Assessment of risk of attack to safflower by Ceratapion basicorne (Coleoptera: Apionidae), a prospective biological control agent of Centaurea solstitialis (Asteraceae)

Ceratapion basicorne (Coleoptera: Apionidae) is a prospective biological control agent of yellow starthistle (Centaurea solstitialis, Asteraceae: Cardueae), which is an important invasive alien weed in the western United States. Previous studies have shown that it is possible for this insect to oviposit on and complete development on safflower (Carthamus tinctorius) under no-choice laboratory conditions; however, it has never been reported as a pest of safflower. Field experiments were conducted at three sites in eastern Turkey during 3 years to evaluate the risk of attack on safflower by this insect in its native range. At two sites where C. basicorne was the only apionid observed, no safflower plants were attacked despite high attack rates on yellow starthistle test plants (48–98% of plants infested). At a third site, where C. basicorne and three other species in the same genus; C. scalptum, C. orientale, and C. onopordi were present, 8–26% of safflower plants were infested, but none of the insects reared from safflower during 3 years were C. basicorne. Other authors have reported rearing C. basicorne from field-collected plants of only Ce. solstitialis, Ce. cyanus, Ce. depressa, and Cnicus benedictus. Our results indicate that C. basicorne does not attack safflower under field conditions and that its introduction would not pose a risk to this crop.     

Field assessment in land of origin of host specificity,infestation rate and impact of <Emphasis Type="Italic">Ceratapion basicorne</Emphasis> a prospective biological control agent of yellow starthistle

Yellow starthistle, Centaurea solstitialis (Asteraceae), is an important invasive alien weed in the western United States. Currently established biological control agents attack only the capitula (flowerheads), and are not effectively controlling the plant in much of its range. The geographic center of diversity for the plant appears to be in Turkey, but no agents have been introduced from this country. Ceratapion basicorne (Coleoptera: Apionidae) is common in Central Turkey, attacking 25–100% of yellow starthistle plants. In a field experiment, Ceratapion spp. attacked 90% of yellow starthistle plants and 88% of milk thistle plants (Silybum marianum) but not seven other plant species, including artichoke and safflower. We suspect that a different species of insect attacked milk thistle, but they emerged before the plants were sampled. Laboratory tests showed that C. basicorne does not oviposit in milk thistle. Ceratapion basicorne appears to be more host specific than was suggested by previous studies of a population in Italy (Clement etal. 1989. Ann. Entomol. Soc. Am. 82: 741–747). The insect is gregarious, and the number of larvae per plant was positively correlated to root diameter. The level of damage to individual plants was positively correlated to the proportion of plants attacked, indicating aggregation both among plants and within plants. Field data did not show any impact of the insect on plant size or number of capitula, but germination rate of seeds produced by infested plants was 15% lower than for uninfested plants at two of three sites studied.     

Host plant oviposition preference of Ceratapion basicorne (Coleoptera: Apionidae), a potential biological control agent of yellow starthistle

Ceratapion basicorne is a weevil native to Europe and western Asia that is being evaluated as a prospective classical biological control agent of Centaurea solstitialis (yellow starthistle) in the United States. Choice oviposition experiments were conducted under laboratory conditions to help assess host-plant specificity of the insect. Mean oviposition rates were highest on C. solstitialis (66% of eggs, on a per replicate basis) followed by Centaurea cyanus (bachelor's button 22%), Centaurea melitensis (6%), Centaurea americana (1%), Saussurea americana (3%) and Carthamus tinctorius (safflower 2%). Adult feeding damage followed a similar pattern; however, there was less oviposition relative to the amount of adult feeding on each of the non-target species than on the target host plant, C. solstitialis. Thirteen safflower varieties were tested, and oviposition occurred on eight of them, at low rates. Adult feeding occurred on all safflower varieties tested, although at rates much lower than on yellow starthistle. The results were intermediate between those of previously reported no-choice laboratory and open field experiments. Overall, the combined results support the hypothesis that C. basicorne is not likely to attack any of the non-target plant species tested here except possibly C. cyanus and C. melitensis, which are both invasive alien plants.     

