Importance of long-term research in classical biological control: an analytical review of a release against the cabbage seedpod weevil in North America

Abstract:  Cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Col., Curculionidae), is an invasive alien pest that is spreading in North America. To aid with planning for introductions of European parasitoids in North America, we examined the status of the only classical biological control release against this pest in North America, which in 1949 introduced Mesopolobus morys , Stenomalina gracilis and Trichomalus perfectus (Hym., Pteromalidae). Weevils and parasitoids were reared in 2005 from mass collections of seedpods of Brassica napus , Brassica rapa and Raphanus raphanistrum (Brassicaceae) from 18 sites in the Fraser Valley, near Vancouver, British Columbia, Canada. Of the three European parasitoid species that were originally released, only S. gracilis was found. The predominant hymenopterous parasitoid species were Trichomalus lucidus , S. gracilis , Mesopolobus moryoides (Pteromalidae), Necremnus tidius (Eulophidae) and Eupelmus vesicularis (Eupelmidae). These constituted over 97% of the parasitoids reared, although overall parasitism was low. Only M. moryoides is clearly North American in distribution; other than S. gracilis , the remaining species were either accidentally introduced or are Holarctic in distribution. Based on these results, re-releases of M. morys and T. perfectus in North America should be considered as part of a classical biological control programme. However, redistribution of S. gracilis is not recommended at present because of potential conflicts with biological control programmes against weeds. Ongoing re-examination of classical biological control programmes can further our understanding of failure of release programmes, particularly when re-examination can be made in the light of improved taxonomy and systematics of the target and agent species.     

Survey of parasitoids (Hymenoptera: Pteromalidae) of house fly (Diptera: Muscidae) pupae from broiler-breeder poultry houses in northwest Arkansas

Parasitoids were collected from broiler-breeder poultry houses in northwest Arkansas using sentinel bags containing house fly, Musca domestica L., pupae. At least five species of Pteromalidae were collected over a two-year sampling period: Pachycrepoideus vindemiae (Rondani), Spalangia endius Walker, S. cameroni Perkins, Muscidifurax spp., and Nasonia vitripennis (Walker).     

Establishment of Peristenus digoneutis and P. relictus (Hymenoptera: Braconidae) in California for the control of Lygus spp. (Heteroptera: Miridae)

Lygus hesperus Knight is native to the western United States and is a perennial pest of numerous crops in California. It is responsible for triggering the early season application of insecticides on cotton, Gossypium hirsutum L., and strawberries, Fragaria L. Despite several surveys conducted in alfalfa (Medicago sativa L.) grown in central California, nymphal parasitoids associated with L. hesperus and L. elisus have not been found. Two exotic parasitoids were released into California beginning in 1998. Peristenus relictus (Ruhte), formerly P. stygicus Loan, and P. digoneutis Loan were collected from several locations in southern Europe and released at up to six locations over a 6-year period. At the original release site in Sacramento, a 0.25-ha plot of alfalfa, parasitism by P. digoneutis and P. relictus combined increased from zero to 90%, 3 years after the last releases were made. Parasitoids have been recovered from vacant fields of weedy annuals within 2 km of this site. Recoveries at more southerly release sites in central California have been poor.     

Comparative survey of the phytophagous arthropod faunas associated with Lepidium draba in Europe and the western United States,and the potential for biological weed control

Hoary cress (Lepidium draba L.) is an invasive perennial mustard (Brassicaceae) introduced to North America from Eurasia. In 2001 we initiated a program to investigate the potential for classical biological control of this weed in the US. Literature and field surveys for the arthropods associated with L. draba were conducted on both continents. Field surveys began in Europe in 2001, and in 2002–2003 standardized surveys were conducted in both Europe and the western US. These field surveys resulted in 80 new host records for L. draba in Europe, and 37 new host records in the US. Although total species richness was nearly four times greater in Europe, there were approximately equal proportions of oligophagous and polyphagous species in each range. Monophagous species were only encountered in the European surveys. The literature surveys revealed that the arthropod fauna associated with L. draba is fairly well known in Europe (175 species), but not in the US (eight species), where the literature was virtually derelict of host records. In both the literature and field surveys, the order Coleoptera contained the most species (>50%) in Europe, whereas the order Hemiptera contained the most species (>40%) in the US. Nearly one-half of the species found in literature and field surveys are flower or seed feeders and the other half are primarily foliage or stem feeders. Ten potential biological control agents were discovered from the surveys, of which four are currently being investigated at the CABI Bioscience Centre in Switzerland. The phenologies of these four species are briefly described.     

Mortality of olive fruit fly pupae in California

Efforts to control the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae), in California have focused on insecticidal baits and biological control by parasitoids, which primarily target the adult and larval stages, respectively. The pupal stage, which occurs in the soil, has largely been overlooked. This study investigated mortality factors for olive fruit fly pupae in California olive orchards, using a combination of exclusion experiments and observation and trapping of potential predators. Results show predation and climatic factors contribute to pupal mortality. Ants (Formicidae) were the most numerous predators observed. Soil-borne pathogens caused no mortality in this study. Potential applications of these results in the development of a sustainable management program are discussed.     

