Exotic Weevil Invasion Increases Floral Herbivore Community

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

Tatyana A. Rand and Svata M. Louda

T. A. Rand ([email protected]), USDA-ARS, Northern Plains Agricultural Research Lab, Sidney, MT 59270, USA. TAR and S. M. Louda, School of Biological Sciences, Univ. of Nebraska-Lincoln, NE 68588-0118, USA.

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 infl uence of such species additions on native resident herbivore guilds, along with their individual and combined eff ects 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 fl oral herbivores (tephritid fl ies, pyralid moths) to infl uence 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 signifi cantly 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 eff ects. 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 fl oral guild was associated with a signifi cant increase in herbivore community function and impact on seed production. Th e results suggest that invasion of a functionally dominant herbivore into an unsaturated recipient community can augment function within a resource guild.

Anthropogenically-mediated environmental changes, such infl uence important aspects of consumer community func- as habitat loss and climate change, have been implicated in tion, such as aggregate consumer abundances and levels of the dramatic declines in global biodiversity (Wilcove et al. resource depletion (Cardinale et al. 2006). Changes in com- 1998, Millennium Ecosystem Assessment 2005). Concern munity function may occur through a number of diff erent over the impacts of such declines, in turn, has generated a mechanisms. For example, as the number of consumer spe- large body of research dedicated to elucidating the relation- cies increases in a local community, the chance of adding a ships between biodiversity losses and critical ecosystem func- particularly effi cient consumer increases, thereby potentially tions and services upon which humans depend (reviewed altering ecosystem function via what has been referred to by Hooper et al. 2005, Cardinale et al. 2006, Bruno and as ‘ lottery ’ or ‘ selection ’ eff ects (Denoth et al. 2002, Hector Cardinale 2008, Duff y 2009, Letourneau et al. 2009). Spe- et al. 2002). Alternately, consumer species may interact in cies invasions, while also considered a primary driver of complex ways, with complementarity or interference poten- native species decline globally, may in some cases actually tially impacting the functional outcomes and the ultimate increase richness at regional and local scales (Rosenzweig impacts of consumer richness on resource populations (Ives 2001, Sax and Gaines 2003). While widespread attention et al. 2005, Bruno and Cardinale 2008). Ultimately, the has been given to the functional implications of species eff ect of a consumer species on function within a consumer losses, the functional implications of exotic species additions guild will depend upon both the traits of that species, relative remain less commonly investigated (Sax and Gaines 2003). to other members of the guild, and the factors that structure Rates of species invasion and extinction tend to be the recipient community and so determine the response of skewed by trophic position (e.g. higher trophic levels are guild members to species addition or loss, e.g. whether the often more susceptible to extinction), thereby potentially community exhibits density compensation (Mooney et al. altering the nature and importance of interactions between 1996, Ruesink and Srivastava 2001). Species traits shown to consumers and resources (Duff y 2002, 2003, Byrnes et al. be important in determining functional outcomes include: 2007). Changes in consumer richness or composition may the degree of similarity/overlap in resource use among guild

