Post-establishment assessment of host plant specificity of Arytainilla spartiophila (Hemiptera: Psyllidae), an adventive biological control agent of Scotch broom,Cytisus scoparius

Scotch broom, Cytisus scoparius (Fabaceae), is a shrub native to Europe that is invasive in the USA, New Zealand and Australia. The psyllid Arytainilla spartiophila has been purposely introduced to Australia and New Zealand as a biological control agent of C. scoparius, but is an accidental introduction to California. Lupines (Lupinus spp.) are the closest native taxon to Cytisus in North America, and are therefore considered to be at the highest risk for non-target damage. However, because no lupines are native to Australia or New Zealand, only one imported forage species was evaluated during prior host specificity testing. We conducted a laboratory nymphal transfer experiment, a field choice experiment and a field survey to assess risk to three lupine species (Lupinus albifrons, Lupinus bicolor and Lupinus formosus). In the laboratory, 20% of third-instar nymphs were able to develop to adulthood on L. formosus but not on the other lupine species, while 40% completed development on C. scoparius. In the field experiment, potted lupine and C. scoparius plants were placed beside large infested C. scoparius plants; oviposition occurred on all the potted C. scoparius plants, but on none of the lupines. In the field survey, no A. spartiophila eggs or nymphs were found on naturally occurring lupines growing adjacent to infested C. scoparius. The results indicate that A. spartiophila is not likely to damage or reproduce on lupines in the field. This study provides an example of how field studies can help clarify the host specificity of biological control agents.     

Combined effects of drought stress and psyllid herbivory on the invasive weed Scotch broom,Cytisus scoparius

Increases in the frequency and duration of droughts under global climate change could have implications for plant–insect interactions, and could either increase or decrease the effects of weed biological control agents. In this study, we used greenhouse and field experiments to examine the impacts of drought stress on the abundance and impacts of the adventive psyllid Arytainilla spartiophila Forster (Hemiptera: Psyllidae, Arytaininae) on its target weed Scotch broom, Cytisus scoparius (L.) Link (Fabaceae), in California, USA. The psyllid impacted plant growth in both field and greenhouse experiments, whereas drought stress affected plant growth in the greenhouse only, suggesting that other factors besides water availability may be more limiting for plants in the field. Effects on psyllid survival were consistent with the plant vigor hypothesis, which predicts that herbivores will perform better on vigorously growing plants; psyllid numbers were lower on drought-stressed plants in the greenhouse and were correlated with plant growth in both the greenhouse and the field. In the greenhouse, the combined effects of the psyllid and drought stress were additive, indicating that the effects of the psyllid were consistent across unstressed and drought-stressed plants. Although the psyllid is unlikely to control Scotch broom on its own, results suggest that it may work in conjunction with drought stress to suppress Scotch broom.     

A modelling approach to estimate the effect of exotic pollinators on exotic weed population dynamics: bumblebees and broom in Australia

The role of mutualisms in contributing to species invasions is rarely considered, inhibiting effective risk analysis and management options. Potential ecological consequences of invasion of non‐native pollinators include increased pollination and seed set of invasive plants, with subsequent impacts on population growth rates and rates of spread. We outline a quantitative approach for evaluating the impact of a proposed introduction of an invasive pollinator on existing weed population dynamics and demonstrate the use of this approach on a relatively data‐rich case study: the impacts on Cytisus scoparius (Scotch broom) from proposed introduction of Bombus terrestris. Three models have been used to assess population growth (matrix model), spread speed (integrodifference equation), and equilibrium occupancy (lattice model) for C. scoparius. We use available demographic data for an Australian population to parameterize two of these models. Increased seed set due to more efficient pollination resulted in a higher population growth rate in the density‐independent matrix model, whereas simulations of enhanced pollination scenarios had a negligible effect on equilibrium weed occupancy in the lattice model. This is attributed to strong microsite limitation of recruitment in invasive C. scoparius populations observed in Australia and incorporated in the lattice model. A lack of information regarding secondary ant dispersal of C. scoparius prevents us from parameterizing the integrodifference equation model for Australia, but studies of invasive populations in California suggest that spread speed will also increase with higher seed set. For microsite‐limited C. scoparius populations, increased seed set has minimal effects on equilibrium site occupancy. However, for density‐independent rapidly invading populations, increased seed set is likely to lead to higher growth rates and spread speeds. The impacts of introduced pollinators on native flora and fauna and the potential for promoting range expansion in pollinator‐limited ‘sleeper weeds’ also remain substantial risks.     

