Novel weapons and invasion: biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate (±)-catechin

Recent studies suggest that the invasive success of Centaurea maculosa may be related to its stronger allelopathic effects on native North American species than on related European species, one component of the “novel weapons” hypothesis. Other research indicates that C. maculosa plants from the invasive range in North America have evolved to be larger and better competitors than conspecifics from the native range in Europe, a component of the “evolution of increased competitive ability” hypothesis. These hypotheses are not mutually exclusive, but this evidence sets the stage for comparing the relative importance of evolved competitive ability to inherent competitive traits. In a competition experiment with a large number of C. maculosa populations, we found no difference in the competitive effects of C. maculosa plants from North America and Europe on other species. However, both North American and European C. maculosa were much better competitors against plants native to North America than congeners native to Romania, collected in areas where C. maculosa is also native. These results are consistent with the novel weapons hypothesis. But, in a second experiment using just one population from North America and Europe, and where North American and European species were collected from a broader range of sites, competitive interactions were weaker overall, and the competitive effects of C. maculosa were slightly stronger against European species than against North American species. Also consistent with the novel weapons hypothesis, (±)-catechin had stronger effects on native North American species than on native European species in two experiments. Our results suggest that the regional composition of the plant communities being invaded by C. maculosa may be more important for invasive success than the evolution of increased size and competitive ability. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Effects of the Invasive Forb <Emphasis Type="Italic">Centaurea maculosa</Emphasis> on grassland Carbon and Nitrogen Pools in Montana,USA

Invasions by exotic forbs are changing large areas of North American grasslands, but their biogeochemical impacts are not well characterized. Additionally, although many invasive plants may alter biogeochemistry, an invasive species effects have rarely been evaluated across physically diverse sites. We sampled nine sites containing the perennial Eurasian forb Centaurea maculosa to determine if this invasive species alters soil C and N pools in native grasslands in Montana, USA. We sampled surface soil in adjacent microsites with C. maculosa and native grasses and analyzed soil C and N pools with slow to rapid turnover. None of the pools evaluated in the laboratory showed significant differences between C. maculosa and grass microsites when analyzed across all sites. Some differences were found at individual sites, but they were infrequent and inconsistent: Four sites had no differences, four had differences in one or two pools with intermediate (particulate organic matter C or N) or rapid turnover rates (potentially mineralizable N), and just one site had differences encompassing pools with rapid, intermediate, and slow (total C and N, silt-and-clay-associated N) turnover rates. Where they differed, pools were usually smaller under C. maculosa plants than under native grasses, but the opposite was found at one site. In situ N availability, estimated using ion exchange resins, was significantly lower under C. maculosa than under grasses at one of three sites sampled. Results indicate that C. maculosa may sometimes reduce soil C and N pools, including those related to N availability, but they argue against generalizing about the impacts of C. maculosa in grasslands.     

Shoot herbivory on the invasive plant, Centaurea maculosa, does not reduce its competitive effects on conspecifics and natives

Herbivory can have negative, positive, or no effect on plants. However, insect biological control assumes that herbivory will negatively affect the weed and release natives from competition. Centaurea maculosa, an invader in North America, is tolerant to herbivory, and under some conditions, herbivory may increase its competitive effects on natives. Therefore, we investigated two hypotheses: 1) herbivory stimulates compensatory growth by C. maculosa, which increases its competitive effects, and 2) herbivory stimulates the allelopathic effect of C. maculosa. In the greenhouse, Trichoplusia ni shoot herbivory reduced C. maculosa biomass when shoot damage exceeded 40% of the total original leaf area. Conspecific neighbors had no effect on C. maculosa biomass, and the presence of the natives Festuca idahoensis and F. scabrella had a positive effect on C. maculosa. Neighbors did not alter the effects of shoot herbivory. More importantly, even intense shoot herbivory on C. maculosa did not benefit neighboring plants. In a field experiment, clipping 50% of C. maculosa aboveground biomass in the early summer and again in the late summer reduced final biomass by 40% at the end of the season; however, this clipping did not affect total biomass production or reproductive output. Festuca idahoensis neighbors did not increase the effects of clipping, and aboveground damage to C. maculosa did not release F. idahoensis from competition. In the greenhouse we used activated carbon to adsorb allelochemicals, which reduced the competitive effects of C. maculosa on F. idahoensis but not on F. scabrella or other C. maculosa. However, we found no increase in the allelopathic effects of C. maculosa after shoot herbivory. In summary, our results correspond with others indicating that exceptionally high intensities of herbivory are required to suppress C. maculosa growth and reproduction; however, even intense herbivory on C. maculosa does not insure that native bunchgrasses will benefit.     