85 members, relative functional effi ciency (per capita eff ects 1982, Louda and Potvin 1995). Th ese include two fl y species on resources), relative abundance, and relative competitive (Tephritidae), Paracantha culta and Orellia occidentale, and ability (Lawton and Brown 1993, Morin 1995, Mooney two moths (Pyralidae), Homoeosoma impressale and Pyrausta et al. 1996, Ruesink and Srivastava 2001, Duff y 2002, Hector subequalis plagialis . Th e fl ower head weevil Rhinocyllus coni- et al. 2002, Larsen et al. 2005, Balvanera et al. 2006). cus was introduced from Europe into the United States in Although still understudied compared to plant invasions, 1969 to limit seed production by invasive Eurasian Carduus insect invasions are increasingly common, and their impacts spp. (Surles and Kok 1978). It was introduced into Nebraska have gained recent attention (Kenis et al. 2009, Gandhi and in 1972 (McCarty and Lamp 1982), and subsequently Herms 2010). Invasive insect herbivore impacts tend to be expanded its range to feed on native thistle species including documented more commonly for economic pests of agri- C. canescens, on which it was fi rst reported at two long-term culture and forestry, e.g. soybean aphid and bark beetles, study sites in the Nebraska Sand Hills in 1993 (Louda et than for exotic species in natural systems (National Research al. 1997). Densities of R. conicus within C. canescens fl ower Council 2002). Studies within native systems continue to heads initially increased rapidly and then began to level off be heavily biased towards forest invaders, with few studies by the time this study was initiated in 1996 (Louda 1998). from herbaceous ecosystems (Kenis et al. 2009, Gandhi and Th e native fl oral herbivores (tephritid fl ies, pyralid moths) Herms 2010). Exotic insect herbivores can have important and R. conicus all consume tissues within developing thistle ecological impacts on native communities, both via direct fl ower heads, including fl orets, ovaries, developing ovules eff ects, e.g. by feeding on native plant species, and via indi- and seeds. Additionally, moths and the weevil often under- rect eff ects, e.g. by competing for resources with native her- mine the developing fl orets, ovules and immature seeds that bivores (reviewed by Kenis et al. 2009). However, studies are not destroyed directly, by damaging supporting receptacle that examine how the addition of an exotic insect species to a tissue, causing abortion. Lepidopteran herbivores consume resident herbivore guild simultaneously infl uences herbivore fl ower, seed and receptacle tissues directly, especially in later community function and impacts on resource populations instars (Lamp and McCarty 1982) and R. conicus also feeds are lacking. on all of these tissues (Zwö lfer and Harris 1984). None of Here, we examined patterns of site-to-site and plant- these insects are gall formers. Manipulative fi eld experiments to-plant variation in insect fl oral herbivore composition to have demonstrated that R. conicus can have strong competi- evaluate how the addition of an invasive weevil, Rhinocyl- tive eff ects on fl ies, both by disrupting fl y oviposition behav- lus conicus, combined with the guild of native herbivores ior and competing for resources within thistle fl ower heads; (tephritid fl ies, pyralid moths) to aff ect fl oral herbivore com- however there is no evidence of intraguild predation among munity structure, function and, ultimately, seed production herbivores (Louda and Arnett 2000, Louda et al. 2011). of a native host thistle, Cirsium canescens, across most of its While some diff erences in phenology exist (Lamp and range in midgrass sand prairie. We fi rst compared plants at McCarty 1982), there is a great degree of temporal overlap sites that were either invaded or not invaded by this exotic among these insects. Adults of all the fl oral herbivores are herbivore across the regional spatial scale to ask whether the active in May and June, signifi cantly overlapping the period species addition aff ected two key components of herbivore during which C. canescens fl ower heads develop and mature community function: aggregate fl oral herbivore density and (Lamp and McCarty 1982, Gassmann and Louda 2001). levels of seed destruction. We then examined plant-to-plant Rhinocyllus conicus has the greatest temporal overlap with the variation in patterns of attack by the three herbivore groups dominant tephritid fl y Paracantha culta (Louda 1998). Th us, to explore the potential roles of insect functional traits and overall, the strategies of the herbivores in this fl oral guild are community response (i.e. density compensation or lack similar, with a high degree of overlap in resource use. thereof) in infl uencing functional outcomes. Finally, we asked how addition of the invasive weevil to the herbivore Sites and sampling design guild infl uenced seed production by the native thistle, both across sites and among individual plants. By examining the To quantify the interaction of native fl oral insect herbivores structural and functional response of the herbivore guild to with this exotic species over the majority of the plant’ s global invasion over the regional distributional scale of the interac- distribution, we sampled in sites throughout sand prairie in tions, these data provide both an important complement to the northcentral Great Plains. In planning, potential sam- smaller scale, intensive experimental studies and added insight pling sites were laid out in a grid across the Sand Hills and into the functioning of native herbivore communities. major peripheral sand formations in Nebraska in 1996, and then extended in 1997 and 1998 to include more sand and peripheral gravelly sand prairie in Colorado, Wyoming, and Methods South Dakota (n ϭ 94, 113 and 112 sites, in 1996, 1997 and 1998 respectively); original sites were re-sampled in 1997 Study system and 1998. In collecting, actual sampling sites were selected based on occurrence of at least 5– 10 thistles in proximity Cirsium canescens (Platte thistle), a native monocarpic species, to the pre-planned sampling location and by site accessibil- occurs in small local patches in midgrass prairie on sand and ity, with at least 15 km between sites. Th istles were sampled gravelly sand soils in the northcentral Great Plains and south- along rangeland edges and roadside, due to ease of access, ern Rocky Mountains, USA (Great Plains Flora Association and thus were located in predominantly ungrazed grassland 1986). Four native insects commonly feed within the devel- areas. All samples were collected in the last week of June each oping infl orescences of C. canescens (Lamp and McCarty year, near the end of the fl owering season for Platte thistle.