Shrub succession and invasibility in a New Zealand montane grassland

Abstract Two successive shrub invasions of a short tussock grassland induced by grazing and burning were examined in montane South Island, New Zealand. The first invasion was by a native shrub, matagouri (Discaria toumatou Raoul). The second invasion was by an exotic shrub, Scotch broom (Cytisus scoparius (L.) Link), which invaded the matagouri shrubland that had developed over the grassland. The invasions were investigated using analysis of spatial patterns of both shrubs and tussocks, and age, growth rates and size structure of the shrubs. Competition between the two shrub species was examined using spatial patterns and comparing allometric relationships. After initial invasion by matagouri of the grasslands, stand density increased by consolidation about its initial colonization points. Current matagouri distribution is often negatively associated with tussocks. Scotch broom occurs most frequently in a dense sward of introduced grasses and occasionally in tussocks in interstices among matagouri shrubs. Despite the palatability of Scotch broom to sheep that graze the site, there was no evidence that the spiny matagouri facilitates invasion by protecting Scotch broom seedlings; rather there was negative association between the shrub species. The two species probably compete for above-ground space. However, diameter and height growth rates of Scotch broom far exceed those of matagouri so Scotch broom is likely to increase in biomass rapidly at the site. The autogenic organization and disturbance history of the resident plant communities have rendered each vulnerable to successive invasions.     

Isolation and characterization of polymorphic microsatellite loci for the invasive plant Cytisus scoparius

Scotch broom (Cytisus scoparius) is a serious weed of natural and pastoral ecosystems and is invasive in many countries worldwide. Eight polymorphic microsatellite loci were developed and characterized for this species. The number of alleles per locus ranged from five to 23. The range of observed heterozygosity was between 0.207 and 0.928. These microsatellite markers will be useful tools for studies of population genetics in the native and invasive range of this species.     

Relationships between Scotch broom (Cytisus scoparius), soil nutrients, and plant diversity in the Garry oak savannah ecosystem

Scotch broom (Cytisus scoparius), is a leguminous shrub, native to the Mediterranean, which has invaded most of the remaining Garry oak savannah ecosystems in Oregon, Washington, and British Columbia. Here, it is considered to be a threat to the native plant community. We tested the hypothesis that broom would increase available soil nitrogen by comparing soil nutrients in contiguous broom-invaded and non-invaded sites. We then looked for changes in patterns of diversity in the herbaceous community that might indicate a role of Scotch broom in changing conditions following its invasion. Finally we carried out greenhouse assays to test whether broom had a greater impact on the growth of a native and an introduced grass compared to that of a native shrub. Broom was associated with only a weak trend in increased soil nitrogen, but a significant decrease in soil phosphorus was observed. Patterns of plant diversity differed between two sites. At one site, 60% of the plants whose abundances increased in the broom-invaded plots were introduced species while native species abundances decreased in the broom-invaded plots compared to broom-free plots. At the other site, 60% of the plants that caused the differences between broom-invaded and un-invaded plots were native species that were less abundant in the broom-invaded plots. Finally, in greenhouse assays grass growth was not affected as a result of being grown with broom; however, grasses appeared to produce more flowers when grown with broom. We conclude that broom does not necessarily modify soil nitrogen availability but may deplete soil phosphorus availability and that broom invasion can be associated with increase of exotic species and/or the decline of native species.     

The Effect of Variability in the Phenology of the Reproductive Stages of Scotch Broom (Cytisus scoparius) on the Synchronization of the Life Stages of Broom Seed Beetle (Bruchidius villosus) in New Zealand

Variability in timing of the reproductive stages of Scotch broom (Cytisus scoparius) may influence synchronization and establishment of the broom seed beetle (Bruchidius villosus), a biological control agent. A sampling scheme was devised to compare the phenologies of Scotch broom at different sites in the same season and in different seasons at the same site. The synchrony of the broom seed beetle's life stages with those of the host plant was also determined. The phenology of Scotch broom varied only slightly from season to season at Lincoln, but could vary considerably between sites in the same season. At both sites where it is established, the broom seed beetle was synchronized with its host; adult beetles were present throughout the flowering period. Eggs were found on suitable green pods. The broom seed beetle appears capable of adapting to the phenology of its host and has the potential to be an effective agent for Scotch broom. Variability in phenology of the reproductive stages of Scotch broom, even at nearby sites, must be taken into account by practitioners of biological control when releasing broom seed beetles and later when sampling beetles to determine establishment.     