History of exposure to herbivores increases the compensatory ability of an invasive plant

Release from natural enemies is frequently cited as an important factor contributing to plant invasions. But such effects are likely to be temporary—native herbivores can form new plant-herbivore associations and co-evolved insects might reach the new range. While the potential effects of the initial enemy release have been well studied, the consequences of any resumption of herbivory are poorly understood. Alternanthera philoxeroides is one of the most widespread invasive plants in China and is attacked both by a specialist herbivore introduced from the native range, Agasicles hygrophila, and a native beetle Cassida piperata Hope which has formed a new association. However, these insects are not found throughout the invaded range. To test the effect of the history of population exposure to herbivory on compensatory ability, plants were cultured from 14 populations around China that differed in whether A. hygrophila or C. piperata were present. Treatment plants were exposed to herbivory by A. hygrophila for a week until 50% of the leaf area was defoliated, then grown for 80 days. Plants from populations with prior exposure to herbivory (of any kind) accumulated more root mass than populations without prior exposure, indicating that prior exposure to insects can stimulate plant compensation to herbivory. We would recommend that potential changes in plant tolerance in response to prior exposure to herbivory are considered in invasive plant management plans that employ bio-control agents.     

The effect of a rosette-crown fly, Botanophila turcica, on growth,biomass allocation and reproduction of the thistle Carthamus lanatus

Plant growth and reproductive output of the winter annual invasive thistle, Carthamus lanatus was characterised in relation to plant size in three native populations in southern France. The effects of the rosette-crown feeding fly Botanophila turcica on these plant characteristics were assessed by comparing unattacked with naturally attacked plants at each site and by a field experiment. Indirect effects of B. turcica on plant seed production were also compared with direct seed loss caused by a guild of capitulum-feeding insects that incidentally attacked the marked plants at these sites. C. lanatus showed no size or weight requirement for flowering, but larger flowering plants produced less total receptacle surface and less seed production (female reproductive potential) in proportion to plant weight than smaller flowering plants. B. turcica did not select hosts on the basis of size or density. B. turcica reduced plant relative growth rate (RGR) in all situations, but attacked plants compensated fully at two of three sites as attack failed to halt rosette growth. Attacked plants suffered 12 % mortality, and 71 % lower seed production than unattacked plants at the site with the lowest RGR. This corresponded to 9 % lower seed production for the whole thistle population compared to 8.6–19.5 % direct seed loss to capitulum insects across all sites.     

Invasive plant architecture alters trophic interactions by changing predator abundance and behavior

