Inconsistent annual compensation for floral herbivory by an iterocarpic thistle.

PREMISE: Plants experiencing steep reproductive losses from herbivores should favor strategies promoting tolerance or resistance to that herbivory. However, the degree to which such strategies succeed in improving plant fitness under natural conditions needs further evaluation, especially for iterocarpic species. We tested whether reproductive effort by the iterocarpic Cirsium undulatum Spreng. (Wavyleaf thistle) provided within-season tolerance for floral herbivory through response to apical damage. METHODS: We imposed apical damage and manipulated floral herbivory on later-flowering, non-apical flowerheads for two seasons. We asked: (1) is there evidence of compensatory potential to tolerate apical flowerhead damage? If so, (2) does the amount of herbivore pressure on non-apical flowerheads influence the magnitude of any compensatory response; and (3) is the response to apical damage sufficient to increase plant seed production under ambient floral herbivory over the flowering season? RESULTS: Plants showed compensatory potential for apical head loss; apical damage increased seed contributions from later, lower positioned flowerheads. Further, the intensity of subsequent herbivore pressure influenced compensation outcomes. Equitable seed production under both levels of ambient herbivory occurred only in the year in which plants were larger and insect pressure was lower. Finally, the response to apical damage was sufficient to compensate for apical seed loss, but it did not consistently increase overall annual seed production under ambient floral herbivory. CONCLUSIONS: Although this iterocarpic species can compensate for apical damage, tolerance for floral herbivory varied between years.

Post-dispersal factors influence recruitment patterns but do not override the importance of seed limitation in populations of a native thistle.

Whether plant populations are limited by seed or microsite availability is a long-standing debate. However, since both can be important, increasing emphasis is placed on disentangling their relative importance and how they vary through space and time. Although uncommon, seed addition studies that include multiple levels of seed augmentation, and follow plants through to the adult stage, are critical to achieving this goal. Such data are also vital to understanding when biotic pressures, such as herbivory, influence plant abundance. In this study, we experimentally added seeds of a native thistle, Cirsium canescens, at four augmentation densities to plots at two long-term study sites and quantified densities of seedlings and reproductive adults over 9 years. Recruitment to both seedling and adult stages was strongly seed-limited at both sites; however, the relative strength of seed limitation decreased with plant age. Fitting alternative recruitment functions to our data indicated that post-dispersal mortality factors were important as well. Strong density-dependent mortality limited recruitment at one site, while density-independent limitation predominated at the other. Overall, our experimental seed addition demonstrates that the environment at these sites remains suitable for C. canescens survival to reproduction and that seed availability limits adult densities. The results thus provide support for the hypothesis that seed losses due to the invasive weevil, Rhinocyllus conicus, rather than shifting microsite conditions, are driving C. canescens population declines. Shifts in the importance of density-dependent recruitment limitation between sites highlights that alternate strategies may be necessary to recover plant populations at different locations.

Cumulative herbivory outpaces compensation for early floral damage on a monocarpic perennial thistle.

Floral herbivory represents a major threat to plant reproductive success, driving the importance of plant tolerance mechanisms that minimize fitness costs. However, the cumulative insect herbivory plants experience under natural conditions complicates predictions about tolerance contributions to net fitness. Apical damage can lead to compensatory seed production from late season flowering that ameliorates early season fitness losses. Yet, the compensation realized depends on successful development and herbivore escape by later season flowers. Using monocarpic perennial Cirsium canescens, we quantified seed-reproductive fitness of plants with vs. without experimental damage to the early-developing large apical flower head, with and without a 30-40% herbivory reduction on subsequent flower heads, for two flowering cohorts. Plants with reduced herbivory clearly demonstrated the release of apical dominance and compensation, not overcompensation, for apical damage via greater seed maturation by later flower heads. In contrast, plants that experienced ambient herbivory levels on subsequent heads undercompensated for early apical damage. Individuals had lower total seed set when the apical head was damaged. Compensation was, therefore, possible through a small increase in total flower heads, caused by a higher rate of floral bud survival, and a higher seed maturation rate by subsequent heads, leading to more viable seeds per matured flower head. With ambient cumulative floral herbivory, compensation for apical damage was not sufficient to improve fitness. Variation in the intensity of biological interactions played a role in the success of plant tolerance as a mechanism to maximize individual fitness.