Implications of individual variation in insect behavior for host specificity testing in weed biocontrol

This study shows that individual behavioral variation is an under-recognised source of error that may affect the outcome of host range tests in a stenophagous species. Original specificity testing of the broom seed beetle, Bruchidius villosus (F.) (Coleoptera: Chrysomelidae: Bruchinae), a biocontrol agent for Scotch broom, Cytisus scoparius (L.) Link (Fabaceae: Genisteae), failed to detect its ability to oviposit in the field on a congeneric non-target plant, the exotic Cytisus proliferus L.f. (Fabaceae: Genisteae). These tests were repeated using individual beetles from the original UK collection sites and from New Zealand, 15 generations post release. In the original tests, low replication of small batches of females masked high levels of individual variation in oviposition preference. Although most beetles showed strong preference for the target weed, there was some indication that New Zealand beetles showed higher preference for the non-target than UK beetles.     

The Scotch broom,Cytisus scoparius (Fabaceae), a paradox in Denmark – an invasive plant or endangered native species?

Scotch broom, Cytisus scoparius, spreads rapidly in parts of Denmark and is considered an invasive species by some authors. However, the species has been present in the Danish flora for centuries and is therefore considered native to Denmark. In the present study we explore whether Danish Scotch broom consists of one or two gene pools with potential differences in phenotype and invasiveness. One plastid and five nuclear microsatellite markers were used to reveal potential substructuring of Danish Scotch broom. Nine populations were included representing populations exhibiting invasive behaviour and populations showing non‐invasive behaviour. An Italian population was used as reference. Bayesian analysis based on genetic markers indicated that the sampled populations form two distinct gene pools, and this pattern was supported by neighbour‐joining trees. Measurements of height and width of the analysed plants showed that the two gene pools correspond to populations exhibiting either a horizontal habit and non‐invasive behaviour or an erect habit and, in some cases, invasive behaviour. The Italian population clustered with the erect ones. We discuss the origin and taxonomic status of the two gene pools and conclude that Danish horizontal Scotch broom should be given a formal taxonomic status in order to initiate conservation activities for its protection. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, ●● , ●●–●●.     

Snowpack,fire, and forest disturbance: interactions affect montane invasions by non‐native shrubs

Montane regions worldwide have experienced relatively low plant invasion rates, a trend attributed to increased climatic severity, low rates of disturbance, and reduced propagule pressure relative to lowlands. Manipulative experiments at elevations above the invasive range of non‐native species can clarify the relative contributions of these mechanisms to montane invasion resistance, yet such experiments are rare. Furthermore, global climate change and land use changes are expected to cause decreases in snowpack and increases in disturbance by fire and forest thinning in montane forests. We examined the importance of these factors in limiting montane invasions using a field transplant experiment above the invasive range of two non‐native lowland shrubs, Scotch broom (Cytisus scoparius) and Spanish broom (Spartium junceum), in the rain–snow transition zone of the Sierra Nevada of California. We tested the effects of canopy closure, prescribed fire, and winter snow depth on demographic transitions of each species. Establishment of both species was most likely at intermediate levels of canopy disturbance, but at this intermediate canopy level, snow depth had negative effects on winter survival of seedlings. We used matrix population models to show that an 86% reduction in winter snowfall would cause a 2.8‐fold increase in population growth rates in Scotch broom and a 3.5‐fold increase in Spanish broom. Fall prescribed fire increased germination rates, but decreased overall population growth rates by reducing plant survival. However, at longer fire return intervals, population recovery between fires is likely to keep growth rates high, especially under low snowpack conditions. Many treatment combinations had positive growth rates despite being above the current invasive range, indicating that propagule pressure, disturbance, and climate can all strongly affect plant invasions in montane regions. We conclude that projected reductions in winter snowpack and increases in forest disturbance are likely to increase the risk of invasion from lower elevations.     