As primary producers, plants are known to influence higher trophic interactions by initiating food chains. However, as architects, plants may bypass consumers to directly affect predators with important but underappreciated trophic ramifications. Invasion of western North American grasslands by the perennial forb, spotted knapweed (Centaurea maculosa), has fundamentally altered the architecture of native grassland vegetation. Here, I use long-term monitoring, observational studies, and field experiments to document how changes in vegetation architecture have affected native web spider populations and predation rates. Native spiders that use vegetation as web substrates were collectively 38 times more abundant in C. maculosa-invaded grasslands than in uninvaded grasslands. This increase in spider abundance was accompanied by a large shift in web spider community structure, driven primarily by the strong response of Dictyna spiders to C. maculosa invasion. Dictyna densities were 46–74 times higher in C. maculosa-invaded than native grasslands, a pattern that persisted over 6 years of monitoring. C. maculosa also altered Dictyna web building behavior and foraging success. Dictyna webs on C. maculosa were 2.9–4.0 times larger and generated 2.0–2.3 times higher total prey captures than webs on Achillea millefolium, their primary native substrate. Dictyna webs on C. maculosa also captured 4.2 times more large prey items, which are crucial for reproduction. As a result, Dictyna were nearly twice as likely to reproduce on C. maculosa substrates compared to native substrates. The overall outcome of C. maculosa invasion and its transformative effects on vegetation architecture on Dictyna density and web building behavior were to increase Dictyna predation on invertebrate prey ≥89 fold. These results indicate that invasive plants that change the architecture of native vegetation can substantially impact native food webs via nontraditional plant → predator → consumer linkages.     

Neighboring plant influences on arbuscular mycorrhizal fungal community composition as assessed by T-RFLP analysis

Controls on root colonization by arbuscular mycorrhizal fungi (AMF) include host nutrient status, identity of symbionts and soil physico-chemical properties. Here we show, in the field, that the subset of the AMF community colonizing the roots of a common grass species, Dactylis glomerata, was strongly controlled by neighboring roots of a different plant species, Centaurea maculosa, an invasive forb, thus adding a biological spatial component to controls on root colonization. Using an AMF-specific, 18s rDNA-based terminal restriction fragment length polymorphism (T-RFLP) analysis method, significant differences were found between AMF community fingerprints of samples derived from roots of grasses with (G_Cm) and without (G₀) neighboring C. maculosa. There were also significant differences between samples derived from C. maculosa roots (C_mac) and both G_Cm and G₀ roots. Sample ordination indicated three generally distinct groups consisting of C_mac, G_Cm and G₀, with G_Cm samples being of intermediate distance between G₀and C_mac. Our results indicate that, with the presence of C. maculosa, AMF communities of D. glomerata shift to reflect community composition associated with C. maculosa roots. These results highlight the importance of complex spatial distributions of AMF communities at the scale of a root system. An additional dimension to our study is that C. maculosa is an aggressively invasive plant in the intermountain West. Viewed in this light, these results suggest that pervasive influences of this plant on AMF communities, specifically in roots of its competitors, may represent a mechanism contributing to its invasive success. However, further work is clearly required to determine the extent to which AMF genotypic alteration by neighboring plants influences competitive relationships.     

Plant neighbor identity influences plant biochemistry and physiology related to defense

Background  

Chemical and biological processes dictate an individual organism's ability to recognize and respond to other organisms. A small but growing body of evidence suggests that plants may be capable of recognizing and responding to neighboring plants in a species specific fashion. Here we tested whether or not individuals of the invasive exotic weed, Centaurea maculosa, would modulate their defensive strategy in response to different plant neighbors.     

Exotic weevil invasion increases floral herbivore community density,function, and impact on a native plant

