Centaurea Stoebe) Growth and Reproduction

Ecological Applications, 20(7), 2010, pp. 1903–1912 Ó 2010 by the Ecological Society of America Reconciling contradictory findings of herbivore impacts on spotted knapweed (Centaurea stoebe) growth and reproduction 1 DAVID G. KNOCHEL AND TIMOTHY R. SEASTEDT Department of Ecology and Evolutionary Biology, Institute of Arctic and Alpine Research, University of Colorado, Boulder, Colorado 80309 USA Abstract. Substantial controversy surrounds the efficacy of biological control insects to reduce densities of Centaurea stoebe, a widespread, aggressive invasive plant in North America. We developed a graphical model to conceptualize the conditions required to explain the current contradictory findings, and then employed a series of manipulations to evaluate C. stoebe responses to herbivores. We manipulated soil nitrogen and competition in a field population and measured attack rates of a foliage and seed feeder (Larinus minutus), two gall flies (Urophora spp.), and a root feeder (Cyphocleonus achates), as well as their effects on the growth and reproduction of C. stoebe. Nitrogen limitation and competing vegetation greatly reduced C. stoebe growth. L. minutus most intensively reduced seed production in low- nitrogen soils, and removal of neighboring vegetation increased Larinus numbers per flower head and the percentage of flowers attacked by 15% and 11%, respectively. Cyphocleonus reduced flower production and aboveground biomass over two years, regardless of resources or competition. Our results, in conjunction with other published studies, demonstrate that positive, neutral, and negative plant growth responses to herbivory can be generated. However, under realistic field conditions and in the presence of multiple herbivores, our work repudiates earlier studies that indicate insect herbivores increase C. stoebe dominance. Key words: biological control; Centaurea stoebe; compensation; Cyphocleonus achates; herbivory; Larinus minutus; plant competition; resource limitation; spotted knapweed; Urophora spp.; weed management. INTRODUCTION The biological control insects studied here, a flower head weevil Larinus minutus Gyllenhal (Coleoptera: Spotted knapweed (Centaurea stoebe L. subsp. mi- Curculionidae), two gall fly species of the genus cranthos [Gugler] Hayek [Asteraceae]), also identified as Urophora, U. affinis Frfld and U. quadrifasciata C. maculosa and C. biebersteinii (see Ochsmann 2001, Meigen (Diptera: Tephrididae), and the root-feeding Hufbauer and Sforza 2008), is one of several species of weevil, Cyphocleonus achates Fahr. (Coleoptera: the Eurasian knapweeds (Centaurea spp.) that have Curculionidae), have been at least locally abundant at become dominant components of the rangeland vegeta- sites across North America for about two decades. tion in western North America (Sheley et al. 1999). C. These insects established on spotted knapweed, but to stoebe now occupies over three million ha in rangeland date, reports of significant population reductions and forest ecosystems in North America, and 13 species attributed to insect effects are few (Corn et al. 2006, of insects have been released since 1970 in an attempt to Cortilet and Northrop 2006, Jacobs et al. 2006, Story et reduce its abundance (Story and Piper 2001). However, al. 2006, 2008, Michels et al. 2009). The perennial the effectiveness of insect introduction as a sustainable growth habit of spotted knapweed likely improves its method to control the plant remains controversial, and capacity to maintain dense populations, despite reduc- other unsustainable and cost-prohibitive management tions of seed production and tissue damage from techniques still predominate. Further, despite intense biological control insects. scientific inquiry aimed at understanding and explaining Other field studies of a root-feeding moth (Agapeta the unusually high dominance seen in this invasive zoegana L. [Lepidoptera: Tortricidae]) and clipping species, we lack information on how reintroduced treatments to simulate herbivory demonstrated that natural enemies, resource availability, and plant com- plant fitness may improve if plants respond to damage petition might collectively influence densities and by releasing allelopathic compounds that harm adjacent population dynamics of the plant. vegetation (Callaway et al. 1999, Thelen et al. 2005, Newingham et al. 2007). The efficacy of these compounds has been challenged (e.g., Chobot et al. 2009, Manuscript received 20 October 2009; revised 15 December Duke et al. 2009); however, competitive outcomes in 2009; accepted 16 December 2009. Corresponding Editor: T. J. Stohlgren. response to herbivory may be valid, regardless of the 1 E-mail: [email protected] specific mechanism(s) producing this response. Urophora 1903 1904 DAVID G. KNOCHEL AND