Using molecular genetics to identify immature specimens of the weevil Ceratapion basicorne (Coleoptera: Apionidae)

Molecular analyses can play a primary role in the process of host specificity evaluation at species and population levels. Here we present an example of their application with a promising candidate biological control agent for yellow starthistle, Centaurea solstitialis L. Although it is highly host specific, Ceratapion basicorne (Coleoptera: Apionidae) can develop on safflower in laboratory tests. A field experiment was conducted to further evaluate host plant specificity; however, it was not possible to rear all larvae to the adult stage, which was necessary for species determination. Therefore molecular genetic methods were used to identify immature specimens. A 731 bp fragment of mtDNA cytochrome C oxidase I gene (COI) was sequenced from 41 individuals of C. basicorne and four congeners: Ceratapion orientale, Ceratapion onopordi, Ceratapion penetrans and Ceratapion scalptum. Intraspecific variability ranged from 0.0% to 0.2%, and interspecific divergences ranged from 1.7% to 17.6%. All larvae that were sequenced from the field study, clearly matched one of the five species, enabling us to unambiguously identify them. Use of molecular genetics to identify larvae should also help the process of foreign exploration, enabling the identification of field-collected larvae, which often provide more reliable host plant associations than field collected adults.     

Larval densities and field hosts of Ceratapion basicorne (Coleoptera: Apionidae) and an illustrated key to the adults of Ceratapion spp. that feed on thistles in the eastern Mediterranean and Black Sea regions

Many members of the tribe Cardueae are invasive weeds, including yellow starthistle (Centaurea solstitialis L.), one of the most important weeds in the Western United States. We examined the root crowns and stems of yellow starthistle and related plants growing in five countries (Armenia, Republic of Georgia, Greece, Russia, and Turkey) where yellow starthistle is native. In its native range, the root crowns and lower stems of yellow starthistle are frequently attacked by the internal feeding larvae of apionid weevils. We present illustrations and a key to the adults of the six apionid species that we reared from yellow starthistle and its relatives: Ceratapion basicorne (Illiger), C. carduorum (Kirby), C. gibbirostre (Gyllenhal), C. onopodri (Kirby), C. orientale (Gerstaecker), and C. penetrans (Germar). The only apionid we reared from yellow starthistle was C. basicorne. In Turkey, where we collected most intensively, 58% of the yellow starthistle at 20 sites had larvae of this weevil, and at sites where C. basicorne was present, there were an average of 1.8 immatures per yellow starthistle plant. This apionid is currently being further researched for its potential as a biological control agent for yellow starthistle.     

Assessing the biological control of yellow starthistle (Centaurea solstitialis L): prospective analysis of the impact of the rosette weevil (Ceratapion basicorne (Illiger))

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Eustenopus villosus (Coleoptera: Curculionidae) Feeding of Herbicide-Resistant Yellow Starthistle (Centaurea solstitialis L.)

A population of yellow starthistle (Centaurea solstitialis L.) near Dayton, Washington developed herbicide resistance in response to repeated applications of picloram and other auxin-type herbicides. Laboratory and field experiments were conducted in 1998 to determine host acceptability and suitability of this herbicide-resistant yellow starthistle population to the biological control weevil Eustenopus villosus (Boheman) (Coleoptera: Curculionidae). In choice and no-choice feeding and oviposition experiments using excised buds, the weevil did not demonstrate a consistent preference for either herbicide-resistant (R) or -susceptible (S) yellow starthistle. When caged on buds of intact plants, the E. villosus feeding rate of 97% did not differ between R and S types. Host plant suitability, measured as larval damage and development to adult weevils, was equivalent in R and S types, with weevils maturing in 46% of the R and in 32% of the S capitula bearing oviposition scars. The number of viable achenes per capitulum was reduced by 87% due to larval feeding, with no difference between R and S types. Observations at the field site where resistance was found revealed oviposition scars on 78% of the late-bud-stage capitula on 23 June 1998 and 73% of the flowering and postflowering capitula on 15 August 1998. Selection for herbicide resistance has not created host incompatibility for E. villosus nor reduced the effectiveness of E. villosus as a biological control agent.     