Consumer communities are being re‐arranged through unprecedented rates of human‐mediated invasions and extinctions. Such changes in consumer diversity potentially alter community function and impact on resource populations. Although insect herbivore invasions are increasingly common, the influence of such species additions on native resident herbivore guilds, along with their individual and combined effects on native plant resources, are rarely investigated. Here, we used site‐to‐site and plant‐to‐plant variation in herbivore composition to examine how the addition of an invasive exotic weevil, Rhinocyllus conicus, combines with a guild of native floral herbivores (tephritid flies, pyralid moths) to influence two key components of herbivore community function – aggregate herbivore densities and cumulative levels of seed destruction – on a native thistle, Cirsium canescens. Invasion of a site by R. conicus more than doubled aggregate herbivore density, resulting in increased levels of seed destruction and a halving of seed production by the native thistle. Further, herbivore function was significantly higher on individual plants attacked by R. conicus, compared to plants attacked only by native herbivores. Insect densities and levels of seed destruction on plants attacked by multiple herbivore taxa never exceeded those observed for plants attacked by R. conicus alone, suggesting that increases in herbivore community function with invasion resulted from the inclusion of a functionally dominant insect rather than any complementarity effects. Some evidence for interference between insects emerged, with a trend towards reduced moth and weevil densities in two and three taxon mixtures compared with plants attacked by each taxon alone. However, density compensation was limited so that, overall, the addition of a novel herbivore to the floral guild was associated with a significant increase in herbivore community function and impact on seed production. The results suggest that invasion of a functionally dominant herbivore into an unsaturated recipient community can augment function within a resource guild.     

Climate warming increases biological control agent impact on a non‐target species

Climate change may shift interactions of invasive plants, herbivorous insects and native plants, potentially affecting biological control efficacy and non‐target effects on native species. Here, we show how climate warming affects impacts of a multivoltine introduced biocontrol beetle on the non‐target native plant Alternanthera sessilis in China. In field surveys across a latitudinal gradient covering their full distributions, we found beetle damage on A. sessilis increased with rising temperature and plant life history changed from perennial to annual. Experiments showed that elevated temperature changed plant life history and increased insect overwintering, damage and impacts on seedling recruitment. These results suggest that warming can shift phenologies, increase non‐target effect magnitude and increase non‐target effect occurrence by beetle range expansion to additional areas where A. sessilis occurs. This study highlights the importance of understanding how climate change affects species interactions for future biological control of invasive species and conservation of native species.     

The parasitic fly Nemorilla maculosa exploits host‐plant volatiles to locate the legume pod borer,Maruca vitrata

Nemorilla maculosa Meigen (Diptera: Tachinidae) is a solitary endoparasitoid of the legume pod borer, Maruca vitrata Fabricius (Lepidoptera: Crambidae), a key pest of cowpea, Vigna unguiculata (L.) Walp. (Fabaceae) in Africa. A colony of N. maculosa, introduced for experimental purposes from Taiwan to the laboratories of the International Institute of Tropical Agriculture (IITA) in Benin, was used for our studies. Olfactory reponses of N. maculosa to leaves of infested or uninfested cowpea and yellow peabush, Sesbania cannabina (Retz.) Pers. (Fabaceae), and to M. vitrata larvae were evaluated in a four‐arm olfactometer. For all combinations of odor sources, responses between naïve and oviposition‐experienced female flies did not differ. Nemorilla maculosa females were attracted by odors from uninfested leaves of yellow peabush and flowers of cowpea when compared with clean air, and they were attracted to plants damaged by M. vitrata with larvae removed. However, the female fly did not discriminate between odors from infested and uninfested plants. The parasitic fly N. maculosa proved well able to use volatile compounds from various host plants (peabush and cowpea) to locate its host, with a more pronounced attraction by the combination of host larvae and infested host plant parts. These findings are discussed in light of the prospective use of N. maculosa as a biological control agent against the legume pod borer.     

Species-specific effects of polyploidisation and plant traits of Centaurea maculosa and Senecio inaequidens on rhizosphere microorganisms