86 Five plants were sampled at each site in each year. Individ- condition of the seeds remaining, the condition of the recep- ual thistles were selected by walking in straight lines through tacle, and the number of seeds expected for an undamaged the local patch, using every second or third fl owering plant head in that position on a plant. depending upon the number available. For each plant sam- Since insect feeding on fl ower heads destroys seed both pled, we recorded stem height (soil to base of terminal head), directly, by consuming developing ovules, and indirectly, by total number of fl ower heads initiated (Ն 5 mm diameter) feeding on subtending receptacle tissues that disrupts ovule and number of heads that fl owered (exerted at least one fl o- development, an actual count of total seed initiated was ret). We collected fl ower heads for dissection (terminal heads impossible in heads with extensive insect feeding. For such on main stem and alternating side branches, plus the fi rst heads, we calculated the expected total number of seeds initi- sub-terminal fl ower head that fl owered); the collected heads ated for that fl ower head, based on its position on the plant, represent those with the highest probability of setting seed and used this to estimate the number of seeds destroyed by (Louda and Potvin 1995). insect feeding in the head. Th e expected number of seeds was the mean total number of seeds observed for undam- Quantifi cation of insect densities, seed aged fl ower heads in that fl ower head position across all destruction and seed production years and sites. Th e whole head estimates of the numbers of undamaged, insect-destroyed, and other damaged seeds were In the laboratory, each fl ower head was measured (mean then calculated from the dissection data using the following diameter), weighed, halved, and each half dissected rules. For fl ower heads that fl owered and had not released (n ϭ 1282, 1370 and 1101 fl ower heads representing 466, seed, the number of good seed was the actual count of the 636 and 561 plants, in 1996, 1997 and 1998, respectively). fi lled and undamaged seeds per head; the number of other- On the fi rst half dissected, we recorded number and pro- damaged seeds was twice the number other-damaged seed portion of countable seeds in three categories: undamaged, counted in the fi rst half; and, the number of insect-destroyed fi lled potentially viable ‘ good ’ seed; insect damaged fi lled seeds was total seed initiated (either actual count or estimate or unfi lled ‘ destroyed seed ’ ; and, undeveloped or aborted for head position) minus the numbers of undamaged and seed without direct evidence of insect feeding, called ‘ other other-damaged seeds. Finally, for fl ower heads that fl owered damaged seed ’ ; we also recorded type of insect damage and and had released some seed, the total number of fi lled and the number insects by taxon. On the second half, we only undamaged seeds, along with the proportion missing in each recorded number of undamaged, fi lled ‘ good ’ seeds; type of seed category, was estimated using the ratio among catego- insect damage, and insects present. In addition, we scored ries observed among the seeds remaining and the condition the condition of the fl ower head receptacle under the develop- (damage) of the receptacle. ing fl orets and seeds, and recorded evidence of insect damage (e.g. chewing, tunneling, frass, kinked pappi, etc.). Statistical analyses Th e number of insects was counted, or estimated if the insect was no longer present, using the following rules. Th e For the large-scale, across site analyses, each site was catego- number of R. conicus weevils was either the tally of adult, rized as invaded or not invaded by the exotic weevil, R. coni- pupal, and larval weevils present or the number of distinc- cus: invaded sites had evidence of R. conicus on the sampled tive, compacted chambers made by late instar weevils in the plants (egg cases, larvae, pupae, adults or characteristic wee- head; since weevils began emerging from fl ower heads before vil damage) in any year, whereas uninvaded sites had no evi- heads were collected, the best estimate of the number that dence of R. conicus on sampled plants over the entire study. developed per fl ower head was the larger of the two: number Per site means were calculated for three response variables: of weevils present or number of pupal chambers. Th e num- aggregate (total) insect density, proportion insect-destroyed ber of fl ies, composed predominantly of Paracantha culta seed, and total undamaged, fi lled ‘ good ’ seed per fl ower head that generally pupates within the fl ower head, was recorded per plant; each was calculated as the mean value across all as the larger of the number of adults or pupal cases observed. plants sampled across all years at a site. Th ese were used in Evidence of feeding by the less common native fl ies, pri- the site-level regional analysis (site ϭ unit of replication). marily Orellia occidentale, in the absence of either adults or Bigger fl ower heads contain more seed resources, and can pupal cases or larvae, was treated as ‘ at least one ’ fl y pres- attract and support the development of more insects (Louda ent. Similarly, the number of native moths, predominantly and Potvin 1995). Similarly, insects may be attracted to Homoeosoma impressale and Pyrausta subequalis plagialis , plants with greater overall levels of resources. Th us, we con- developing per fl ower head was recorded as the number of trolled for any potential confounding infl uences of resource moth larvae present, or in the absence of the larvae but pres- size and availability by including them as covariates in all ence of distinctive feeding evidence, the number of moths statistical models examining the potential infl uences of R. was recorded as ‘ at least one ’ moth present. conicus addition on consumer function and impact. For the To quantify the total number of good seed produced and site scale analysis, we used linear models to examine the infl u- the proportion insect-destroyed seeds per fl ower head, we ence of R. conicus invasion (presence vs absence at a site) on used the following rules. For unreleased heads (evident from each response variable, with mean fl ower head diameter and condition of the fl ower head), potentially viable good seed the mean number of fl ower heads initiated per plant included was the sum of the fi lled, undamaged seeds in both halves as covariates in the model. Proportion data were arcsine of the head. For the few heads that had started releasing square root-transformed for analysis, and mean numbers of their seeds prior to collection (Ͻ 5%), total undamaged seed good seeds and insect densities per fl ower head were power- released was estimated using three pieces of information: the transformed (x0.5 ) to best normalize distributions. Similar