The effect of Puccinia jaceae var. solstitialis on the yellow starthistle biological control insects Eustenopus villosus and Chaetorellia succinea

Six insect biocontrol agents have been introduced, with limited success, for managing the invasive plant yellow starthistle (Centaurea solstitialis). In 2003, a recently introduced fungal rust agent, Puccinia jaceae var. solstitialis, was approved for release in California. The presence of the rust in this multi-species complex was evaluated for its effect on performance of the two most common insect biocontrol agents for yellow starthistle, Chaetorellia succinea and Eustenopus villosus. To accomplish this, yellow starthistle was planted in 1 m² plots in monocultures at three densities and in a competition replacement series with wild oat (Avena fatua) in both 2006 and 2007. Twenty seedheads were dissected from each plot to evaluate the effect of P. jaceae on seedhead maturation and insect attack rate. In the replacement series experiment in 2007 and in 2006 and 2007 combined, P. jaceae caused a 35% and 20% increase, respectively, in the proportion of mature seedheads compared to total seedheads. However, there were no significant differences in the density experiment in either year or in the replacement series experiment in 2006. Although P. jaceae appeared to have a slight effect on yellow starthistle seedhead maturation, there was no effect of the rust on seedhead attack rates of either insect biological control, regardless of the experiment or year. These results indicate that P. jaceae does not interact significantly with the insect biological control agents for yellow starthistle.     

Biology of Larinus curtus Hochhut (Coleoptera: Curculionidae), a European Weevil for Biological Control of Yellow Starthistle Centaurea solstitialis L (Asteraceae), in the United States

The biology of the weevil Larinus curtus Hochhut was studied in the field in northern Greece and in the laboratory in Rome, Italy, and in Thermi, near Thessaloniki, Greece. The species is univoltine, and adults overwinter in ground litter. Eggs are inserted into the flowers of yellow starthistle (Centaurea solstitialis L.) where the larvae feed mainly on developing achenes, destroying on average over 96% of the seeds in infested flowerheads. Overwintered adults lived up to 84 days, females laid up to 70 eggs each, eggs hatched 4.2 ± 0.6 days after being laid, larvae required 17 to 20 days to develop through the four instars, and pupal development required 4 to 5 days under laboratory conditions. Six percent of 360 seedheads collected on July 13 and 28, 1988 were infested with L. curtus larvae and up to 89% of the larvae were parasitized. The species is recommended for the biological control of C. solstitialis in the United States.     

Increased seed consumption by biological control weevil tempers positive CO2 effect on invasive plant (Centaurea diffusa) fitness

Predicted increases in atmospheric CO₂ and temperature may benefit some invasive plants, increasing the need for effective invasive plant management. Biological control can be an effective means of managing invasive plants, but the anticipated range in responses of plant–insect interactions to climate change make it difficult to predict how effective biological control will be in the future. Field experiments that manipulate climate within biological control systems could improve predictive power, but are challenging to implement and therefore rare to date. Here, we show that free air CO₂ enrichment in the field increased the fitness of Centaurea diffusa Lam., a problematic invader in much of the western United States. However, CO₂ enrichment also increased the impact of the biological control agent Larinus minutus (Coleoptera: Curculionidae) on C. diffusa fitness. C. diffusa plants flowered earlier and seed heads developed faster with both elevated CO₂ and increased temperature. Natural dispersal of L. minutus into the experimental plots provided a unique opportunity to examine weevil preference for and effects on C. diffusa grown under the different climate change treatments. Elevated CO₂ increased both the proportion of seed heads infested by L. minutus and, correspondingly, the amount of seed removed by weevils. Warming had no detectable effect on weevil utilization of plants. Higher weevil densities on elevated CO₂ plants reduced, but did not eliminate, the positive effects of CO₂ on C. diffusa fitness. Correlations between plant development time and weevil infestation suggest that climate change increased weevil infestation by hastening plant phenology. Phenological mismatches are anticipated with climate change in many plant–insect systems, but in the case of L. minutus and C. diffusa in mixed-grass prairie, a better phenological match may make the biological control agent more effective as CO₂ levels rise.     