Invasive plant species represent a threat to terrestrial ecosystems, but their effects on the soil biota and the mechanisms involved are not yet well understood. Many invasive species have undergone polyploidisation, leading to the coexistence of various cytotypes in the native range, whereas, in most cases, only one cytotype is present in the introduced range. Since genetic variation within a species can modify soil rhizosphere communities, we studied the effects of different cytotypes and ranges (native diploid, native tetraploid and introduced tetraploid) of Centaurea maculosa and Senecio inaequidens on microbial biomass carbon, rhizosphere total DNA content and bacterial communities of a standard soil in relation to plant functional traits. There was no overall significant difference in microbial biomass between cytotypes. The variation of rhizosphere total DNA content and bacterial community structure according to cytotype was species specific. The rhizosphere DNA content of S. inaequidens decreased with polyploidisation in the native range but did not vary for C. maculosa. In contrast, the bacterial community structure of C. maculosa was affected by polyploidisation and its diversity increased, whereas there was no significant change for S. inaequidens. Traits of S. inaequidens were correlated to the rhizosphere biota. Bacterial diversity and total DNA content were positively correlated with resource allocation to belowground growth and late flowering, whereas microbial biomass carbon was negatively correlated to investment in reproduction. There were no correlations between traits of the cytotypes of C. maculosa and corresponding rhizosphere soil biota. This study shows that polyploidisation may affect rhizosphere bacterial community composition, but that effects vary among plant species. Such changes may contribute to the success of invasive polyploid genotypes in the introduced range.     

Distribution of Insect Attacks in Biological Control of Weeds: Infestation of Centaurea virgata Flowerheads by a Gall Fly

The success of biological control efforts to reduce weed density through release of insects may depend as much on the distribution of insect attacks among individual plants or plant parts as on the mean level of infestation. We used an index of dispersion to describe the distribution of Urophora quadrifasciata (Diptera: Tephritidae) galls among squarrose knapweed (Centaurea virgata) flowerheads at 18 west central Utah sites in the first 5 years following introduction of the biological control agent. Two thirds of the samples showed a significantly aggregated distribution of galls among flowerheads. Statistical analysis showed that site and year accounted for relatively small proportions of the variance in the index of dispersion. The degree of gall aggregation among flowerheads was positively correlated with the mean flowerhead quality (mean number of seeds per flowerhead; P = 0.013) and tended to be negatively correlated with the mean fly density per flowerhead at a site in a given year (P = 0.097). Our data suggest that higher quality flowerheads, and possibly higher quality plants, are preferentially attacked by U. quadrifasciata and therefore are more heavily subject to reduced reproductive potential through biological control. However, an aggregated distribution of fly attacks may undercut the potential of the fly to reduce seed production by the weed population as a whole. Understanding both the distribution of insect attacks among individual plants and the behavioral mechanisms producing such distribution patterns is important to the biological control of weeds.     

Biological control of invasive plants through collaboration between China and the United States of America: a perspective

For more than 100 years, classical biological control of invasive plants through screening, introducing and releasing of host-specific natural enemies from native regions has been regarded as one of the promising approaches to the management of invasive plants. Many invasive plants in the United States of America are native to China, and vice versa. China and the USA also share a number of invasive plant species, including water hyacinth (Eichhornia crassipes), alligator weed (Alternanthera philoxeroides) and cordgrass (Spartina spp.). Collaboration between the two countries on biological control benefits both the nations by reciprocal opportunities to research and exchange natural enemies, by exchanging information on common invasive species, and by providing training for students and professionals. Here we review the history of collaboration between China and the US on biological control of more than 20 invasive plants. Current collaborative projects associated with four plant species, Polygonum perfoliatum L., Trapa natans L. Pueraria montana (Lour.) Merr. var. lobata and Ailanthus altissima (Mill.) Swingle, are also covered. We prioritize 14 invasive plants as targets for future collaborative biological control based on information on their importance in introduced areas, natural enemy records, and their potential biocontrol risk to introduced ecosystems. They are: Ampelopsis brevipendunculata, Celastrus orbiculatus, Dioscorea oppositifolia, Euonymus alata, Euonymus fortunei, Ligustrum sinense, Melia azedarach, Paulownia tomentosa, Sapium sebiferum and Ulmus pumila for the US, as well as Spartina alterniflora, Ambrosia artemisiifolia, Ambrosia trifida and Solidago canadensis for China. In addition, we emphasize that we must very carefully consider any potential non-target effect when we intend to introduce and release new natural enemies. We anticipate that the high priority both countries have placed on control of invasive plants will stimulate increasing collaboration on biological control.     