87 models were run to compare densities of native insects at above, site and year (random eff ects), as well as mean head invaded versus uninvaded sites. Statistical models were run diameter and the number of fl ower heads per plant (fi xed in JMP ver. 8.0.1 (SAS Inst.). eff ects), were included in the model. Tukey HSD tests For the individual plant scale analyses, each plant was cat- were used to test for diff erences among guild composition egorized by the presence or absence of each insect taxon (fl ies, categories. moths, weevil) using evidence from the dissections (above). Plants occurred in all eight possible categories: no evidence of feeding by any of the three insect taxa, each taxon as the Results sole attacker on a given plant (evidence of feeding by only one of the taxa), and all two and three taxon combinations; Among site variation in herbivore community we refer to these categories hereafter as insect guild composi- function and impact in relation to insect invasion tion. Plant level estimates of insect density, proportion insect destroyed seed and good seeds produced were calculated on Th e weevil invasion was extensive across Cirsium cane- a per fl ower head basis, since collected fl ower heads were a scens’ range, with Rhinocyllus conicus present at 114 of sub-sample and unequal numbers of heads were available to the 126 total sites sampled. Invasion by R. conicus more be sampled per plant. Both aggregate insect density, i.e. the than doubled the mean aggregate insect density observed sum of the counts across all insect taxa, and insect density by per plant at the site scale (Fig. 1a). Native insect densi- taxon were calculated. We calculated mean insect density for ties were similar at invaded and uninvaded sites (Fig. 1a), each individual plant as the cumulative number of all insects with no signifi cant diff erences observed in fl y densities ϭ ϭ observed in all the heads dissected divided by the number (F 1,122 1.27; p 0.2623), while moth densities were ϭ ϭ fl ower heads sampled for that plant. Estimates of good seed slightly lower at invaded sites (F1,122 6.07; p 0.0151). produced for an individual plant also was calculated as the Th e proportion of insect destroyed seeds was signifi cantly total count of fi lled and undamaged good seed in all the heads higher at invaded sites (85% vs 71%: Fig. 1b); and seed dissected divided by the number of heads sampled on that production by the native thistle decreased dramatically, to plant. Per plant estimates of proportion seed lost to insect ∼50% of the level when only native insects were present feeding was calculated by averaging the proportion of insect (Fig. 1c). Th ese eff ects of R. conicus were independent of destroyed seed per fl ower head (number of insect-destroyed any infl uences of resource size or per plant resource avail- seeds divided by the sum of total expected seed initiated for a ability, since indices of these variables were included as fl ower head) across all fl ower heads sampled for a plant. covariates in statistical models. We fi t mixed eff ects linear models, using the REML Aggregate insect density at a site was positively related ϭ Ͻ (restricted maximum likelihood) method in JMP, to examine to mean fl ower head diameter (F1,122 31.0; p 0.0001), the infl uence of each insect taxon and each combination of but not to the average number of fl ower heads per plant ϭ ϭ insect taxa (n ϭ 7 insect categories out of 8 total) on aggregate (F 1,122 1.82; p 0.1795). Neither the proportion of insect insect densities (ln(x ϩ 1) transformed) and on the propor- destroyed seeds nor the total seeds produced per plant were tion insect destroyed seed (arcsine square-root transformed). aff ected by site to site variance in fl ower head size or mean In each model, predictor variables included: site and year number of fl ower heads per plant (p Ͼ 0.10 in all cases). (random factors), as well as head diameter, total number of Th us, overall, the data indicate that addition of the exotic fl ower heads initiated per plant and insect guild composi- insect herbivore increased two key community functional tion (fi xed factors). Similar models were run to compare the attributes, aggregate densities and levels of resource deple- eff ects of insect guild composition on ln(x ϩ 1) transformed tion; and, it resulted in signifi cantly reduced native plant individual taxon densities, i.e. density of each insect taxon in seed production. isolation compared with its density in two or in three species combinations. Tukey HSD posthoc tests were used to Among plant variation in herbivore community quantify diff erences among the herbivore guild composition function in relation to guild composition categories for all models. In order to examine potential diff erences in the func- Overall, insect guild composition signifi cantly infl uenced ϭ Ͻ tional effi ciencies of each insect taxon, i.e. per capita eff ect aggregate insect density (Fig. 2a; F6,1273 130.85; p 0.0001). on resource consumption (Balvanera et al. 2006), we evalu- As in the results of the overall cross-site regional scale analysis, ated the subset of plants from the individual plant-level data plants attacked by R. conicus had signifi cantly higher aggregate set that had been attacked by only a single insect taxon, i.e. insect densities than those attacked only by native herbivore insects occurred in ‘ monoculture ’ . Using a mixed eff ects lin- taxa, either individually or in combination (Fig. 2a). No sig- ear model, we examined variation in insect-destroyed seed nifi cant diff erences were found among guild composition cat- (arcsine square-root transformed proportion) as a function egories with R. conicus, either alone or in combination with of head diameter (index of resource size), number of fl ower one or two native taxa (Fig. 2a). heads per plant (index of resource abundance), insect taxon Among plants attacked only by the native herbivore taxa (fl ies, moths or R. conicus ), insect density, and the interaction (without R. conicus ), those attacked by fl ies and moths in between insect density and insect taxon. Site and year were combination had signifi cantly higher aggregate insect den- included in the model as random eff ects. sities compared to those attacked by either taxon alone; Finally, we used an additional linear mixed model analysis and, evidence of fl ies alone suggested higher overall densi- to examine insect guild composition eff ects on good seed ties than for moths alone (Fig. 2a). Aggregate insect density production of the native thistle (ln(x ϩ 1) transformed). As was signifi cantly positively related to both mean fl ower head