TIMOTHY R. SEASTEDT Ecological Applications Vol. 20, No. 7 range from low to high, depending on both the identities and densities of biological control insects present and whether multiple species are feeding on root and foliar tissues and seeds (Knochel 2009). In this context, a range of local resource conditions (e.g., soil nutrients, water, sunlight) and competition for these resources by adjacent vegetation will determine how C. stoebe plants fare. Collectively, these plant–insect–resource interactions at small spatial scales are hypothesized to govern spotted knapweed dominance and its population dynamics. These interactions may explain the high variability in the previously discussed outcomes ob- served for biological control insects on C. stoebe. In a field population of C. stoebe, we measured the effects of herbivory by specialist root-feeding FIG. 1. A hypothetical gradient of spotted knapweed (Cyphocleonus achates) and stem-, foliage-, and flower- (Centaurea stoebe) fitness responses to herbivory, as regulated head-feeding (Larinus minutus, Urophora spp.) biologi- by the combined influence of resource availability and plant cal control insects, which were allowed free access to competition. This is analogous to the compensatory continuum plants in plots that differed in levels of soil nitrogen (N) model proposed by Maschinski and Whitham (1989), except that here the intensity rather than the timing of herbivory is availability and plant competition. We tested three considered. At a given intensity of herbivory (sliding the vertical predictions related to the model shown in Fig. 1. (1) bar left or right) spotted knapweed could potentially (A) Does spotted knapweed lose its competitive advantage overcompensate, (B) equally compensate, or (C) undercom- when soil resources are in low supply, and is the plant pensate for damage, depending on the levels of resource availability. Further, the presence of competition from neigh- susceptible to competition from neighboring plants? (2) boring vegetation could shift the response downward at a given Does a gradient in soil nutrient availability and resource level. neighboring plant cover affect attack rates of biological control insects? (3) Do the effects on plant performance by root-feeding and flower head insects depend on N gall flies may also indirectly benefit spotted knapweed supply or neighboring plant competition? This field through interactions with deer mice that reduce seed experiment sought to demonstrate the range of potential abundance of native competitors (Pearson and Callaway responses that occur when spotted knapweed interacts 2008). Further, others hypothesized that a persistent with variable levels of soil resources, plant competitors, drought throughout the western United States contrib- and biological control insects. uted at least partially to population declines (Corn et al. 2007, Pearson and Fletcher 2008). Thus the extent to METHODS which these insects might control C. stoebe over the Field site description three million ha of invaded rangelands remains uncer- tain. Similar to the theoretical approach used by Shea et Field research was conducted 15 km northwest of al. (2005) to assess biological control impacts on an the city of Boulder, Colorado, USA (4080701400 N, invasive thistle, we suggest that variation in resource 10581902600 W), between 1865 m and 2070 m elevation, conditions and plant competition are likely to govern on meadows and on rugged 15–60% slopes that are spotted knapweed responses to herbivory and ultimately dominated by ponderosa pine (Pinus ponderosa Douglas govern population growth. A complete analysis of how Ex. Lawson). Soils at the site are composed of the Fern environmental drivers interact with herbivory is essential Cliff-Allens Park-Rock outcrop complex, and the soils in order to understand or predict the long-term of experimental meadows within the stream drainage are relationship between C. stoebe populations and special- of mixed loamy alluvium parent material, with a stony, ist biological control insects. sandy clay loam profile at 0–100 cm depth (National Here we propose an herbivory–resource gradient Resources Conservation Service 2008). Mean annual air model, which describes how resource constraints and temperature is 6–88C, with a frost-free period of 80À120 plant competition moderate the interactions between C. days. In the mid 1980s, Centaurea stoebe was acciden- stoebe individuals and biological control insects (Fig. 1). tally introduced to this area and has spread over 40 ha of The model is built upon the conceptual frameworks of meadows, riparian areas, and forest that burned in a McNaughton (1979), Maschinski and Whitham (1989), wildfire in 1988. This fire apparently facilitated the and most recently,

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