Biological control of Rhamnus cathartica: is it feasible? A review of work done in 2002–2012

Rhamnus cathartica (common buckthorn) is a shrub (or small tree) of Eurasian origin, which has become invasive in North America. Internal feeders and sap suckers were prioritized for biological control from over 30 specialized insects identified from the target plant in its native European range. Five leaf‐feeding moths were also considered for further investigations. Field observations and preliminary host range tests with the stem‐boring beetle Oberea pedemontana, the root‐boring moth Synanthedon stomoxiformis, the shoot‐tip‐boring moth Sorhagenia janiszewskae and the leaf‐feeding moths Ancylis apicella, A. unculana, Triphosa dubitata, Philereme transversata and P. vetulata confirmed that all of these species were lacking host specificity in no‐choice conditions. Choice oviposition tests carried out with most of the prioritized species to assess their ecological host range yielded unreliable results. Three psyllids, Trichochermes walkeri, Cacopsylla rhamnicolla and Trioza rhamni are promising in terms of host specificity, but are infected with the plant disease ‘Candidatus Phytoplasma rhamni’. Fruit‐ or seed‐feeding insects may present the best potential for biological control of buckthorn in directly reducing seed set and thus seedling establishment. However, it was not possible to obtain adult fruiting trees of native North American Rhamnus species for testing. It is concluded that there are no promising arthropod agents based on what is known to date. Pathogens could offer new opportunities for biological control of R. cathartica in North America.     

Processes regulating the invasion of European buckthorn (Rhamnus cathartica) in three habitats of the northeastern United States

Invasion by exotic plants often is restricted by processes, such as seed predation, acting on early life-history stages; however, the relative importance of these processes might vary among habitats. Modern human land use has created a mosaic of habitats in many landscapes, including the landscape of the northeastern United States. European buckthorn (Rhamnus cathartica) is an exotic plant that has achieved varying success in North American habitats. We studied dispersal, seed survival, germination, and seedling survival of buckthorn populations at four plots in each of sugar maple (Acer saccharum) forests, old fields, and abandoned conifer plantations in central New York State. Dispersal was low in maple forests, as evidenced by low collection rates of R. cathartica seeds in seed traps. Rates of post-dispersal seed predation were highest in maple forests and lowest in old fields, suggesting greater use of maple forests by granivorous rodents. Germination rates did not vary among seeds planted in soils of these habitats when studied in the laboratory despite differences in soil pH. Survival of transplanted seedlings was low in maple forests relative to old fields and plantations. Buckthorn invasion of old fields and abandoned plantations was not strongly constrained by factors we considered, and the buckthorn populations in these habitats were large. A combination of low dispersal by frugivores, low seed survival due to predation, and low seedling survival due to dim light conditions apparently prevents R. cathartica from invasion of intact maple forests of our area. Native fauna and canopy closure may act synergistically to reduce success of invasive plants in natural habitats.     

Removal of invasive shrubs reduces exotic earthworm populations

Invasive species are a leading threat to native ecosystems, and research regarding their effective control is at the forefront of applied ecology. Exotic facilitation has been credited with advancing the success of several aggressive invasive species. Here, we suggest using the knowledge of exotic facilitations to control invasive earthworm populations. In northern hardwood forests, the invasive shrubs Rhamnus cathartica (buckthorn) and Lonicera x bella (honeysuckle) produce high quality leaf litter, and their abundance is positively correlated with exotic earthworms, which increase nutrient cycling rates. We performed an invasive plant removal experiment in two northern hardwood forest stands, one dominated by buckthorn and the other by honeysuckle. Removal of invasive shrubs reduced exotic earthworm populations by roughly 50% for the following 3 years. By targeting invasive species that are part of positive feedback loops, land managers can multiply the positive effects of invasive species removal.     