Orientation behavior of predaceous ground beetle species in response to volatile emissions identified from yellow starthistle damaged by an invasive slug

We investigated indirect defense in the yellow starthistle (Centaurea solstitialis)–grey garden slug (Deroceras reticulatum)–ground beetle (Pterostichus melanarius and Scaphinotus interruptus) system. In this host plant/herbivore/predator system, the ground beetles are the primary predator of D. reticulatum, the dominant herbivore of the highly invasive weed, C. solstitialis. The aim of our study was to examine the behavioral responses of two species of ground beetle to olfactory stimuli emitted from yellow starthistle damaged by D. reticulatum. The beetle P. melanarius showed a significant preference for the odor of damaged yellow starthistle relative to the odor of intact plants, while S. interruptus did not. Volatiles from D. reticulatum-damaged yellow starthistle were collected and identified as trans-β-farnesene, germacrene D, bicyclogermacrene, and 1,5,9-trimethyl-1,5,9-cyclododecatriene. No quantitative relationship was observed between beetle plant choice or decision time and the level of herbivory. Similarly, there was no relationship between volatile compound relative abundance and level of herbivory, suggesting that our range of leaf damage produces either undetectable semiochemicals or no variation in volatile emission.     

How to find a needle in a haystack – host plant finding of the weevil Ceratapion onopordi

The weevil Ceratapion onopordi Kirby (Coleoptera: Apionidae) shows a mutualistic interaction with the rust fungus Puccinia punctiformis (Str.) Röhl (Pucciniaceae). One of the weevil’s host plants, the thistle Cirsium arvense (L.) Scop. (Asteraceae), is also the host of the rust fungus. It has been argued that weevils prefer rust‐infected thistle shoots for egg deposition and consequently should be able to detect such shoots. Olfactory, visual, and gustatory orientation was tested using a four‐chamber olfactometer, a visual testing arena, and feeding choice tests. Whereas the weevils used olfactory cues to find their host plants, visual orientation does not seem to be important. Rust‐infected thistle shoots were not preferred over healthy shoots in any of the tests. We conclude that host plants infected with rust fungi, which are rather rare in the field, appear to be found more or less by chance.     

Sitona weevils (Coleoptera: Curculionidae) as agents for rapid transfer of nitrogen from white clover (Trifolium repens L.) to perennial ryegrass (Lolium perenne L.)

The effects of root feeding by larvae of Sitona hispidulus (F.) (a common weevil pest of white clover) on the rate of transfer of nitrogen between plants of white clover (Trifolium repens L.) and perennial ryegrass (Lolium perenne L.) were investigated using a nutrient slant board technique. Clover plants, labelled with ¹⁵N were grown adjacent to ryegrass plants and were either infested with Sitona larvae or not infested. Ryegrass plants associated with the infested clover plants had a significantly higher dry matter yield and nitrogen content (75% and 74% respectively) than the uninvested plants, after 33 days exposure to insect herbivory. It was concluded that root feeding insects could play an important role in the cycling of nitrogen in grass/clover swards.     

Growth and development of the knapweed root weevil,Cyphocleonus achates,on a meridic larval diet

Cyphocleonus achates, the knapweed weevil, is an effective biological control agent of the invasive weed, Centaurea maculosa Lam. A meridic diet was developed and tested for the rearing of the larval stage of this insect. Using this diet, C. achates was reared for over three generations, with the adults being offered knapweed plants for feeding and oviposition in greenhouse conditions. Slight or no differences were seen between insects reared on a standard meridic diet formulation and one containing knapweed tissues. The following life history parameters were monitored over the three generations: percent egg hatch (ranging from 42.9 to 59.1%), time to egg hatch (20.0–23.2 days), time to adult emergence (52.0–54.1 days), adult weights 3 days post-eclosion (101.9–117.0 mg), percent adult emergence (48.3–58.6%), and percent mortality/deformity in the different stages (with mortality occurring primarily in the early larval stages). Additionally, a study involving low temperature and short day conditions suggested that C. achates could be maintained for longer periods of time in larval diet cells when placed in growth-retarding conditions, although percent adult emergence was lower. External morphology was also studied in order to distinguish between the sexes to ensure that each adult cage had a similar ratio of females to males. Abdominal features were found to be the most dependable characteristics for use when determining the sex of adult C. achates.     

