Experiments have demonstrated that plant growth can be negatively affected by pot size and that often when plants are grown in pots that are too small they may become root bound and a general reduction in growth occurs (Townend and Dickinson 1995) and therefore their treatments may have been more detrimental due to potentially stressed root bound Canada thistle plants.
Canada Thistle Reproductive Potential.
Canada Thistle Flower Number. Weevil presence, common sunflower presence, and soil nutrients each influenced Canada thistle flower number, but no interaction terms were significant (Table 1). Canada thistle plants that were exposed to H. litura weevils produced 40% fewer flowers than plant that were not exposed to weevils (Figure 3A). Furthermore, flower number: main stem shoot biomass ratios did not differ between weevil treatments (P=0.115, data not shown), demonstrating that this effect resulted from more than a simple reduction of biomass. Our study is the first (to our knowledge) to document a negative impact of H. litura presence on Canada thistle flower number, but we did not quantify seeds per flower. However, one previous study found that exposure to H. litura weevils and seed head parasites did not reduce the number of seeds per seed head (Larson et al. 2005). Also, Canada thistle is a dioecious plant and male Canada thistle shoots have been shown to produce fewer flowers than female shoots (Becker et al. 2008). We did not identify the gender of individual Canada thistle plants, so this could be a source of error in our study.
Canada thistle plants grown with common sunflower neighbors produced 65% fewer flowers than Canada thistle plants grown alone (Figure 3B). Plant competition also negatively impacted Canada thistle flower production in a previous study in which a mixture of three grass species (perennial ryegrass, Italian ryegrass, and orchardgrass) reduced Canada thistle flower production by 81% compared to Canada thistle plants grown without grass competition (Friedli and Bacher 2001). In our study, flower number:main stem shoot biomass ratios did not differ between common sunflower treatments (data not shown), indicating that the decrease in flower number associated with common sunflower presence scaled with biomass reduction. This was likely caused by a reduction in soil nutrients available to Canada thistle plants.
Canada thistle plants grown in low soil nutrients produced 68% fewer flowers than Canada thistle plants grown in high soil nutrients. A previous study (Loehle 1987), along with our study, demonstrated that increased soil nutrients are associated with production of more reproductive structures by perennial plants. A model constructed by Loehle (1987), which evaluated energy partitioning in clonal plants, predicted that increased soil nutrients would be associated with a decrease in the cost of producing sexual reproductive structures, which ultimately leads to increased seed production. Our results, which showed that Canada thistle plants grown in stressful low soil nutrient environments produced fewer flowers than Canada thistle plants grown in high soil nutrients, support this theoretical model. Also, the ratio of flowers: main stem biomass was 45% greater for Canada thistle plants grown in high soil nutrients (P=0.006, data not shown). This demonstrates that the increase in flower number in high soil nutrients was not a simple function of increasing plant biomass.
Canada Thistle Side Shoot Number. Side shoot production is important because it is indicative of vegetative reproductive capacity, which is the primary means by which Canada thistle spreads (Donald 1994). We failed to detect any impact of H. litura weevil presence on Canada thistle side shoot number (Table 1, Figure 4A). In a microcosm study performed under controlled greenhouse settings, Sciegienka et al. (2011) reported that Canada thistle plants exposed to H. litura produced on average 29% fewer side shoots than Canada thistle plants without weevil exposure. In our study not every Canada thistle plant that received the H. litura treatment sustained visible larval stem mining damage. Sciegienka et al. (2011) did not report the extent of H. litura larval mining; if the damage was more extensive than in our study, this may have been another source of variation between the two studies that could have played a large role in the discrepancy between results. Differences could also be related to the environmental conditions in which the two experiments were conducted (greenhouse versus outdoor).
Canada thistle side shoot number was affected by both plant competition and soil nutrient level (Table 1). Canada thistle plants grown with common sunflower plants produced 57% fewer side shoots than Canada thistle plants grown without common sunflower plants (Figure 4B). These results are not consistent with results reported by Ferrero-Serrano et al. (2008), who reported plant competition by alkali sacaton and needle and thread grass grown together and alone with Canada thistle in microcosm experiments had no impact on the number of side shoots produced by Canada thistle throughout the experiment. We hypothesize that differences in competitor functional type (i.e., perennial grass vs. annual forb) may be the basis for these differential results.