A window of opportunity: Subdominant predators can use suboptimal prey

Introduced species have been linked to declines of native species through mechanisms including intraguild predation and exploitative competition. However, coexistence among species may be promoted by niche partitioning if native species can use resources that the invasive species cannot. Previous research has shown that some strains of the aphid Aphis craccivora are toxic to a competitively dominant invasive lady beetle, Harmonia axyridis. Our objective was to investigate whether these aphids might be an exploitable resource for other, subdominant, lady beetle species. We compared larval development rate, survival, and adult weight of five lady beetle species in no‐choice experiments with two different strains of A. craccivora, one of which is toxic to H. axyridis and one that is nontoxic. Two lady beetle species, Cycloneda munda and Coleomegilla maculata, were able to complete larval development when feeding on the aphid strain that is toxic to H. axyridis, experiencing only slight developmental delays relative to beetles feeding on the other aphid strain. One species, Coccinella septempunctata, also was able to complete larval development, but experienced a slight reduction in adult weight. The other two lady beetle species, Hippodamia convergens and Anatis labiculata, demonstrated generally low survivorship when consuming A. craccivora, regardless of aphid strain. All five species showed increased survival and/or development relative to H. axyridis on the “toxic” aphid strain. Our results suggest that this toxic trait may act as a narrow‐spectrum defense for the aphids, providing protection against only some lady beetle enemies. For other less‐susceptible lady beetles, these aphids have the potential to provide competitive release from the otherwise dominant H. axyridis.     

Strong feeding preference of an exotic generalist herbivore for an exotic forb: a case of invasional antagonism

Many hypotheses dealing with the success of invasive plant species concern plant–herbivore interactions. The invasional meltdown and enemy inversion hypotheses suggest that non-native herbivores may indirectly facilitate the invasion of a non-native plant species by either favorably changing environmental conditions or reducing competition from native plant species. Our objective was to determine the role of herbivory by the non-native snail Otala lactea in structuring California grassland communities. We conducted two experiments to examine the feeding preferences of O. lactea for eight representative grassland species. Overall, O. lactea preferred Brassica nigra, a non-native forb, over all other species tested. Field monocultures of B. nigra supported significantly higher snail densities than monocultures of any of the other species tested. O. lactea also preferred B. nigra over all other species tested in controlled laboratory feeding trials. However, based on trait comparisons of each of the eight grassland species, we cannot pinpoint the preference for B. nigra to a basic nutritional requirement on the part of the herbivore or an allocation to defense on the part of the plants. Our study provides evidence for an antagonistic relationship between a non-native herbivore and a non-native plant species in their invasive range. We term this relationship “invasional antagonism”.     

Modelling the spread of European buckthorn in the Region of Waterloo

Established invasive species, such as European buckthorn (Rhamnus cathartica), pose a challenging problem for land managers who must decide when and how to control them. In order to make an informed decision land managers need to be able to predict the spread of these invasive species at local scales and without the need for excessive sampling. Our approach uses a hybrid model, combining habitat suitability and the presence of the invasive in neighbouring cells to predict the probability of a cell being invaded over time. A generalized linear mixed-effects model was used to create a habitat suitability model and a spread model. The habitat suitability model predicts the presence of buckthorn based on environmental characteristics and the results are used in the spread model. The spread model indicates that the invasion of buckthorn is influenced by the suitability of habitat and the presence of buckthorn in neighbouring cells. The success of the spread model suggests that this approach can be used to create a spatiotemporally explicit model with limited sampling effort.     

Positive interactions among plant species for pollinator service: assessing the ‘magnet species’ concept with invasive species