Native insect herbivory overwhelms context dependence to limit complex invasion dynamics of exotic weeds.

Understanding the role of consumers in density-dependent plant population dynamics is a long-standing goal in ecology. However, the generality of herbivory effects across heterogeneous landscapes is poorly understood due to the pervasive influence of context-dependence. We tested effects of native insect herbivory on the population dynamics of an exotic thistle, Cirsium vulgare, in a field experiment replicated across eight sites in eastern Nebraska. Using hierarchical Bayesian analysis and density-dependent population models, we found potential for explosive low-density population growth (λ > 5) and complex density fluctuations under herbivore exclusion. However, herbivore access drove population decline (λ < 1), suppressing complex fluctuations. While plant-herbivore interaction outcomes are famously context-dependent, we demonstrated that herbivores suppress potentially invasive populations throughout our study region, and this qualitative outcome is insensitive to environmental context. Our novel use of Bayesian demographic modelling shows that native insect herbivores consistently prevent hard-to-predict fluctuations of weeds in environments otherwise susceptible to invasion.

Native insect herbivory limits population growth rate of a non-native thistle.

The influence of native fauna on non-native plant population growth, size, and distribution is not well documented. Previous studies have shown that native insects associated with tall thistle (Cirsium altissimum) also feed on the leaves, stems, and flower heads of the Eurasian congener C. vulgare, thus limiting individual plant performance. In this study, we tested the effects of insect herbivores on the population growth rate of C. vulgare. We experimentally initiated invasions by adding seeds at four unoccupied grassland sites in eastern Nebraska, USA, and recorded plant establishment, survival, and reproduction. Cumulative foliage and floral herbivory reduced C. vulgare seedling density, and prevented almost any reproduction by C. vulgare in half the sites. The matrix model we constructed showed that this herbivory resulted in a reduction of the asymptotic population growth rate (λ), from an 88% annual increase to a 54% annual decline. These results provide strong support for the hypothesis that indigenous herbivores limit population invasion of this non-native plant species into otherwise suitable grassland habitat.

Insect herbivory and propagule pressure influence Cirsium vulgare invasiveness across the landscape.

A current challenge in ecology is to better understand the magnitude, variation, and interaction in the factors that limit the invasiveness of exotic species. We conducted a factorial experiment involving herbivore manipulation (insecticide-in-water vs. water-only control) and seven densities of introduced nonnative Cirsium vulgare (bull thistle) seed. The experiment was repeated with two seed cohorts at eight grassland sites uninvaded by C. vulgare in the central Great Plains, USA. Herbivory by native insects significantly reduced thistle seedling density, causing the largest reductions in density at the highest propagule inputs. The magnitude of this herbivore effect varied widely among sites and between cohort years. The combination of herbivory and lower propagule pressure increased the rate at which new C. vulgare populations failed to establish during the initial stages of invasion. This experiment demonstrates that the interaction between biotic resistance by native insects, propagule pressure, and spatiotemporal variation in their effects were crucial to the initial invasion by this Eurasian plant in the western tallgrass prairie.

Combined effects of plant competition and insect herbivory hinder invasiveness of an introduced thistle.

The biotic resistance hypothesis is a dominant paradigm for why some introduced species fail to become invasive in novel environments. However, predictions of this hypothesis require further empirical field tests. Here, we focus on evaluating two biotic factors known to severely limit plants, interspecific competition and insect herbivory, as mechanisms of biotic resistance. We experimentally evaluated the independent and combined effects of three levels of competition by tallgrass prairie vegetation and two levels of herbivory by native insects on seedling regeneration, size, and subsequent flowering of the Eurasian Cirsium vulgare, a known invasive species elsewhere, and compared its responses to those of the ecologically similar and co-occurring native congener C. altissimum. Seedling emergence of C. vulgare was greater than that of C. altissimum, and that emergence was reduced by the highest level of interspecific competition. Insect leaf herbivory was also greater on C. vulgare than on C. altissimum at all levels of competition. Herbivory on seedlings dramatically decreased the proportion of C. vulgare producing flower heads at all competition levels, but especially at the high competition level. Competition and herbivory interacted to significantly decrease plant survival and biomass, especially for C. vulgare. Thus, both competition and herbivory limited regeneration of both thistles, but their effects on seedling emergence, survival, size and subsequent reproduction were greater for C. vulgare than for C. altissimum. These results help explain the unexpectedly low abundance recorded for C. vulgare in western tallgrass prairie, and also provide strong support for the biotic resistance hypothesis.