Entomopathogenic nematodes to control black vine weevil (Coleoptera: Curculionidae) on strawberry.

We investigated the potential of heterorhabditid nematodes to control larvae of the black vine weevil, Otiorhynchus sulcatus (F.), in 2 field experiments in commercial strawberry plantings. In both experiments, nematodes were applied directly onto the straw mulch, or onto the soil after temporary removal of the mulch. Heterorhabditis marelatus Lui & Berry (Rhabditida: Heterorhabditidae) reduced numbers of weevil larvae and the percentage of plants infested in both experiments, irrespective of straw removal. In the 1st field experiment, a sponge-packed H. marelatus formulation produced lower numbers of O. sulcatus larvae per strawberry plant (mean O. sulcatus larvae per plant = 0.7) and proportion of infested plants (42%) compared with a vermiculite formulation (mean O. sulcatus larvae per plant = 1.8, proportion infested plants 67%) and an untreated control (mean O. sulcatus larvae per plant = 1.9, proportion infested plants 75%). In the first 2 wk after application, more H. marelatus were found in soil samples collected from plots treated with sponge-packed nematodes, than from plots treated with vermiculite-formulated nematodes. In the 2nd field experiment, sponge-packed formulations of H. bacteriophora Poinar (Rhabditida: Heterorhabditidae) and H. marelatus were tested. H. marelatus caused a reduction in both numbers of weevil larvae (mean O. sulcatus larvae per plant = 0.1) and proportion of infested plants (9%) but H. bacteriophora did not (mean O. sulcatus larvae per plant = 0.45, proportion infested plants 34%). More H. bacteriophora were recovered from soil samples than H. marelatus during the first 7 d of this experiment. However, laboratory studies revealed no difference in the persistence of these 2 nematodes in sand.     

Laboratory and field experimental evaluation of host plant specificity of Aceria solstitialis, a prospective biological control agent of yellow starthistle

Centaurea solstitialis (yellow starthistle, Asteraceae) is an invasive annual weed in the western USA that is native to the Mediterranean Region and is a target for classical biological control. Aceria solstitialis is an eriophyid mite that has been found exclusively in association with Ce. solstitialis in Italy, Greece, Turkey and Bulgaria. The mite feeds on leaf tissue and damages bolting plants, causing stunting, witch’s broom and incomplete flower development. Field experiments and laboratory no-choice and two-way choice experiments were conducted to assess host plant specificity of the mite in Bulgaria. Mites showed the highest degree of host specificity in the field and lowest in the no-choice experiments. In the field, highest densities of mites occurred on Ce. solstitialis and Ce. cyanus (bachelor’s button), and either no mites or trace numbers occurred on the other test plants: Ce. diffusa (diffuse knapweed), Carthamus tinctorius (safflower) and Cynara scolymus (artichoke). In no-choice experiments, mites persisted for 60 days on Ce. diffusa, Ce. cyanus, Ce. solstitialis, Ca. tinctorius and Cy. scolymus, whereas in two-way choice experiments mites persisted on 25% of Cy. scolymus plants for 60 days and did not persist on Ca. tinctorius beyond 40 days. The eight other species of plants that were tested in the laboratory were less suitable for the mite. These results suggest that although A. solstitialis can persist on some nontarget plants for as long as 60 days in the laboratory, it appears to be much more specific under natural conditions, and warrants further evaluation as a prospective biological control agent.     