Plants with poorly attractive flowers or with little floral rewards may have inadequate pollinator service, which in turn reduces seed output. However, pollinator service of less attractive species could be enhanced when they are associated with species with highly attractive flowers (so called ‘magnet‐species’). Although several studies have reported the magnet species effect, few of them have evaluated whether this positive interaction result in an enhancement of the seed output for the beneficiary species. Here, we compared pollinator visitation rates and seed output of the invasive annual species Carduus pycnocephalus when grow associated with shrubs of the invasive Lupinus arboreus and when grow alone, and hypothesized that L. arboreus acts as a magnet species for C. pycnocephalus. Results showed that C. pycnocephalus individuals associated with L. arboreus had higher pollinator visitation rates and higher seed output than individuals growing alone. The higher visitation rates of C. pycnocephalus associated to L. arboreus were maintained after accounting for flower density, which consistently supports our hypothesis on the magnet species effect of L. arboreus. Given that both species are invasives, the facilitated pollination and reproduction of C. pycnocephalus by L. arboreus could promote its naturalization in the community, suggesting a synergistic invasional process contributing to an ‘invasional meltdown’. The magnet effect of Lupinus on Carduus found in this study seems to be one the first examples of indirect facilitative interactions via increased pollination among invasive species.     

Rhizobial hitchhikers from Down Under: invasional meltdown in a plant–bacteria mutualism?

Aim This study analysed the diversity and identity of the rhizobial symbionts of co‐existing exotic and native legumes in a coastal dune ecosystem invaded by Acacia longifolia. Location An invaded coastal dune ecosystem in Portugal and reference bradyrhizobial strains from the Iberian Peninsula and other locations. Methods Symbiotic nitrogen‐fixing bacteria were isolated from root nodules of plants of the Australian invasive Acacia longifolia and the European natives Cytisus grandiflorus, Cytisus scoparius and Ulex europaeus. Total DNA of each isolate was amplified by polymerase chain reaction (PCR) with the primer BOX A1R. Subsequent PCR‐sequencing and phylogenetic analyses of the internal transcribed spacer region and the nifD and nodA genes were performed for all different strains. Results The four plant species analysed were nodulated by bacteria from three different Bradyrhizobium lineages, although most of the isolates belonged to the Bradyrhizobium japonicum lineage sensu lato. Ninety‐five per cent of the bradyrhizobia isolated from A. longifolia, C. grandiflorus and U. europaeus in the invaded ecosystem had nifD and nodA genes of Australian origin. Seven isolates obtained in this study define a new distinctive nifD group of Bradyrhizobium from western and Mediterranean Europe. Main conclusions These results reveal the introduction of exotic bacteria with the invasive plant species, their persistence in the new geographical area and the nodulation of native legumes by rhizobia containing exotic symbiotic genes. The disruption of native mutualisms and the mutual facilitation of the invasive spread of the introduced plant and bradyrhizobia could constitute the first report of an invasional meltdown documented for a plant–bacteria mutualism.     

Above‐ and Belowground Impacts of European Buckthorn (Rhamnus cathartica) on Four Native Forbs

Fast‐growing European buckthorn (Rhamnus cathartica) shrubs are aggressively invading woodlands in eastern and midwestern North America. Buckthorn casts dense shade, alters soil conditions, and may be allelopathic. We used greenhouse and field experiments to investigate above‐ and belowground effects of Rhamnus on four herbaceous species native to southern Wisconsin. In the greenhouse, we assessed how Rhamnus leaves and fruit affected seed germination and seedling growth relative to sugar maple (Acer saccharum) leaves. Fewer seeds of Eurybia macrophylla and Thalictrum dasycarpum germinated under Rhamnus leaves, and those that germinated were slowed. We planted seedlings of the four natives into four treatments at three sites in the field to assess how their survival, growth, and flowering respond to the separate and combined effects of light levels, buckthorn canopies, and buckthorn soils. Buckthorn consistently reduced native plant performance by diminishing survival, flowering, and growth in Thalictrum, survival and flowering in Eurybia, and flowering and growth in Symphyotrichum lateriflorum. Removing buckthorn canopies enhanced growth of these native species, but buckthorn soils separately inhibited growth at least as much (despite being more fertile). Buckthorn's impacts on native plants exceed effects attributable to light levels and soil fertility, suggesting allelopathy. Buckthorn reduced performance more in the uncommon species (Thalictrum and Eurybia) than the common species (Geranium maculatum and Symphyotrichum). As we do not yet know how long these inhibitory soil effects persist, we need additional research to learn how best to control buckthorn's impacts on native plant communities.     