The Distributions of Parasitoids (Hymenoptera) of Anastrepha Fruit Flies (Diptera: Tephritidae) along an Altitudinal Gradient in Veracruz, Mexico

In the state of Veracruz, Mexico, fruits from 38 sites at various altitudes were collected monthly over a period of 2 years, and the tephritid fruit flies of the genus Anastrepha and associated parasitoids that emerged from these fruits were identified and counted. Of the 26 species of fruits that contained Anastrepha larvae, 18 species also contained a total of 10 species of Anastrepha parasitoids. These consisted of 4 native and 1 exotic species of opiine braconid larval–pupal parasitoids, 2 native species of eucoilid larval–pupal parasitoids, 1 exotic species of eulophid larval–pupal parasitoid, 1 exotic species of pteromalid pupal parasitoid, and 1 native species of diapriid pupal parasitoid. Overall parasitism (including flies from fruit species that bore no parasitoids) was 6% and was greatest, 16%, at 600–800 m in altitude. The relative contributions of individual parasitoid species to overall parasitism were frequently influenced by both the altitude (and correlated changes in temperature and precipitation) and the species of plant in which the Anastrepha larvae were found. This was particularly the case among the more abundant and widespread Braconidae. To distinguish the role of altitude from that of the distributions of the host plants, these braconids were examined in 4 individual species of fruit that grew over a broad range of altitudes. In guava (Psidium guajava L.) and “jobo” (Spondias mombin L.) the parasitoid Doryctobracon areolatus (Szepligeti) was relatively more common at low altitudes. Its congener, Doryctobracon crawfordi (Viereck), was relatively more abundant at high altitudes in sour orange (Citrus aurantium L.). Utetes anastrephae (Viereck) became relatively more common at higher altitudes in S. mombin, whereas Diachasmimorpha longicaudata (Ashmead) tended to become relatively rare at the highest altitudes in C. aurantium, but increased at high altitudes in P. guajava compared to other braconids. Different altitudinal patterns of abundance in different fruits suggests the importance of both biotic and abiotic factors in parasitoid distributions. We discuss the effect of an expanding agricultural frontier on parasitoid abundance and relate our findings to the design of a fruit fly biological control program that tailors mass releases to parasitoid climate preferences.     

PCR–RFLP assays for discerning three weevil stem feeders (Ceutorhynchus spp.) (Col.: Curculionidae) on garlic mustard (Alliaria petiolata)

Polymerase chain reaction–restriction fragment length polymorphism (PCR–RFLP) assays were developed to rapidly and cost-effectively differentiate the morphologically indistinguishable larval stages of three species, Ceutorhynchus alliariae, C. roberti and C. scrobicollis, proposed for the biological control of Alliaria petiolata. A PCR–RFLP using TaqαI restriction enzyme can differentiate the three target species only, while a PCR–RFLP double digestion using the restriction enzymes AluI and TaqαI should enable, based on virtual digestion, distinguishing them from 12 other Ceutorhynchus species associated with A. petiolata.     

Spatial patterns of Trybliographa rapae parasitism of Delia radicum larvae in oilseed rape and cauliflower

Trybliographa rapae (Westwood) is an important parasitoid of Delia radicum (L.). Parasitism of D. radicum larvae by T. rapae in relation to host density on canola (oilseed rape) and cauliflower roots was examined at 10 field sites in Germany and Switzerland. For roots with host larvae, the proportion of roots with one or more parasitized hosts increased with increasing host density. However, for these infested roots, the parasitism of individual larvae was not consistently related to host density. When considering only roots on which there were parasitized larvae and the opportunity for multiple attacks, the proportion of larvae that were parasitized decreased with increasing host density in the field locations, and in a cage study under controlled conditions. A model of patch‐finding and number of attacks by female parasitoids suggests that patch‐finding is density‐dependent, but that low attack rate and interference effects limit numbers of attacks to three or less per visit to a host patch; the reduced number of attacks per visit leads to the inverse relationship of larval parasitism with host density in the host patches visited. The interplay of the density‐dependent and inversely density‐dependent processes appears to be responsible for the inconsistency of density dependence of overall larval parasitism in this and previous studies. In the laboratory, adult female T. rapae parasitized hosts at ≤4 cm deep in soil, but not at 6 cm deep. From the depth distribution of larval feeding sites in the field, we infer that between 4% and 20% of Delia larvae may be in a physical refuge from T. rapae parasitism, which may have a stabilizing influence on the host–parasitoid interaction.     

Intraguild predation and successful invasion by introduced ladybird beetles

Introductions of two ladybird beetle (Coleoptera: Coccinellidae) species, Coccinella septempunctata and Harmonia axyridis, into North America for aphid biocontrol have been followed by declines in native species. We examined intraguild predation (IGP) between larvae of these two exotic species and larvae of the two most abundant native coccinellids in eastern Washington State, C. transversoguttata and Hippodamia convergens. In pairings between the two native species in laboratory microcosms containing pea (Pisum sativum) plants, neither native had a clear advantage over the other in IGP. When the natives were paired with either Harmonia axyridis or C. septempunctata, the natives were more frequently the victims than perpetrators of IGP. In contrast, in pairings between the exotic species, neither had an IGP advantage, although overall rates of IGP between these two species were very high. Adding alternative prey (aphids) to microcosms did not alter the frequency and patterns of relative IGP among the coccinellid species. In observations of encounters between larvae, the introduced H. axyridis frequently survived multiple encounters with the native C. transversoguttata, whereas the native rarely survived a single encounter with H. axyridis. Our results suggest that larvae of the native species face increased IGP following invasion by C. septempunctata and H. axyridis, which may be contributing to the speed with which these exotic ladybird beetles displace the natives following invasion.     

Susceptibility of Various Species of Lepidopterous Pupae to the Entomogenous Nematode Neoaplectana carpocapsae

The susceptibility of certain species of lepidopterous pupae occurring in different ecological situations to the entomogenous nematode, Neoaplectana carpocapsae, was tested. Soil- or litter-pupating lepidopterous insects were not highly susceptible to N. carpocapsae. The most susceptible insect pupating in the soil was Spodoptera exigua with 63% pupal mortality, while Harrisinia brillians, which pupates in litter, had 55% mortality. Other soil- and litter-pupating insects had mortalities of less than 25%. Some insect species that pupate above ground were highly susceptible (> 84% mortality) to N. carpocapsae infection.