Studies on host preference and its biological effects on the Red Palm weevil,Rhynchophorus ferrugineus Olivier in Egypt B. vegetable crops

The investigation on some Egyptian vegetables preference by the Red Palm weevil (RPW), Rhynchophorus ferrugineus has been carried out under laboratory conditions to explore a suitability of alternative host plants. The choice test of insect larvae showed that Taro, Squash, Eggplant, common potato, yellow carrot, tomato and sweet pepper were accepted food, while the Table beet (Vegetable) was rejected. Non-choice feeding of R. ferrugineus larvae on vegetables affected larval body weight and increased larval mortality. Highest rate of pupation was recorded from larvae fed on C. pepo (92%) and B. vulgaris (97%). Adult emergence reached 80% and 92% on C. pepo and Sugar beet (field crop) (field crop). The external skin of sugar cane was not acceptable food for insect larvae, while injured sites and internal soft fibres were preferred as food. Therefore, vegetable fruits, stem of sugarcane are believed to be the most vulnerable hosts for red weevil attack. The alternative host plant examined can be used to monitor the dynamics of the population of RPW in order to take effective preventive measures and most powerful tool available for use in pest management.     

Penetration of Crotalaria juncea,Dolichos lablab,and Sesamum indicum Roots by Meloidogyne javanica

Penetration of Crotalaria juncea (PI 207657 and cv. Tropic Sun) Dolichos lablab cv. Highworth, and Sesamum indicum by juveniles (J2) of Meloidogyne javanica was assessed to investigate the mechanism by which these plants may reduce nematode numbers in the field. Growth chamber experiments were conducted at 25 C, with vials containing 90 g sand infested with 450 J2; tomato (UC 204 C) was included as a susceptible host. Fifteen days after inoculation, roots were stained and the nematodes within stained roots were counted. Both C. juncea lines were highly resistant to penetration, as they contained significantly fewer nematodes per cm of root and per root system than the other plants. Although containing more nematodes per cm of root than C. juncea, S. indicum and D. lablab had significantly fewer nematodes per root system and per cm of root than tomato. Roots were significantly longer in the plants with the lowest nematode penetration. Although C. juncea, D. lablab, and S. indicum may have potential utility as cover or rotation crops in soil infested with M. javanica, further quantitative information on the reproduction of M. javanica and other nematodes in these plants is needed.     

Non-target plant use by a weed biocontrol agent in idaho: host expansion or opportunistic behavior?

Larinus curtus Hochhuth (Coleoptera: Curculionidae) was first introduced into the western United States from Greece for the biological control of yellow starthistle (YST), Centaurea solstitialis L., in 1992. The discovery of L. curtus adults in the open flowerheads of safflower (SF), Carthamus tinctorius L., near Lewiston, Idaho in 2007 suggested this weevil might be expanding its host range to include a non-target crop species closely related to YST. In 2008 field plots near the 2007 observation site, 92 L. curtus adults fed in open SF flowerheads (pollen feeding and minor feeding on corolla tubes). No eggs were found in the ovarioles of 19 pollen-feeding females. No eggs, larvae, or evidence of larval feeding were detected in 39 tagged SF capitula, and no adults emerged from approximately 7,135 post-flowering SF capitula. These collective results are not indicative of an expanding developmental host-range of L. curtus. Also, they are consistent with pre-release host-specificity test results.     

A mechanistic model of pollinator-mediated gene flow in agricultural safflower

In many species of crop plant, gene flow by cross-pollination is possible between spatially separate fields. To preserve a crop's varietal purity or to restrict ingress into conventional varieties of genetically modified (GM) genes, a quantitative understanding of gene flow is useful. Previous measurements of gene flow in safflower (Carthamus tinctorius L.), a crop with GM varieties, were made in plots of less than 1 ha. Here, I evaluate a mathematical model of field-to-field gene flow due to insect pollination using parameter values appropriate to a large agricultural field of safflower. The model was solved based on laboratory pollination experiments and observations made on a large (40 ha) safflower field in Lethbridge, Canada that was pollinated by honey bees (Apis mellifera) and bumble bees (Bombus spp.). The model estimated the maximum feasible level of bee-mediated, field-to-field gene flow to range between 0.05% and 0.005% of seed set (95% upper confidence intervals of 0.23% and 0.023%), depending on the composition of the bee fauna. These relatively low values emerged for two reasons: safflower has a high capacity for automatic self-fertilization; and bees undertook long foraging bouts in the field, which made between-field pollinations relatively rare. A strategy for minimizing GM gene flow should utilize a conventional safflower variety that has a high capacity for automatic self-fertilization and should allow the conventional plants to grow in large stands to encourage long foraging bouts by bees.