Non-target effects of an introduced biological control agent on deer mouse ecology

Release of exotic insects as biological control agents is a common approach to controlling exotic plants. Though controversy has ensued regarding the deleterious direct effects of biological control agents to non-target species, few have examined the indirect effects of a ”well-behaved” biological control agent on native fauna. We studied a grassland in west-central Montana infested with spotted knapweed (Centaurea maculosa) to examine the effects of knapweed invasion and two gall flybiological control agents (Urophora affinis and U. quadrifasciata) on the native deer mouse (Peromyscus maniculatus). Stomach-content analysis revealed that Urophora were the primary food item in Peromyscus diets for most of the year and made up 84–86% of the winter diet. Stomach contents indicated that wild-caught mice consumed on average up to 247 Urophora larvae mouse^–1 day^–1, while feeding trials revealed that deer mice could depredate nearly 5 times as many larvae under laboratory conditions. In feeding trials, deer mice selected knapweed seedheads with greater numbers of galls while avoiding uninfested seedheads. When Urophora larvae were present in knapweed seedheads, deer mice selected microhabitats with moderately high (31–45% cover) and high knapweed infestation (≥46% cover). After Urophora emerged and larvae were unavailable to Peromyscus, mice reversed habitat selection to favor sites dominated by native-prairie with low knapweed infestation (0–15%). Establishment of the biological control agent, Urophora spp., has altered deer mouse diets and habitat selection by effecting changes in foraging strategies. Deer mice and other predators may reduce Urophora populations below a threshold necessary to effectively control spotted knapweed. Received: 04 May 1999 / Accepted: 14 August 1999     

A strategy for evaluating the safety of organisms for biological weed control

A strategy for establishing the specificity and safety of an organism as a biological weed control agent is described. A critical first step is to expose to its attack a small group of plants very closely related and exhibiting morphological and biochemical similarities to the weed. To prevent an erroneous negative result tests are also made on selected cultivated plants, including those closely related to the weed, those of which the associated insects and fungi are little known, those that have evolved apart from or been little exposed to the agent, those attacked by closely related organisms and those already recorded as hosts. The circumstances under which the strategy might fail to indicate safety are discussed, i.e. polyphagous organisms attacking plants irregularly distributed throughout many families, organisms highly specific to two alternate hosts, and those attacking two or three phylogenetically widely separated plant groups. The additional crop plant testing, included in the overall strategy to deal with such possible failures, is discussed. It is shown that the strategy would have included Sesamum tndicum in the list of plants challenged by the bug Teleonemia scrupulosa in biological testing for control of Lantana camara, thereby forewarning of the attack that was subsequently observed in Africa.     

Establishment and Dispersal ofUrophora affinis(Diptera: Tephritidae) andMetzneria paucipunctella(Lepidoptera: Gelechiidae) in Southwestern Virginia

Two European gall-producing insects,Urophora affinisFrfld. (Diptera: Tephritidae) andMetzneria paucipunctella(Zeller) (Lepidoptera: Gelechiidae) were introduced into Virginia in 1986 for biological control of spotted knapweed (Centaurea maculosaLam.). Adults ofU. affinis(n = 2625) andM. paucipunctella(n = 450) were released at two sites in Montgomery County, Virginia, and their populations were monitored yearly by dissecting spotted knapweed flower heads. Beginning in 1992, knapweed samples collected at various distances from the release sites were checked for dispersal.U. affinisis well established and is spreading slowly. The number of larvae per flower head and the seed numbers are inversely related as plants with the greatest number of larvae per spotted knapweed head had the lowest number of seeds. Knapweed density has declined at one of the release sites which had the highest rate of infestation byU. affinis.Establishment of the moth,M. paucipunctella,is less certain as it has been recovered at a very low level from only one site.     