Characterization of Phages Virulent for Sarothamnus scoparius Bradyrhizobia

Four virulent phages—ΦDl, ΦTl, ΦCYT21, and ΦOS6, infective on Sarothamnus scoparius rhizobia—were isolated from the soil and characterized for morphology, host range, rate of adsorption to bacterial cells, and genome size. New phages were separated into two morphological families: Siphoviridae with long, noncontractile tails (ΦDl, ΦTl) and Myoviridae with long, contractile tails (ΦCYT21, ΦOS6). They were also classified into two groups by a host specificity. One of them included viruses (ΦDl and ΦTl) that lysed S. scoparius bradyrhizobia and Bradyrhizobium sp. (Lupinus) strain Dl, and the second one comprised phages (ΦCYT21 and ΦOS6) that parasitized only Scotch broom native microsymbionts. Phages specific for S. scoparius rhizobia were differentiated not only by morphology and host range but also by a genome size that was in the range from 47,583 to 60,098 b.p. An erratum to this article is available at .     

Demography of the invasive shrub Scotch broom (Cytisus scoparius) at Barrington Tops,New South Wales: insights for management.

The exotic shrub Scotch Broom (Cytisus scoparius) has invaded large areas of eucalypt woodland at Barrington Tops, New South Wales, where it forms dense stands that have significant impacts on vegetation structure, flora and fauna. Data are presented from four 25 m² plots, which have been studied since 1985. Two plots were located in uniform broom thickets of different ages, and two were located across the margins of broom stands, which have since expanded to cover the entire plots. All broom plants in the plots (other than young seedlings, which were counted) were mapped, tagged and monitored annually. New seedlings appeared annually, but there was no relationship between their numbers (varying between years) and subsequent recruitment of older plants. The probability of seedlings reaching first flowering was less than 2%, and of surviving to mature size (>10 cm² basal area) was negligible. Seedlings mainly died through suppression (shade). Individuals less than 50 cm high were also browsed. Recruitment occurred only where light levels were high, either before closure of the broom canopy or after senescence had led to canopy opening. From approximately 12–30 years after initial invasion, broom stands underwent self‐thinning of mature plants, accelerated by collapse of plants on to each other. Recruitment of new, maturing plants, after this period produced a stand that was less dense than that found after initial invasion. Broom is creating more disturbance‐prone environments due to its impacts on other biota, likely alterations to the fire regime, and by harbouring feral pigs. Further disturbance favours broom, and elsewhere it has resulted in massive seedling regeneration. While fire or other disturbance can be used to stimulate germination, and thereby reduce a large part of the soil seed bank, denser broom infestations are likely to result unless follow‐up treatments can be applied over long time periods. A wiser management option, at least in the short term, may be avoidance of all disturbance, especially for stands of mature broom.     

Safe Site and Seed Limitation in Cytisus Scoparius (Scotch Broom): Invasibility, Disturbance, and the Role of Cryptogams in a Glacial Outwash Prairie

In all plant populations, establishment is controlled by two factors: the supply of propagules and their access to ‘safe sites’ for growth. An infestation of invading pest plants results in a seed-production gradient, from the edge where seeds are limiting, to the center where seeds may be in excess. Do invaded sites become ‘saturated’ with seeds? How rapidly does this occur, and how does the process depend on the availability of safe sites? Are safe sites, and consequently invasion, promoted by disturbance? I quantified the response of seedling establishment to seed input and disturbance in Cytisus scoparius (Scotch broom), an exotic shrub invading glacial outwash prairie remnants in western Washington, USA. I used disturbance treatments to investigate the role of the thick cryptogamic layer in these prairies, disturbing cryptogams by scraping or by fire. The effect of fire was partitioned into two factors: burning of the background vegetation/substrate versus breaking C. scoparius seed dormancy, by adding seeds either before or after the burn. Seed treatments ranged from 20 to 1000 seeds per m². Both seed number and surface treatment showed significant effects on seedling density, along with a significant interaction between the two factors. Disturbance did not promote C. scoparius establishment; undisturbed plots produced more seedlings than burned or scraped plots. Within the burned plots, fire scarification appeared to increase germination but this effect was not significant. For germinated seedlings, mortality through the dry season (June–August) was not significantly different among surface treatments, nor did survivorship depend on density, with the result that initial differences in germination among the treatments persisted. The message that the undisturbed cryptogam layer facilitates C. scoparius establishment suggests that ‘ecosystem management’ strategies promoting healthy, undisturbed sites will not always be effective against invasive pest species.     