Competition between similar invasive species: modeling invasional interference across a landscape

As the number of biological invasions increases, interactions between different invasive species will become increasingly important. Several studies have examined facilitative invader–invader interactions, potentially leading to invasional meltdown. However, if invader interactions are negative, invasional interference may lead to lower invader abundance and spread. To explore this possibility, we develop models of two competing invaders. A landscape simulation model examines the patterns created by two such species invading into the same region. We then apply the model to a case study of Carduus nutans L. and C. acanthoides L., two economically important invasive weeds that exhibit a spatially segregated distribution in central Pennsylvania, USA. The results of these spatially-explicit models are generally consistent with the results of classic Lotka–Volterra competition models, with widespread coexistence predicted if interspecific effects are weaker than intraspecific effects for both species. However, spatial segregation of the two species (with lower net densities and no further spread) may arise, particularly when interspecific competition is stronger than intraspecific competition. A moving area of overlap may result when one species is a superior competitor. In the Carduus system, our model suggests that invasional interference will lead to lower levels of each species when together, but a similar net level of thistle invasion due to the similarity of intra- and interspecific competition. Thus, invasional interference may have important implications for the distribution and management of invasive species.     

The diversity of juvenile salmonids does not affect their competitive impact on a native galaxiid

We used an invaded stream fish community in southern Chile to experimentally test whether the diversity of exotic species affects their competitive impact on a native species. In artificial enclosures an established invasive, rainbow trout, Oncorhynchus mykiss, and a potential invader, Atlantic salmon, Salmo salar, reduced the growth rate of native peladilla, Aplochiton zebra, by the same amount. In enclosures with both exotic salmonids, the growth rates of all three species were the same as in single exotic treatments. While neither species identity nor diversity appeared to affect competitive interactions in this experiment, the impact of salmonid diversity may vary with the type of interspecific interaction and/or the species identity of the exotics. Our experiment links two prominent concepts in invasion biology by testing whether the result of invasional meltdown, an increase in the diversity of exotic species, affects their impact through interspecific competition, the mechanism invoked by the biotic resistance hypothesis.     

Increased light availability due to forestry mowing of invasive European buckthorn promotes its regeneration

The invasive shrub Rhamnus cathartica L. (common buckthorn) dominates the understory of many temperate forests of eastern North America. Common buckthorn outcompetes native understory species for light, forming monospecific stands that suppress plant and animal diversity. Removing common buckthorn is a common management priority within its invasive range. In recent years, forestry mowing has become popular in removing common buckthorn. This control method removes a midstory of common buckthorn, increasing light availability to the lower understory (which could favor buckthorn regeneration) and creating a layer of mulch on the forest floor (which could suppress buckthorn regeneration). Here we investigate whether and how increased light availability and increased ground cover (mulch) resulting from forestry mowing affects buckthorn regeneration from the seed bank. We evaluated buckthorn germination, survival, and early growth in response to a factorial combination of shading treatments and buckthorn mulch depth treatments in an oak forest in Minnesota, U.S.A. Increased light availability increased buckthorn seedling survival and growth, whereas increased mulch depth did not significantly affect the number of buckthorn establishing from seed over one growing season and winter. Thus, removing buckthorn by forestry mowing (or any other method) is likely to facilitate buckthorn reestablishment by increasing light availability at the ground.     

Invasional meltdown: an experimental test and a framework to distinguish synergistic,additive, and antagonistic effects

The potential role of positive interactions among co-invaders is at the core of the invasional meltdown hypothesis. The interaction of non-native species could result in an exacerbation of each other’s effects. Thus, the resulting effect of multiple non-native species on ecosystems can be greater than the sum of their individual effects. We designed an analytical framework and a set of mesocosm experiments to assess the potential synergistic effects of three non-native species (Limnoperna fortunei, Astronotus crassipinnis, and Hydrilla verticillata) in a highly invaded floodplain in southern Brazil. We analyzed ecosystem, community, and population attributes in scenarios with non-natives. Our hypothesis of a synergistic effect was not supported. Even though effects of the invasive species were detected for all ecological levels, evidence indicated that these effects were additive. In addition to adding to the statement that origin (i.e., native vs. non-native status) does matter, we provide a tool to differentiate additive, synergistic, and antagonistic effects in situations with multiple invasions, and experimentally demonstrate additive effects of non-native species at different ecological levels.