Biology and host specificity of Aulacobaris fallax (Coleoptera: Curculionidae), a potential biological control agent for dyer’s woad,Isatis tinctoria (Brassicaceae) in North America

Dyer’s woad, Isatis tinctoria, a plant of Eurasian origin is a problematic weed in western North America against which a classical biological weed control programme was initiated in 2004. Three European insect species were selected as candidate agents to control this invasive species, including the root‐mining weevil Aulacobaris fallax. To determine its suitability as an agent, the biology and host specificity of A. fallax were studied in outdoor plots and in the field between 2004 and 2006 in its native European range. Aulacobaris fallax is a univoltine species that lays its eggs from March to August into leaf stalks and roots of dyer’s woad. Larvae mine and pupate in the roots and adults emerge from August to October. Up to 62% of the dyer’s woad plants at the field sites investigated were attacked by this weevil. In no‐choice host‐specificity tests, A. fallax attacked 16 out of 39 species and varieties within the Family Brassicaceae. Twelve of these are native to North America. In subsequent multiple‐choice tests, seven species, all native to North America, suffered a similar level of attack as dyer’s woad, while none of the European species were attacked. Our results demonstrate the importance of including test plant species that have not co‐evolved with the respective candidate agent. In sum, we conclude that the risk of non‐target effects is too high for A. fallax to be considered as a biological control agent for dyer’s woad in the United States.     

Effects of a nematode Meloidogyne incognita and its interaction with above‐ground herbivory on an invasive wetland plant,alligator weed (Alternanthera philoxeroides)

Invasive plants may be attacked both above ground and below ground. Few studies have, however, investigated the simultaneous effects of above‐ground and below‐ground herbivory. In the present study, we report the effects of beetle herbivory and nematode infection on alligator weed, Alternanthera philoxeroides, an invasive plant in China. We found that the root‐knot nematode Meloidogyne incognita widely occurred on the plant in south China. To examine its effect on the plant in conjunction with above‐ground herbivory, we conducted a field common garden experiment with a local insect defoliator, Cassida piperata. We also included the native congener Alternanthera sessilis in our experiments for a comparison of the response of invasive and native species. We found no significant effects on plant biomass of the nematode infection in conjunction with the above‐ground herbivory. Further chemical analysis, however, showed that the water‐soluble carbohydrate content in roots of A. philoxeroides was significantly increased in plants attacked by both the nematode and the herbivore compared with the water‐soluble carbohydrate content in plants attacked by only the nematode or herbivore alone. We found no such change in the native congener A. sessilis. Together these results may suggest that A. philoxeroides tolerates joint above‐ground and below‐ground damage by allocating more resources to below‐ground material.     

The lesser of two weevils: physiological responses of spotted knapweed (Centaurea stoebe) to above- and belowground herbivory by Larinus minutus and Cyphocleonus achates

The physiological responses of plants to variable levels of root and shoot herbivory in the field may yield valuable insights regarding potential compensation or tolerance responses for herbivory. In an infestation of Centaurea stoebe (spotted knapweed) located in the Colorado foothills, we measured physiology, biomass, and flower production of individual plants undergoing a natural range of herbivory by the above- and belowground biological control insects, Larinus minutus and Cyphocleonus achates. Over the growing season, net carbon assimilation rate, transpiration, stomatal conductance, and intercellular leaf [CO₂] (C _i) all decreased, while water use efficiency increased. The decrease in these physiological traits was due to an increase in the intensity of L. minutus damage over time; effects of C. achates root damage to plant physiology, including transpiration were only marginally significant. The effects of these two species on plant physiology were not interactive, and Larinus minutus was found to exert larger negative effects on this invasive plant in terms of plant physiology and potential reproductive output than C. achates. While previous studies have shown C. achates to have significant negative effects on population densities of spotted knapweed, the addition of Larinus minutus to the suite of insects used in biological control of spotted knapweed should facilitate continued or enhanced reduction in densities of this noxious weed.