Canada thistle plants grown in low soil nutrients produced 39% fewer side shoot than plants grown in high soil nutrients (Figure 4C). The negative impact of low soil nutrients on Canada thistle side shoot production is similar to findings by McIntyre and Hunter (1975), who reported a 68% decrease in side shoot production by Canada thistle plants grown in soil treated with 21 ppm nitrogen compared to Canada thistle plants grown in soil treated with 210 ppm nitrogen.
Canada thistle Final Root Biomass. Canada thistle root biomass was not affected by either weevil presence or soil nutrients (Table 1, Figures 5A and 5C). The lack of weevil impact on root biomass is consistent with previous research showing that H. litura herbivory failed to reduce Canada thistle root biomass in two of three experimental runs (Collier et al. 2007). However, Ferrero-Serrano et al. (2008) and Sciegienka et al. (2011) both reported a negative impact of H. litura on Canada thistle root biomass. These two studies found that H. litura attack decreased Canada thistle root biomass by 81 and 18%, respectively. Variables that could have caused differential responses include the size of the pots or microcosms, the initial size of the Canada thistle plants, the intensity or severity of weevil attack, soil resource status, and climatic variables.
Root biomass is critically important for Canada thistle spread and persistence, but common sunflower plant presence was the only treatment that negatively affected Canada thistle root biomass (Table 1, Figure 5B). Common sunflower presence resulted in an 83% reduction in root dry biomass. Previous studies (Ferrero-Serrano 2008; Friedli and Bacher 2001) have reported reductions in Canada thistle root biomass resulting from intraspecific competition with grass competitors. Surprisingly, soil nutrients did not affect Canada thistle root biomass (Table 1, Figure 5C), in contrast to previous results that showed when Canada thistle infestations were treated with 100 kg ha-1 nitrogen fertilizer, root biomass excavated from a 1 and 2 yr old stand from the top 20 cm of soil was approximately three times greater than the root mass from unfertilized plots (Nadeau and Vanden Born 1990). These results are somewhat perplexing because the mechanism for negative impacts on root biomass resulting from competition would presumably be competition for soil nutrients. But since soil nutrients did not affect root biomass, perhaps the mechanism for changes in root biomass caused by common sunflower presence can be attributed to changes in root:shoot ratios caused by shading. Also, root:shoot ratios differed between Canada thistle plants grown with common sunflower and those grown without (P=0.001, data not shown).
Summary and Management Implications.
Though interactive effects among H. litura herbivory, soil nutrients, and common sunflower presence were absent, these treatments did have substantial individual and additive effects on many measures of Canada thistle growth and reproductive output. Our results indicate that both H. litura weevil attack and interspecific plant competition can reduce Canada thistle shoot height, which is a proxy for size and thus competitive ability and general robustness. Therefore, integrating interspecific competition with insect biological control could place additional stress or pressure on Canada thistle populations beyond that supplied by biocontrol alone. But our results also highlight the importance of selecting a plant competitor with specific functional characteristics, since other studies have demonstrated no impact of intraspecific competition on Canada thistle height. Common sunflower proved to be a good competitor against Canada thistle, but this species is often also considered undesirable by land managers. Often, plant species that compete strongly enough to inhibit invasive perennials will also inhibit desirable native vegetation (Perry et al. 2009). Seeding of a fast-growing competitive annual forb such as common sunflower could potentially be the first step in a restoration process which would be followed by restoration of more desirable perennial native vegetation.
New Canada thistle infestations occur via wind dispersed seed and Canada thistle seed also remains viable in the soil for long periods of time (Piper and Andres 1995; Tiley 2010); therefore, decreasing seed inputs into the soil seed bank would be advantageous for future restoration efforts. Our research demonstrated the ability of H. litura and common sunflower presence to negatively impact Canada thistle flower production. Although these results are encouraging, we did not quantify the number of viable achenes produced by each flower head nor did we discriminate among male vs. female shoots, so our results should be considered preliminary.