     

Induction of colony initiation by Japanese native bumble bees using cocoons of the exotic bumblebee Bombus terrestris

The colony initiation rates of Bombus hypocrita (a native Japanese bumblebee) and Bombus terrestris (a European species) foundresses were compared after 4 weeks of exposure to B. terrestris cocoons. The B. terrestris cocoons, when replaced weekly, were effective for inducing oviposition by foundresses of both species. There were no significant differences in the colony initiation rates of B. terrestris and B. hypocrita, either with the control treatment or with the cocoons. The cocoon method was also tested for five species and two subspecies of native Japanese bumblebees. The colony initiation rate was higher for foundresses of the subgenus Bombus s. str. than for foundresses of the subgenera Pyrobombus, Diversobombus, and Thoracobombus. When replaced weekly, the cocoons of B. terrestris are effective inducers of colony foundation in three Japanese native species, namely B. ignitus, B. hypocrita hypocrita, and B. h. sapporoensis.     

Cover Caption

Like most aphid species, the Vetch aphid, Megoura viciae, produces honeydew while feeding on broad bean, Vicia faba. After being rejected on the host plant surface, honeydew releases a kairomonal blend of volatile molecules that guide aphid predators, including the Asian lady beetle, Harmonia axyridis, toward aphid colonies (Credits F.J. Verheggen, see pages 498–506).     

Impact of intraguild predation by adult Harmonia axyridis (Coleoptera: Coccinellidae) on Aphis glycines (Hemiptera: Aphididae) biological control in cage studies

The soybean aphid, Aphis glycines Matsumura, has become a principal arthropod pest of soybean in the U.S. since its first detection in 2000. This species threatens soybean production through direct feeding damage and virus transmission. A diverse guild of insect predators feeds on soybean aphid in Michigan including the exotic coccinellid Harmonia axyridis, the native gall midge Aphidoletes aphidimyza and the native lacewing Chrysoperla carnea. In addition to feeding on A. glycines some members of this guild may also engage in intraguild predation. These interactions may produce positive, negative, or neutral impacts on A. glycines biological control. We explored the impact of intraguild predation on soybean aphid population dynamics by comparing aphid populations in microcosms with either A. aphidimyza larvae or C. carnea larvae alone, with both a H. axyridis adult and either A. aphidimyza or C. carnea larvae, and without predators. When H. axyridis was present with larval A. aphidimyza or C. carnea, the lady beetle acted as an intraguild predator. However, intraguild feeding did not result in a release of aphid populations compared with microcosms containing only the intraguild and aphid prey. A similar result was found in field cages. Cages allowing large predators had reduced numbers of A. aphidimyza and C. carnea larvae but also significantly fewer aphids compared with predator exclusion cages. Thus, in both lab and field studies the direct impact of H. axyridis on A. glycines overcame its negative impact as an intraguild predator. Together, these studies indicate that while the exotic H. axyridis does act as an intraguild predator and may contribute to local declines in A. aphidimyza and C. carnea, it is also currently important in overall biological control of A. glycines.     