Association of flower color with pollen reward may explain increased bumblebee visitation to the Scotch broom yellow morph

Given that pollinators usually visit flowers for hidden rewards, they need to rely on floral traits that indicate reward status (“honest signals”). However, the relationship between pollination, honest signals, and floral rewards is little documented in natural conditions. The Scotch broom (Cytisus scoparius) is an invasive shrub with polymorphism in the color of its flowers that can be yellow, orange, or red. In three areas dominated by the Scotch broom, we described the abundance of the floral morphs and estimated bumblebee (Bombus terrestris) visitation rate. We examined whether bumblebee visitation to the floral morphs was related to pollen reward. We collected flowers and classified their stamens according to their function: reward or pollen export. Then, we measured anther size and estimated pollen quantity. The yellow morph was more abundant and more visited by bumblebees than the orange and red morphs. The yellow flowers did indeed offer more pollen than the other morphs and this occurred only for rewarding anthers, suggesting that bumblebees could use yellow color as an honest signal to visit the most rewarding flowers. We discuss whether innate and/or learned preferences of bumblebees can explain why the yellow morph is more visited, pollinated, and abundant, while the other morphs are maintained at a lower frequency. This is one of the few field works that shows that variation in intra-specific floral traits is associated with variation in floral reward and pollinator visitation rate, helping to understand the foraging preferences of pollinators and the coexistence of floral morphs in nature.

Clinical trials registration: Not applicable.

     

Climatic analysis to determine where to collect and release Puccinia jaceae var. solstitialis for biological control of yellow starthistle

Puccinia jaceae var. solstitialis is an autoecious rust fungus that is native to areas of Afro-Eurasia with a Mediterranean climate. An isolate collected near Sivas, Turkey was released for classical biological control of yellow starthistle (YST), which is an invasive alien weed in California, USA. The fungus has been released throughout California, but long-term establishment rates are generally low, apparently because this ecotype is not well adapted to the climate where the weed is most invasive. Using a site with excellent establishment as a target, the Match Climates function in CLIMEX climate modeling software identified similar sites in and around the San Francisco Bay Area, east to the Central Valley and Sierra foothills, and along the coast of Southern California. Similar sites in other states include Walla Walla, Washington, Pendelton, Oregon and Salt Lake City, Utah. A Compare Locations model based primarily on experimentally measured temperature and humidity requirements of the rust produced similar results. Using Sacramento, California, which is in the center of YST distribution, as a target, the Match Climates function predicted that the best locations to search for rust accessions to use in California are near Tunis, Tunisia, Foggia, Italy, Khalkis, Greece, Kayseri, Turkey, and possibly Constantine, Algeria. This generally agrees with the prediction of a Compare Locations model based on the geographic distribution of YST in California. Climatic factors that limit the long-term establishment of the fungus are likely to be summer heat and/or dry stress and short dew periods.     

The root-nodule symbiosis between Sarothamnus scoparius L. and its microsymbionts

When nitrogen fixing root nodules are formed, Sarothamnus scoparius (broom) is inoculated with its microsymbionts. Nodules studied under light and electron microscopy exhibited typical indeterminate nodule histology with apical, persistent meristem, age gradient of nodule tissues, and open vascular bundles, and also with some particular features such as: the presence of mitotic activity in the infected meristematic cells, lack of infection threads, distribution of bacteria by process of host cell division, and occurrence of a large bacteroid zone only with infected cells. The results of cross-inoculation tests have shown a broad host range for S. scoparius microsymbionts including not only the native host but also species such as: Lupinus luteus, Ornithopus sativa, Lotus corniculatus, Genista tinctoria, Chamaecitisus ratisbonensis, Macroptilium atropurpureum, and Phaseolus vulgaris. In addition, our data established a close symbiotic relationship of S. scoparius nodulators to Bradyrhizobium sp. (Lupinus) by comparison of the partial sequence of nodC gene of the strain CYT7, specific for the broom, to those from Bradyrhizobium sp. (Lupinus) strain D1 and others available in the public databases.     