88 7 (a) Flies *** (a) 12 6 Moths R. conicus E 5 10 DE D 4 8 D

3 6

Insect density 2 C 4 A

(no. insects / flower head) 1 2 B Aggregate insect density 0 head) (no. insects / flower 0

1.0 *** (b) (b) 1.0 D 0.8 D D D C B 0.6 0.8 A

0.4 0.6

0.4 0.2 Proportion destroyed seed 0.2 0.0 Proportion destroyed seed 0.0 60 FMRFMFRMRFMR *** (c) 50 Insect guild composition

40 Figure 2. (a) Aggregate insect density and b) proportion destroyed seed per ﬂ ower head per plant, in relation to insect guild composi- ϭ ϭ ϭ 30 tion (natives: F Flies and M moths; invasive weevil: R R. conicus; and combinations thereof). Data represent raw means Ϯ SE across plants within a guild composition category. Diﬀ erent letters 20

Seed production above bars represent signifi cant diff erences between insect composition categories from Tukey HSD tests following mixed eff ects linear

(no. seeds / flower head) 10 models (REML method) with site and year included as random factors and fl ower head diameter and total number of fl ower heads 0 as covariates (Methods). Absent Present Rhinocyllus conicus did fl ies alone (Fig. 2b). Th e proportion of insect destroyed seed was signifi cantly negatively related to mean fl ower head Figure 1. (a) Aggregate insect density b) proportion insect destroyed ϭ Ͻ diameter (F1,1628 57.27, p 0.0001), and positively related seed and c) number of good seeds produced per fl ower head per ϭ to the total number of fl ower heads per plant (F1,1617 4.06, plant at sites invaded versus uninvaded by R. conicus over the three ϭ years of this study. Data represent raw means Ϯ SE at sites with p 0.0442). Th us, overall the data suggest that adding (n ϭ 114) versus without (n ϭ 12) R. conicus present. Asterisks R. conicus to the herbivore guild attacking a plant signifi - above bars indicate signifi cance levels for the eff ect of R. conicus cantly increases aggregate insect density and the proportion presence or absence: ∗ ∗ ∗ p Յ 0.0005. of seeds lost to herbivory, independent of eff ects of fl ower head size or plant level resource availability. ϭ Ͻ diameter (F1,627.8 106.91; p 0.0001) and to total num- Per plant variation in insect density by ϭ Ͻ ber of fl ower heads per plant (F1, 1221 19.11; p 0.0001). taxon in relation to guild composition Plants attacked by R. conicus had a signifi cantly higher proportion of seeds destroyed per head than did those Resource size (i.e. head diameter) and availability (i.e. number of attacked only by native herbivore taxa, either individually or heads), and insect guild composition all had signifi cant eff ects ϭ in combination (Fig. 2b, overall eff ect of guild composition: on per plant densities of R. conicus (diameter F1,868 23.73, ϭ Ͻ Ͻ ϭ Ͻ F6,1593 40.89; p 0.0001). Additionally, among individ- p 0.0001; number of heads F1,912.7 35.33, p 0.0001; ϭ Ͻ ual plants without any evidence of R. conicus attack, those guild composition F3,898.3 27.10, p 0.0001), and of moths ϭ Ͻ attacked by both fl ies and moths had signifi cantly higher (diameter F1,1112 99.40, p 0.0001; number of heads ϭ Ͻ ϭ levels of seed damage compared to those attacked by either F 1,1122 23.75, p 0.0001; guild composition F3,1113 21.60, taxon alone; and, moths alone destroyed more seed than p Ͻ 0.0001). Both R. conicus and moth densities were

89 highest when each was the sole insect attacking a plant and 1.0 on plants with larger and greater numbers of fl ower heads; and, densities of both declined consistently in two- and 0.8 three-taxon mixtures (Fig. 3). In contrast, fl y densities did not diff er signifi cantly between plants attacked by fl ies alone ϭ versus in mixtures (Fig. 3; guild composition F3,1232 1.88, 0.6 Flies ϭ Moths p 0.1314). Fly densities were also signifi cantly positively R. concius related to mean fl ower head diameter (F ϭ 52.37, 1,1238 0.4 p Ͻ 0.0001), but total number of fl ower heads per plant had ϭ Ͻ no eff ect (F 1,1244 1.60, p 0.2055). Overall, R. conicus dominated numerically (Fig. 3), whether in monoculture 0.2 or mixture, with average densities two- to three-fold higher seed destroyed Proportion than either native insect taxon. 0.0 0 5 10 15 20 25 30 Relationship of insect density and seed Insect density damage for each insect taxon (no. insects / flower head)