Life history characteristics of Orius insidiosus (Say) fed Aphis glycines Matsumura

The soybean aphid, Aphis glycines Matsumura, is a new invasive pest of soybeans throughout most of the soybean production areas of North America. Field studies have demonstrated that the indigenous predator, Orius insidiosus (Say), is an important natural enemy of the soybean aphid early the soybean crop season. Because soybean aphid is newly introduced into North America, the life history characteristics of predators fed this aphid are not known. In laboratory assays, we measured the survival, development, longevity and reproduction of O. insidiosus fed 1, 3, 6 or 12 seconds to third instars of soybean aphid. O. insidiosus nymphal development decreased from 34.0 to 21.4 days as the number of soybean aphid nymphs provided increased from 1 to 6 aphid nymphs daily. Stage-specific mortality was highest at 68% for first instar O. insidiosus nymphs fed 1 soybean aphid nymph per day. Adult longevity (43.9 days) and fecundity (49.7 eggs per female) was highest for O. insidiosus fed 6 soybean aphid nymphs daily, but longevity (23.5 days) and fecundity (10.1 eggs per female) declined for adults fed 1 soybean aphid nymph daily. The intrinsic rate of increase of O. insidiosus ranged from 0.048 to 0.133. Compared to other prey species, soybean aphid is an adequate prey item for O. insidiosus. Our results suggest that O. insidiosus will be most effective in suppressing soybean aphid population growth in the initial phase of the aphid’s colonization of soybeans.     

Experimental test of the Invasional Meltdown Hypothesis: an exotic herbivore facilitates an exotic plant,but the plant does not reciprocally facilitate the herbivore

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Quantifying how acquired interactions with native and invasive insects influence population growth rates of a non-indigenous plant

Non-native species often acquire novel interspecific interactions, which are central to several hypotheses of invasion success, including biotic resistance and invasional meltdown. However, the outcome of these interactions is not often linked with the demographic evidence based on the full life cycle of the species. The Philippine Ground Orchid (Spathoglottis plicata) has invaded Puerto Rico and has acquired both negative and positive interspecific interactions involving the native weevil Stethobaris polita and the invasive red fire ant Solenopsis invicta, respectively. We studied a population in the Rio Abajo Forest, and asked how these interactions affect population demography by using a combination of field, experimental and modelling approaches. Stage-structured matrix population models based on four years of field observations showed that the population of S. plicata is growing at a rate (λ) of 1.05 under natural conditions. When we modified fecundity values based on experimental exclusion of weevils and ants, the control treatment showed a similar λ. Excluding weevils increased λ to 1.20, whereas the exclusion of ants decreased λ to 1.03. When we incorporate demographic and environmental stochasticity in our models, exclusion of invasive red fire ants significantly reduces the orchid abundance over time. Although weevils offer some biotic resistance to S. plicata, these effects do not prevent orchid population growth and expansion. On the other hand, invasive red fire ants have a positive effect on the invasive orchid’s λ, partially supporting the invasional meltdown hypothesis. This study presents a method that allows one to combine opposing mechanisms of species interactions within the same quantitative framework, and the results highlight the importance of considering acquired plant–animal interactions and stochastic processes when evaluating the population growth rates and dynamics of invasive plants.     

Predation and avoidance behaviour in aphid‐ladybird interactions of native and invasive ladybirds in Europe

1. While detrimental effects of invasive predators on native species are well documented, we often lack a mechanistic understanding of the invasion success. Lack of prey avoidance behaviour can lead to higher consumption rates by invasive predators compared to native predators. This competitive advantage is expected to contribute to the invasion success of non‐native predators.
2. We compared aphid consumption and cue avoidance behaviour of aphids between four native ladybird species (Coccinella septempunctata, Adalia bipunctata, Propylea quatuordecimpunctata, and Hippodamia variegata) and the invasive Asian ladybird Harmonia axyridis.
3. The invasive H. axyridis and the native C. septempunctata consumed more aphids than the three smaller native ladybird species. In line with our expectations, aphids avoided leaves bearing cues of most native ladybird species but not of the invasive H. axyridis.
4. Our results indicate that body size rather than ladybird origin determined aphid predation rates. The lack of aphid avoidance behaviour towards cues of H. axyridis indicates that they were not able to recognise the chemical cues of the invasive predator.
5. Relatively large body size and the absence of cue avoidance in aphids might benefit the invasive H. axyridis, particularly in comparison to smaller native ladybird species. The absence of avoidance behaviour in aphids might lead to even higher predation rates of H. axyridis under more natural conditions.