Complete development on Elodea canadensis (Hydrocharitaceae) eliminates Hydrellia egeriae (Diptera,Ephydridae) as a candidate biological control agent of Egeria densa (Hydrocharitaceae) in the U.S.A.

The leaf-mining fly Hydrellia egeriae Rodrigues-Junior (Diptera: Ephydridae) was evaluated under quarantine conditions as a candidate biological control agent of the invasive aquatic weed Egeria densa Planchon (Hydrocharitaceae) in California, U.S.A. The objective of this study was to test the fly’s feeding preference for E. densa as compared to the North American native Elodea canadensis Michaux (Hydrocharitaceae), an important benchmark species. No choice testing revealed that H. egeriae can complete development on E. canadensis and choice testing indicated the fly presents little oviposition discrimination between E. densa and E. canadensis. It is concluded that the host range of H. egeriae is too broad for use as a biological control agent of E. densa in the U.S.A.     

The host specificity of Anomalococcus indicus Ayyar (Hemiptera: Lecanodiaspididae), a potential biological control agent for prickly acacia (Vachellia nilotica ssp. indica) in Australia

ABSTRACT

Prickly acacia, Vachellia nilotica ssp. indica (Benth.) Kyal. & Boatwr, is a significant weed of northern Australia and has been a target of weed biological control in Australia since the 1980s. Following native range surveys in India, the scale insect Anomalococcus indicus Ayyar was identified as the most promising agent and was imported into Australia for further research. A. indicus is a major pest of prickly acacia on the Indian subcontinent, where it causes shoot tip dieback and plant death. Despite field observations suggesting the species was specific to V. nilotica, A. indicus completed development on 17 of the 84 non-target plant species tested during no-choice host specificity trials under quarantine conditions. Of these, Acacia falcata, V. bidwillii, V. sutherlandii and Neptunia major supported high numbers of mature females in all replicates. All of these species were utilised in choice trials. Combined risk scores indicate that V. sutherlandii, N. major and A. falcata may be attacked in the field. Due to the limited ability of scale insects to disperse, only those non-target species that occur on the Mitchell grass downs (i.e. V. sutherlandii) are considered to be at risk. Nevertheless, in view of the disparity between quarantine test results and the observed field host specificity of A. indicus in India, field trials are currently being conducted in India using Australian native species on which complete development has occurred. The future of A. indicus as a biological control agent for prickly acacia in Australia will be determined once results from these field trials are known.     

The double life cycle of Lepidapion argentatum,a promising candidate for the biological control of French Broom.

Lepidapion argentatum (Gerstaecker) (Brentidae) is a weevil from the Mediterranean region collected and recorded from French broom (Genista monspessulana) (L.) LAS Johnson (Fabaceae), a major invasive plant in the USA. We studied feeding and oviposition of L. argentatum under laboratory conditions. Overwintering adults can oviposit in either seed-pods or stem tips of French broom. Larvae in seed-pods consume seeds whereas those in stems develop inside a gall. The development time of L. argentatum in stem galls ranged from 34 to 40 days at mean 23.67?±?2.43°C. The double ability of L. argentatum to develop in stems and pods appears not to have been recorded in Coleoptera and rare in other phytophagous insects. Our finding increases its potential value as a biocontrol agent against French broom.     

Host specificity ofAceria (Eriophyes) malherbe, [Acari: Eriophyidae], a biological control agent for the weed,Convolvulus arvensis [Convolvulaceae]

The host specificity of the gall mite,Aceria (Eriophyes) malherbe (Nalepa), from Greece was studied under quarantine conditions at Albany, California USA. Of the species, ecotypes, or strains tested, onlyConvolvulus andCalystegia spp. supported gall formation and mite reproduction. Although 2 of the native, North AmericanCalystegia species that served as laboratory hosts are threatened or endangered species,A. malherbe is considered safe for release in the USA as a biological control agent of the weed,Convolvulus arvensis (L.).