Analysis of the subset of plants attacked by only one insect, Figure 4. Relationship between the proportion seed destroyed by which allowed comparisons of functional performance by insect feeding and insect density for each insect taxon when that each taxon in ‘ monoculture ’ , demonstrated signifi cant dif- taxon was the only insect attacking a plant (in ‘ monoculture ’ ). ferences among insect taxa in their capacity to destroy Points represent means across all fl ower heads sampled per plant. ϭ ϭ seeds (F2,387.4 5.88; p 0.0031; Fig. 4). Insect density also had a signifi cant eff ect on the proportion of seeds show that of the three insect taxa, the invasive R. conicus destroyed (F ϭ 24.26, p Ͻ 0.0001). Furthermore, a sig- 1,388.8 had the highest functional impacts at the average densities nifi cant interaction between insect taxon and insect density ϭ Ͻ typically observed in the fi eld. (F2,399.3 9.77; p 0.0001), indicated that the relationship between insect density and seed destruction diff ered among Variation among plants in seed production in insect taxa. At low densities (Ͻ fi ve individuals per head), R. relation to guild composition conicus had the highest functional eff ect, i.e. impact on proportion seeds destroyed, followed by moths, and then by fl ies Th e average good seed produced per head was signifi cantly (Fig. 4). On plants with an average of only one insect per aff ected by insect presence and composition on a plant fl ower head, average proportion seed damaged by R. conicus (Fig. 5; F ϭ 23.96; p Ͻ 0.0001). Each insect taxon Ͼ ∼ 7,1613 alone was 85%, versus 70% by moths alone and 55% by by itself signifi cantly reduced seed production to levels well fl ies alone. Th e slope of the relationship between proportion below those that occurred when plants were not attacked seed destroyed and insect density for each taxon in monocul- by insects (Fig. 5). Th e number of good seeds produced ture was greatest for moths, which destroyed 100% of seeds per fl ower head also increased signifi cantly as mean fl ower at average densities on a plant greater than seven individuals ϭ Ͻ head diameter increased (F1,1651 89.89; p 0.0001), but per fl ower head (Fig. 4). In contrast, some plants still pro- was not signifi cantly related to total fl ower head number duced some seed even with an average density of greater than Ͻ Ͻ (F 1,1641 0.01; p 0.993). In general, patterns in net seed 15 R. conicus weevils per head (Fig. 4). Overall, these results production were consistent with the patterns found in the proportion insect-destroyed seed (Fig. 2b). Th e most strik- 10 A Flies ing pattern was a dramatic and signifi cant reduction in good Moths seed produced by plants attacked by R. conicus , compared B R. conicus 8 with those attacked only by native insects (Fig. 5). B 6 C Discussion

4 Th e patterns observed in this study provide strong evidence a a Insect density a a in support of the hypothesis that species addition through invasion can result in augmented levels of herbivore com- 2 a

(no. insects / flower head) insects / flower (no. b b c munity function within the aff ected consumer guild. Addi- tion of Rhinocyllus conicus to the fl oral herbivore guild more 0 than doubled aggregate insect densities and was associated F M R FM FR MR FMR with increased levels of seed destruction at both site and Insect guild composition plant scales (Fig. 1, 2). Th e results corroborate recent reviews demonstrating that increased consumer diversity generally Figure 3. Insect densities per fl ower head per plant by insect taxon as a function of insect guild composition (natives: F ϭ Flies and increases consumer community function (Bruno and Cardi- M ϭ moths; invasive weevil: R ϭ R. conicus; and combinations nale 2008, Letourneau et al. 2009). Th e data are consistent thereof). Data represent raw means Ϯ SE for each insect across with patterns predicted from simple abundance eff ects (sensu replicate plants within a guild composition category. Ruesink and Srivastava 2001), with a functionally dominant

90 160 a high degree of resource use overlap with the native taxa, A 140 R. conicus clearly was more functionally eﬃ cient in consuming these shared resources than either native taxon, suggest- 120 ing a lack of complete ‘ functional equivalence ’ (sensu Morin 100 1995), among the insect groups. Th e functional dominance of R. conicus relative to native 80 insects perhaps is not surprising, given that the weevil was purposefully introduced as a biological control to reduce 60 B