Seed availability and insect herbivory limit recruitment and adult density of native tall thistle.

Understanding spatial and temporal variation in factors influencing plant regeneration is critical to predicting plant population growth. We experimentally evaluated seed limitation, insect herbivory, and their interaction in the regeneration and density of tall thistle (Cirsium altissimum) across a topographic ecosystem productivity gradient in tallgrass prairie over two years. On ridges and in valleys, we used a factorial experiment manipulating seed availability and insect herbivory to quantify effects of: seed input on seedling density, insect herbivory on juvenile density, and cumulative impacts of both seed input and herbivory on reproductive adult density. Seed addition increased seedling densities at three of five sites in 2006 and all five sites in 2007. Insect herbivory reduced seedling survival across all sites in both years, as well as rosette survival from the previous year's seedlings. In both years, insecticide treatment of seed addition plots led to greater adult tall thistle densities in the following year, reflecting the increase in juvenile thistle densities in the experimental year. Seedling survival was not density dependent. Our analytical projection model predicts a significant long-term increase in adult densities from seed input, with a greater increase under experimentally reduced insect herbivory. While plant community biomass and water stress varied significantly between ridges and valleys, the effects of seed addition and insect herbivory did not vary with gradient position. These results support conceptual models that predict seedling and adult densities of short-lived monocarpic perennial plants should be seed limited. Further, the experiment demonstrates that even at high juvenile plant densities, at which density dependence potentially could have overridden herbivore effects on plant survival, insect herbivory strongly affected juvenile thistle performance and adult densities of this native prairie species.

No interaction between competition and herbivory in limiting introduced Cirsium vulgare rosette growth and reproduction.

Both competition and herbivory have been shown to reduce plant survival, growth, and reproduction. Much less is known about whether competition and herbivory interact in determining plant performance, especially for introduced, weedy plant species in the invaded habitat. We simultaneously evaluated both the main and interactive effects of plant neighbors and insect herbivory on rosette growth and seed reproduction in the year of flowering for Cirsium vulgare (bull thistle, spear thistle), an introduced Eurasian species, in tallgrass prairie in 2 years. Effects of insect herbivory were strong and consistent in both years, causing reduced plant growth and seed production, whereas the effects of competition with established vegetation were weak. The amount of herbivore damage inflicted on rosettes did not depend on the presence of neighbor plants. We also found no interaction between competition and herbivory on key parameters of plant growth and fitness. The results of this study contradict the hypothesis that competitive context interacts with insect herbivory in limiting the invasiveness of this introduced thistle. Further, the results provide additional, experimental evidence that high levels of herbivory on established rosettes by native insects exert significant biotic resistance to the invasiveness of C. vulgare in western tallgrass prairie.

Occurrence of Trichosirocalus horridus (Coleoptera: Curculionidae) on native Cirsium altissimum versus exotic C. vulgare in North American tallgrass prairie.

Postrelease studies can provide data with which to evaluate expectations based on prerelease tests of biological control insects. In 2004, we observed Trichosirocalus horridus Panzer (Coleoptera: Curculionidae), the rosette weevil introduced into North America against Eurasian thistles, feeding on native tall thistle, Cirsium altissimum L. Spreng., in tallgrass prairie. In this study, we examined the rosette weevil's use of tall thistle, compared with its use of the co-occurring exotic bull thistle, C. vulgare (Savi) Tenore. For both thistle species, we quantified weevil frequency, abundance, and seasonal variation in incidence, using both timed observations at two sites over two growing seasons (2004, 2005) and dissections of thistle flowering shoots from 13 sites (2005). Based on prerelease information, we expected the Eurasian thistle to be the quantitatively preferred host plant for this Eurasian weevil. Instead, we found that both the frequency of infestation and the mean number of adult rosette weevils per plant were at least as high, and sometimes higher, on the native thistle as on the exotic thistle. Furthermore, adult weevil phenology coincided on the two host species. This study provides new quantitative evidence of nontarget feeding by another weevil released for thistle biological control; and it raises important questions for further research. We conclude that continued new releases, as well as augmentation of existing populations, of T. horridus should wait until more research is done on the impact of the nontarget occurrence now reported for this biological control insect.

Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant.

Plant reproduction yields immediate fitness benefits but can be costly in terms of survival, growth, and future fecundity. Life-history theory posits that reproductive strategies are shaped by trade-offs between current and future fitness that result from these direct costs of reproduction. Plant reproduction may also incur indirect ecological costs if it increases susceptibility to herbivores. Yet ecological costs of reproduction have received little empirical attention and remain poorly integrated into life-history theory. Here, we provide evidence for herbivore-mediated ecological costs of reproduction, and we develop theory to examine how these costs influence plant life-history strategies. Field experiments with an iteroparous cactus (Opuntia imbricata) indicated that greater reproductive effort (proportion of meristems allocated to reproduction) led to greater attack by a cactus-feeding insect (Narnia pallidicornis) and that damage by this herbivore reduced reproductive success. A dynamic programming model predicted strongly divergent optimal reproductive strategies when ecological costs were included, compared with when these costs were ignored. Meristem allocation by cacti in the field matched the optimal strategy expected under ecological costs of reproduction. The results indicate that plant reproductive allocation can strongly influence the intensity of interactions with herbivores and that associated ecological costs can play an important selective role in the evolution of plant life histories.

Variation in herbivore-mediated indirect effects of an invasive plant on a native plant.

Theory predicts that damage by a shared herbivore to a secondary host plant species may either be higher or lower in the vicinity of a preferred host plant species. To evaluate the importance of ecological factors, such as host plant proximity and density, in determining the direction and strength of such herbivore-mediated indirect effects, we quantified oviposition by the exotic weevil Rhinocyllus conicus on the native wavyleaf thistle Cirsium undulatum in midgrass prairie on loam soils in the upper Great Plains, USA. Over three years (2001-2003), the number of eggs laid by R. conicus on C. undulatum always decreased significantly with distance (0-220 m) from a musk thistle (Carduus nutans L.) patch. Neither the level of R. conicus oviposition on C. undulatum nor the strength of the distance effect was predicted by local musk thistle patch density or by local C. undulatum density (<5 m). The results suggest that high R. conicus egg loads on C. undulatum near musk thistle resulted from the native thistle's co-occurrence with the coevolved preferred exotic host plant and not from the weevil's response to local host plant density. Mean egg loads on C. undulatum also were greater at sites with higher R. conicus densities. We conclude that both preferred-plant proximity and shared herbivore density strongly affected the herbivore-mediated indirect interaction, suggesting that such interactions are important pathways by which invasive exotic weeds can indirectly impact native plants.

Plant reproductive allocation predicts herbivore dynamics across spatial and temporal scales.

Life-history theory suggests that iteroparous plants should be flexible in their allocation of resources toward growth and reproduction. Such plasticity could have consequences for herbivores that prefer or specialize on vegetative versus reproductive structures. To test this prediction, we studied the response of the cactus bug (Narnia pallidicornis) to meristem allocation by tree cholla cactus (Opuntia imbricata). We evaluated the explanatory power of demographic models that incorporated variation in cactus relative reproductive effort (RRE; the proportion of meristems allocated toward reproduction). Field data provided strong support for a single model that defined herbivore fecundity as a time-varying, increasing function of host RRE. High-RRE plants were predicted to support larger insect populations, and this effect was strongest late in the season. Independent field data provided strong support for these qualitative predictions and suggested that plant allocation effects extend across temporal and spatial scales. Specifically, late-season insect abundance was positively associated with interannual changes in cactus RRE over 3 years. Spatial variation in insect abundance was correlated with variation in RRE among five cactus populations across New Mexico. We conclude that plant allocation can be a critical component of resource quality for insect herbivores and, thus, an important mechanism underlying variation in herbivore abundance across time and space.

Invasive insect abundance varies across the biogeographic distribution of a native host plant.