Difficulties controlling Canada thistle are often attributed to its deep, extensive, and regenerative root system, which facilitates invasiveness, persistence, and tolerance to control measures (Lukashyk et al. 2008; Tiley 2010). However, similar previous studies investigating the impacts of plant competition on Canada thistle did not quantify root biomass impacts (Edwards et al. 2000; Perry et al. 2009). Our research demonstrated the utility of using common sunflower as a plant competitor against Canada thistle, because competition by common sunflower negatively impacted multiple morphological characteristics of Canada thistle, most notably a reduction in root biomass. Chemical control measures often fail to translocate sufficiently (Armel et al. 2005; Petersen and Swisher 1985) to the root system of Canada thistle to cause detrimental damage to the entire network of clonal plants. Control measures that could target and negatively impact the prolific Canada thistle root system would therefore be beneficial.
Canada thistle patches spread and creep into new territories via adventitious shoot production throughout the growing season, making the patches larger and more difficult to manage (Tiley 2010). In our study, low soil nutrients and plant competition reduced side shoot numbers. Planting common sunflower could potentially slow down the rate of expansion of Canada thistle patches, especially in areas where soil nitrogen level are relatively low or in areas where soil nitrogen could be reduced via filter strips or other approaches that mitigate nitrogen pollution (Morghan and Seastedt 1999; Paschke et al. 2000; Vasquez et al. 2008).
The success of biocontrol agents depends not only on the control agent’s ability to damage individual plants, but also on the ecology of both the agent and the weed species in question (McFadyen 1999). Our results suggest that H. litura weevils alone (at least at the level of weevil pressure present in our study) will have minimal impacts on the spread and persistence of Canada thistle, because weevil herbivory does not appear to reduce root biomass, which is the primary means by which this weed spreads and persists. Most practitioners acknowledge that single biological control agents rarely are sufficient to effectively manage an invasive weed species (DiTomaso 2000). Clearly, no single biocontrol measure appears to be a silver bullet for managing Canada thistle. However, results of our research indicate that combining plant competition with biological control could be a potentially effective strategy for reducing population densities of this troublesome weed, especially in areas where low soil nutrients somewhat limit Canada thistle growth and proliferation.
Educational & Outreach Activities
Peer Reviewed Articles:
Prischmann-Voldseth, D., G. Gramig, E. Burns. 2012. Home on the range: establishment of a Canada thistle biocontrol agent. Rangelands: October 2012, Vol. 34, No. 5, pp. 2-5.
Burns, E., Prischmann-Voldseth, D. and G. Gramig. 2012. Integrated management of Canada thistle (Cirsium arvense) with insect herbivory and plant competition under variable soil nutrients. Submitted to Invasive Plant Science and Management. (accepted, in revision)
Conference Proceedings, Abstracts:
Burns, E. E., G. G. Gramig, and D. A. Prischmann-Voldseth. 2011. Effects of native cover crop, introduced weevil herbivory, and soil nutrients on Canada thistle (Cirsium arvense L.) 64th Annual Meeting, Western Weed Science Society of America, Mar 7-10, Spokane, WA. (12).
Role: Substantial input on research conception, execution, data analysis, and writing.
Burns, E. E., G. G. Gramig, and D. A. Prischmann-Voldseth. 2012. Integrating weevil herbivory, a native cover crop, and soil nutrients for Canada thistle (Cirsium arvense L.) control. 52nd Annual Meeting, Weed Science Society of America, February 6-9, Waikoloa, HI. (292).
Talks and Presentations:
Burns, E. 2012. Integrating Weevil Herbivory, A Native Cover Crop, and Soil Nutrients for Canada Thistle Control. Wild World of Weeds Workshop. January 24, Fargo, ND.
Gramig, G., E. Burns, and D. Prischmann-Voldseth. 2013. Canada Thistle Research Update. North Dakota Agriculture Commissioner’s Weed Forum. January 8, Mandan, ND.
Results from this research have been presented publicly several times, to both scientific and stakeholder audiences. Discussion generated from these presentations suggested that stakeholders have a moderate to high level of interest in using biological and other integrated management approaches to control Canada thistle. Many stakeholders (69% according to our survey) already use biological control to address invasive weed issues. Biological control is attractive because it is self-sustaining, inexpensive, and easy to implement. Many stakeholders in North Dakota have a favorable impression of biological control because this approach has been very successful in managing leafy spurge. However, stakeholders seemed to have mixed feelings about the success of Canada thistle biological control efforts. Some stakeholders are convinced that the various biological control agents, which include the H. litura weevil, are effective in reducing Canada thistle stem densities. However, just as many, if not more, stakeholders feel that Canada thistle biological control agents are not very effective. Our research results suggest that the H. litura weevil will likely not be a highly effective biological control agent. This is because the weevil doesn’t damage Canada thistle roots, which are the primary means by which the weed spreads. However, integrating competition with biological control could provide increased Canada thistle suppression compared to using weevils alone, but integrated management requires a high level of management skill. Based on our survey and informal discussions, most stakeholders thought that integrated management of Canada thistle is a good idea in theory, but in practice would not be successful enough to warrant the additional management expertise required to implement such an approach. Before we conducted this research, the North Dakota Department of Agriculture was heavily invested in promoting biological control of Canada thistle. Our results convinced that agency that their limited resources might be better directed at another weed problem. The primary outcome of this research was to demonstrate to stakeholders the potential, but also the limitations, of using biological control for managing Canada thistle.