Seed production seed production of targeted exotic thistles (Zwö lfer and 40 BC C Harris 1984, Gassmann and Louda 2001). However, it is (no. seeds head) / flower DE D 20 DE E interesting that R. conicus exhibits functional dominance 25 198 106 114 402 185 167 466 relative to the native insects on a native North American 0 thistle with which it has no evolutionary history. Fitness N F M R FM FR MR FMR of phytophagous insects generally declines when attacking Insect guild composition novel host species, relative to their ancient hosts (Bertheau et al. 2010). Further, R. conicus was predicted to have reduced Figure 5. Good (fi lled and undamaged) seed produced per fl ower head per plant in relation to herbivore presence and guild composi- fecundity on non-target native plant species, based on pre- tion (N ϭ none, F ϭ Flies, M ϭ moths, R ϭ R. conicus (invasive release testing (Zw ö lfer and Harris 1984, Gassmann and weevil), and combinations thereof). Data represent raw means Ϯ SE Louda 2001). It is clear from our data that, in contrast to across replicate plants within insect guild composition categories. the expectation of low fi tness should expansion occur onto a Numbers on bars represent the number of plants sampled in each novel thistle species (Zwö lfer and Harris 1984), this invasive guild composition category. Diff erent letters above bars represent insect none the less has become the dominant fl oral herbi- signifi cant diff erences from Tukey HSD test following mixed eff ects vore on native C. canescens . linear models (REML method) with site and year included as ran- Th e eff ects of a species on community function will dom factors and fl ower head diameter and total number of fl ower heads included as covariates (Methods). depend not only on its specifi c functional traits relative to other guild members, but also on the response of the recipi- insect herbivore invading a guild exhibiting limited density ent community to its addition or loss (Ruesink and Srivastava compensation. 2001, Larsen et al. 2005, Suding et al. 2006, Jiang 2007). A high degree of overlap in resource use among the fl oral Invasion by a competitive dominant into an herbivore guild herbivores of Cirsium canescens was not unexpected, since structured by strong competitive interactions should result all insects within this resource guild consume tissues of the in reductions in native herbivores. If so, and in the unlikely developing thistle fl ower heads (Lamp and McCarty 1982, case of perfect density compensation (i.e. equivalent reduc- Gassman and Louda 2001). Th us, not surprisingly, we found tions in native insect densities with increases in invasive no evidence of complementarity among native and exotic insect densities) and complete functional equivalence of the herbivore taxa; neither aggregate insect densities nor levels invader and native species (i.e. similar per capita impacts on of seed destruction in two and three taxon mixtures exceeded resources; Morin 1995), no eff ect on community function levels when R. conicus was the sole attacker on a plant would be predicted. Th is scenario is not consistent with the (Fig. 2). In other words, the results provide no evidence patterns observed, given evidence for a lack of functional of transgressive overyielding in mixtures, a strict test for equivalence between native insects and R. conicus . Alterna- complementarity (Hector et al. 2002). tively, in the face of competitive and functional dominance Rhinocyllus conicus was clearly a functional dominant by the invader, increased herbivore guild function would be within the guild, as evidenced by its high relative densi- predicted even as native herbivore densities decline, via posi- ties, and its high per capita impacts on seed destruction at tive selection eff ects (sensu Hector et al. 2002). Finally, in a low densities (i.e. high functional effi ciency). Comparisons community exhibiting relatively weak competitive interac- of fl oral herbivore density by taxon revealed that R. conicus tions, and so limited density compensation, invasion of the reached more than three-fold higher densities than either of herbivore community would be predicted to have little eff ect the native taxa when it was the sole insect to attack a given on densities of resident herbivores while still resulting in plant (Fig. 3). Similarly, at sites invaded by R. conicus , densi- augmented aggregate insect densities and resource depletion, ties of this weevil were more than twice as high as those of the via simple abundance eff ects (sensu Ruesink and Srivastava two native insect taxa combined (Fig. 1a). At the same time, 2001). Given the evidence for the functional dominance of functional effi ciency of R. conicus was extremely high even at the invader and limited evidence that competitive interactions low densities. For example, with a mean density of only one results in strong negative density compensation at the scales individual per fl ower head, R. conicus destroyed over 85% examined in this study, the data here are most consistent with of potential seeds (Fig. 4). Th e weevil imposed the highest this fi nal scenario. levels of seed damage until densities of about fi ve insects per Competitive interactions among herbivorous insects fl ower head occurred, at which point moths became equally generally are strongest for insects feeding internally on dis- effi cient at destroying seeds. Native insect densities per head crete plant resources (Denno et al. 1995), and thistle-feeding on a per plant basis seldom exceeded an average of fi ve indi- fl oral herbivore communities generally are considered to be viduals (Ͻ 1% of plants for moths, ∼11% of plants for fl ies), competitively structured (Goeden 1974, Zw ö lfer 1988). suggesting that their densities and capacity for seed destruc- Furthermore, previous studies within this system show that tion generally do not rival those of R. conicus . Th us, despite within an individual fl ower head, R. conicus is competitively