Studies of biogeographic variation in species abundances are fundamental to understanding and predicting the impacts of invasive exotic species. We quantified the abundance of the introduced and now invasive biocontrol weevil, Rhinocyllus conicus, on a newly adopted native host plant, Cirsium canescens (Platte thistle), across the plant's distributional range. We used regression and structural equation analyses to examine variation in weevil abundance at 92-108 sites over three years in relation to variation in abiotic and biotic parameters hypothesized to be important in insect or plant dynamics and distribution. We found that R. conicus now occurs throughout the majority of the range of C. canescens, even in the center of the native plant's distribution where its coevolved, targeted weed host (Carduus nutans, musk thistle) is absent. In fact, weevil densities were greater in the center of the native plant's distribution in the Sand Hills formation than in peripheral sand patches closer to areas where the targeted 'exotic thistle is common. None of the macroclimatic variables examined were consistent predictors of the large-scale variation in weevil abundance on C. canescens. In addition to biogeographic position, the only other consistent predictor of weevil densities across sites was the number of flower heads per C. canescens plant. These results exclude the "spillover" hypothesis to explain nontarget feeding on this newly adopted native host species. Instead, the results are consistent with the alternative hypothesis that exotic weevil abundance on C. canescens is related to the local availability of native floral resources. Because C. canescens densities have declined with increases in R. conicus at sites central in the plant's distribution, these results suggest that isolated, peripheral populations of C. canescens are likely to be critical for persistence of Platte thistle. More generally, this study suggests that the persistence of a native species that is impacted by an exotic natural enemy may require preservation of populations in habitats outside the optimal portion of the native species' distribution.

Inflorescence spiders: A cost/benefit analysis for the host plant, Haplopappus venetus Blake (Asteraceae).

Predators on flower visitors, such as spiders, could influence plant reproduction by determining the balance between pollination and seed predation by insects. This study examines the net effect of predation by the inflorescence spider, Peucetia viridans (Hentz), for seed production by a native plant species on which it hunts. Both pollination and seed set of Haplopappus venetus (Asteraceae) were reduced on branches with spiders; however, the release of viable, undamaged seed was higher on inflorescence branches with spiders than on those without. Occurrence of P. viridans was associated with the flat-topped inflorescence branch structure characteristic of H. venetus rather than with the vertical structure of its congener, H. squarrosus. Thus, the interaction should be a reinforcing selective pressure on inflorescence branch morphology of H. venetus over time. Two factors providing constraints on the degree and rate of coevolution of the plant-spider interaction are suggested by the results: (1) the critical role of phenological synchrony and (2) the opposing requirements of interacting species and of subsequent life history stages within a species.

Indirect versus direct effects of grasses on growth of a cactus (Opuntia fragilis): insect herbivory versus competition.

Variation in plant performance between microhabitats is usually attributed to direct mechanisms, such as plant physiological tolerances or competitive interactions. However, indirect mechanisms, such as differences in herbivore pressure mediated by microhabitat differences, could create the same pattern of variation. In this study, we investigated the effect of insect herbivore pressure on the growth of the grassland cactus Opuntia fragilis under different regimes of grassland canopy cover. Our purpose was to establish the extent to which canopy cover plays a direct, competitive role versus an indirect, mediatory role in cactus growth. We manipulated aboveground microhabitat, specifically the cover of adjacent grasses. The three treatments were: (1) open canopy, with grass pinned down away from the cactus; (2) shaded canopy, with a partial mesh cage staked over the cactus; and (3) ambient grass canopy. We measured seasonal plant growth and recorded changes in insect herbivore occurrence and damage in relation to cover. Cactus growth, defined as the change in number of live cladodes, was higher in the open than under either treatment where the plant was more shaded (P<0.05). However, allocation to new growth, measured as the proportion of new segments (cladodes) in a patch, did not differ among cover treatments. Thus, the hypothesis that physiological constraints, or competition for light, limited cactus performance in grass is rejected. Instead, we found that both cladode mortality, caused by the larvae of a cactus moth borer (Melitara dentata), and occurrence of the moth were lower in the open microhabitat than in either shaded microhabitat. Thus, higher net growth in the open, unshaded treatment, rather than representing a release from competition for light with grasses, was better explained as an indirect effect of grass cover on the activity and impact of the cactus moth. These results show that indirect effects can lead to a misinterpretation of experimental data on direct effects. These data also contribute to an improved understanding of mixed results in the biological control of weedy cacti. Clearly, future evaluations of the relative importance of physiology, competition, and insect herbivory in plant performance must be environmentally explicit.