No economic analysis was planned as part of this project.
Results from this study were presented to farmer shareholders at the North Dakota Commissioner’s Weed Forum, held in Mandan, ND on January 8th, 2013. This SARE project was to include a survey to gauge stakeholder response to the research. The survey was designed to assess extent of involvement of the stakeholder in weed management decisions,level of concern about various weed problems, and interest in applying the presented research results. The results of the survey are summarized below:
Of the 64 respondents, a majority (>95%) reported that they are personally responsible for making weed management decisions. 14% of respondents manage 0 to 1,000 acres; 31% of respondents manage 1,000 to 10,000 acres; 14% of respondents manage 10,000 to 100,000 acres; and 36% of respondents manage more than 100,000 acres.
Extent and Type of Weed Problems Among Respondents
Among all respondents, 6% reported 0 to 100 acres with a weed problem; 23% reported 100 to 1,000 acres with a weed problem; 20% reported 1,000 to 10,000 acres with a weed problem; and 38% reported greater than 10,000 acres with a weed problem.
Among all respondents, 91% reported a problem with Canada thistle, 73% reported a problem with leafy spurge, and 52% reported a problem with absinth wormwood.
Current Management Practices
Among all respondents, herbicides were the most popular way to manage weeds; 95% of respondents use herbicides. Tillage, grazing, mowing, and burning are used by 25, 36, 15, and 50% of respondents, respectively. Biological control is the second most popular method for managing weed problems; 69% of respondents use this method. Only 9% of respondents plant competitive species to manage weeds. Site specific management techniques are used by 31% of respondents.
Opinions About Alternative Practices to Manage Canada Thistle
On average, the level of interest in using alternatives methods (biological control, competition, nutrient management) to manage Canada thistle was in between “high” and “neutral.” Many respondents felt that alternative methods would not be effective and that their current practices were sufficient. Fewer respondents felt that alternative methods would be too time consuming or expensive. One respondent claimed that research should focus on other more troublesome species, since Canada thistle is naturalized in most places and is “easily managed” in tillable acres. Another respondent reported that in spite of having H. litura and U. carduii present, no Canada thistle control has been observed.
Areas needing additional study
Some stakeholders reported thinking that biological control of Canada thistle is successful, while others took the opposite view. One lingering question is, are there some circumstances under which biological control of Canada thistle is effective? A deeper understanding of the many biotic and abiotic factors that might interrelate to effectively suppress Canada thistle would be helpful. Another issue in managing invasive weeds is distinguishing actual impact from perceived impact. For example, purple loosestrife is one invasive weed that has fewer real ecological consequences than perceived consequences. This is likely because the weed has very showy purple flowers that are quite noticeable, which causes people to overestimate the extent of the invasion. Common milkweed is another weedy species that, because of its large size and showy flower, is often perceived to be more of a problem than it is in reality. One very interesting stakeholder comment was that Canada thistle is now naturalized and as such doesn’t present an enormous ecological problem, compared to other invasive weeds of concern. Canada thistle has relatively showy purple blooms and is a spiny plant, a characteristic that makes it seem unpleasant to humans. However, we have noticed that Canada thistle seldom dominates a plant community. Also the flowers of Canada thistle are highly prized by important pollinators and the weed can also be successfully grazed by sheep and cattle. Perhaps the perception of the harm caused by this weed is greater than the reality of impact? Assessing the true ecological impact of Canada thistle could be an important contribution to the science of invasive weed management. In an era when resources are scarce, we need to focus on addressing problems with substantial negative impacts. Assessing the real impacts of Canada thistle invasions would thus help inform rational invasive weed strategies.