91 dominant to the native fl oral insects (Louda and Arnett thistles were sampled within local stands of C. canescens, 2000, Louda et al. 2011). Th us, we initially expected to which tend to be of a similar order of magnitude (Rose et al. fi nd patterns consistent with the invasion of a competitively 2005), and previous work has shown that levels of R. conicus dominant herbivore into a resident herbivore community attack are not related to site level densities of a related native structured by strong competition for resources. Yet, despite thistle (Rand and Louda 2004). Further, grazing diff erences evidence of the weevil’ s numerical and functional domi- among sites are unlikely, since the thistles were surveyed pre- nance, we found limited support for the inference that on a dominantly along ungrazed rangeland edges. Also, previous per plant basis R. conicus acted as a competitive dominant, a studies found little eff ects of climate variables on R. conicus pre-requisite for strict selection eff ects (Hector et al. 2002). densities across the region (Rand and Louda 2006). Th us, Furthermore, the patterns indicate that site-level invasion by diff erences in local stand densities, vegetation structure and R. conicus did not result in exclusion of the native insects. climate variables are unlikely explanations for the patterns In fact, at the site scale, R. conicus invasion led to little if observed. Finally, the fact that the eff ect of R. conicus addi- any reduction in average densities of native herbivore taxa tion on community function and seed production at the site (Fig. 1a). As a consequence, the dominant eff ect of adding scale was very similar to its eff ect at the plant scale, where we this invasive herbivore was to more than double aggregate statistically controlled for diff erences in plant level resource insect densities per plant at a site, a pattern consistent with availability (head size, total head numbers) as well as spa- abundance eff ects. tial and temporal variation (site and year eff ects), suggests At the fi ner per plant scale, patterns were consistent with that the inference of a causal role of R. conicus in generating some degree of interspecifi c competition among insects for diff erences in herbivore community function and impact is R. conicus and moths (Fig. 3). Average densities per plant likely highly robust. of both weevils and moths decreased signifi cantly and con- Th ree factors have been suggested to be important in sistently when they occurred in two- and three-taxon mix- determining the impact of an invasive species on native tures, compared to when each was the sole taxon attacking populations and communities: its range, its abundance, and a plant (i.e. insects occurred in ‘ monoculture ’ ). However, we its per capita eff ects (Parker et al. 1999). Rhinocyllus conicus found no evidence of competitive dominance by the invasive is predicted to be an important invader by all three criteria. species over the natives. Weevils declined to a greater extent First, it was present at 90% of the sites sampled in this study, than moths across the gradient in taxon richness. Further- consistent with previous work suggesting it uses C. cane- more, fl y densities did not signifi cantly diff er, a pattern scens across the majority of its midgrass distributional range inconsistent with strong competition on a per plant basis. (Rand and Louda 2006). Second, R. conicus abundance was Th is result was unexpected, given experimental evidence of high relative to that of the native insects (e.g. Fig. 1a, 3). strong competitive interactions between R. conicus and the Th ird, the data suggest that R. conicus has a higher per cap- tephritid fl ies within individual thistle fl ower heads (Louda ita eff ect on seed destruction than the native species at the and Arnett 2000, Louda et al. 2011). Under conditions densities typically observed (e.g. Fig. 4). Th e combination of where fl ower head resources are not limiting, competition on high abundance and high per capita impact likely underlies a per plant level would be minimized if insects avoid fl ower the dominant eff ect of this invasive weevil on levels of total heads that are infested by potential competitors and, given seed destruction, which in turn resulted in a strong negative recent evidence for such ovipositional avoidance (Louda impact on thistle seed production. Th e production of good et al. 2011), may in part explain the discrepancy in results seed by plants at sites invaded by R. conicus was half of that between studies at diff erent scales. In sum, competitive inter- by plants at uninvaded sites. Similarly, plants with R. conicus actions clearly occur, but at the scales examined here, they present always exhibited signifi cantly lower seed production do not appear to be suffi ciently strong to result in negative compared with plants attacked by native insects only. Th us, density compensation within the fl oral guild on C. canescens . the survey data suggest that the dominant eff ect of R. conicus In other words, competitive interactions do not result in an addition to the fl oral herbivore guild is a reduction in the equivalent decline in native insect densities with increases in reproductive performance of the native thistle. Previous work R. conicus density following its addition to the fl oral guild. has shown that C. canescens lifetime fi tness and population As a consequence, R. conicus addition was associated with an sizes are seed limited (Louda and Potvin 1995), and that fl oral augmentation of two key community functional attributes: herbivores increasingly limit C. canescens population growth aggregate insect density and levels of resource depletion. at two long term study sites post-R. conicus invasion (Rose Furthermore, the patterns suggest that even if R. conicus et al. 2005). Our results signifi cantly expand on this work, competitively suppressed densities of native herbivores on and support inferences of prior geographic analysis (Rand and C. canescens to near zero, overall fl oral herbivore community Louda 2006), by showing that R. conicus impacts C. canescens function would still exceed pre-invasion levels, due to the seed production, and so potential population growth, across weevil ’ s numerical and functional dominance. the heart of its global geographic distribution. Since these data are observational, it is important to In this study, we examined within guild interactions consider other variables that may co-vary with presence or in a relative simple community, made up of three insect absence of R. conicus and, so, potentially infl uence the inter- taxa attacking a single thistle species. Mooney et al. (1996) pretation of observed patterns. In particular, large diff erences argue that gain or loss of a species will have its greatest in total resource availability among sites could infl uence pat- impact on function when there are few species in the com- terns of invasion, given that herbivorous insects often con- munity, when the species is a dominant, and when the spe- centrate in areas of high host plant abundance or density cies diff ers greatly from others in the community. Th us, (Root 1973). However, this is unlikely in this system since while the low diversity of herbivores examined in our study

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