Spillover of agriculturally subsidized predators as a potential threat to native insect herbivores in fragmented landscapes.

Habitat loss and fragmentation can have strong negative impacts on populations of some native species. Spillover of generalist natural enemies from the surrounding landscape matrix is one mechanism potentially generating such effects, yet this has been rarely studied in insects. We examined the influence of habitat conversion to agriculture on the abundance and potential effects of predatory coccinellid beetles on native insect herbivores within 12 grassland remnants in central Nebraska (U.S.A.). Results of sweep sampling revealed that coccinellids were three to six times more abundant at native grassland sites embedded within cropland-dominated landscapes compared with control sites in grassland-dominated landscapes over the 3 years of the study. Exclusion experiments further demonstrated that predation intensity was strongly related to coccinellid abundances across sites and that coccinellids can dramatically reduce densities of a native aphid herbivore. In contrast to studies of specialized insect parasitoids, which have generally found reduced enemy pressure in fragmented landscapes, our results suggest that native herbivores may in some cases experience increased consumer pressure in landscapes with increasing habitat loss because of spillover of generalist predators from surrounding cropland habitats.

Indirect interaction between two native thistles mediated by an invasive exotic floral herbivore.

Spatial and temporal variation in insect floral herbivory is common and often important. Yet, the determinants of such variation remain incompletely understood. Using 12 years of flowering data and 4 years of biweekly insect counts, we evaluated four hypotheses to explain variation in damage by the Eurasian flower head weevil, Rhinocyllus conicus, to the native North American wavyleaf thistle, Cirsium undulatum. The four factors hypothesized to influence weevil impact were variations in climate, weevil abundance, phenological synchrony, and number of flower heads available, either on wavyleaf thistle or on the other cooccurring, acquired native host plant (Platte thistle, Cirsium canescens), or on both. Climate did not contribute significantly to an explanation of variation in R. conicus damage to wavyleaf thistle. However, climate did influence weevil synchrony with wavyleaf flower head initiation, and phenological synchrony was important in determining R. conicus oviposition levels on wavyleaf thistle. The earlier R. conicus was active, the less it oviposited on wavyleaf thistle, even when weevils were abundant. Neither weevil abundance nor availability of wavyleaf flower heads predicted R. conicus egg load. Instead, the strongest predictor of R. conicus egg load on wavyleaf thistle was the availability of flower heads on Platte thistle, the more common, earlier flowering native thistle in the sand prairie. Egg load on wavyleaf thistle decreased as the number of Platte thistle flower heads at a site increased. Thus, wavyleaf thistle experienced associational defense in the presence of flowering by its now declining native congener, Platte thistle. These results demonstrate that prediction of damage to a native plant by an exotic insect may require knowledge of both likely phenological synchrony and total resource availability to the herbivore, including resources provided by other nontarget native species.

Phenological synchrony affects interaction strength of an exotic weevil with Platte thistle, a native host plant.

Phenological synchrony of a consumer population with its resource populations is expected to affect interaction intensity. We quantified phenological variation and synchrony of populations of an invasive Eurasian flower head weevil, Rhinocyllus conicus, that consumes florets, ovules, and seeds of developing flower heads of a native North American thistle, Cirsium canescens, in Sand Hills prairie in Nebraska, USA. Variation in timing of adult activity among weevil populations was larger than variation in timing of flower head development among C. canescens populations, and it drove the observed variation in the phenological synchrony between weevil and host plant populations. Furthermore, the degree of phenological synchrony between populations was significant in explaining variation in weevil egg load on the newly acquired host plant. Because population growth of C. canescens is limited by predispersal seed losses to floral herbivores, variation in the synchrony of herbivore and plant flowering will affect the density of the plant population. These results provide strong quantitative support for the hypothesis that the synchrony of insect activity with plant resources can determine the magnitude of impact of floral herbivores on their host plant populations.