Western corn rootworm (Diabrotica virgifera virgifera LeConte) population dynamics

1 The western corn rootworm Diabrotica virgifera virgifera LeConte is a major insect pest of field maize, Zea mays L. Larvae can cause substantial injury by feeding on maize roots. Larval feeding may destroy individual roots or root nodes, and reduce plant growth, stability, and yield. Costs associated with managing corn rootworms in continuous maize are annually one of the largest expenditures for insect management in the United States Corn Belt.
2 Even though D. virgifera virgifera has been studied intensively for over 50 years, there is renewed interest in the biology, ecology, and genetics of this species because of its ability to rapidly adapt to management tactics, and its aggressive invasive nature.
3 This article provides a comprehensive review of D. virgifera virgifera population dynamics, specifically: diapause, larval and adult development, seasonality, spatial and temporal dynamics at local and landscape scales, invasiveness in North America and Europe, and non-trophic interactions with other arthropods.
4 Gaps in current knowledge are identified and discussed especially within the context of challenges that scientists in North America and Europe are currently facing regarding pest dynamics and the need to develop appropriate management strategies for each geographic area.     

Development and economic evaluation of spatial sampling plans for corn rootworm Diabrotica spp. (Col., Chrysomelidae) adults

Abstract  To develop spatial sampling plans for corn rootworm ( Diabrotica spp.) adults, their spatial distributions were characterized and economics of sampling plans were evaluated by comparing sampling costs between spatial and conventional (non-spatial) sampling plans. Semivariogram modelling and spatial by with distance indices showed that corn rootworm adults were significantly (P < 0.05) aggregated at peak population densities and any two samples were spatially correlated within approximately 45 m, with 39–90% of the variability explained by spatial dependence. Sampling costs for spatial sampling plans linearly increased as the sampling distance decreased and exponentially increased as the field size increased. Although sampling costs for non-spatial sampling plans were generally lower, spatial sampling plans could be more economical when the mean insect density became lower and the field size became smaller. This study demonstrated that spatial sampling plans could be optimized to minimize the sampling costs and maximize the spatial resolution.     

Influence of corn planting date on the life stage development and phenology of Diabrotica virgifera virgifera

Under field conditions in eastern South Dakota, USA three different planting dates of corn and three times of egg infestation were used to imposed synchronous and asynchronous timing of corn growth and Diabrotica virgifera virgifera LeConte egg hatch and subsequent development. Median occurrence of each of the three larval stages and of the adult stage for each of the infestation-planting treatments was determined by relating occurrence to thermal units and to days after infestation. No significant differences were found among the treatments for median occurrence of each life stage when the thermal unit approach was used. However, significant differences were found among treatments for median occurrence when the day after infestation approach was used. Consistent parameters are needed for prediction of the occurrence of life stages of this insect. Despite the various imposed conditions, this study indicates that the least variable method of predicting life stage occurrence and adult emergence of D. v. virgifera was the use of thermal unit accumulations (base 11°C).

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Résumé Dans les conditions de l'est du Sud Dakota (USA), 3 dates de semailles de maïs et 3 dates de contamination avec des ufs de D. virgifera virgifera LeConte ont servi à imposer ou à empêcher la synchronisation des éclosions des ufs et par conséquent des développements ultérieurs. Les dates médianes d'apparition de chacun des 3 stades larvaires et des imagos ont été déterminées en relation avec les unités de température et le nombre de jours depuis la contamination. Aucune différence significative entre les dates médianes d'apparition n'a été mise en évidence par utilisation des unités de température; par contre, ces différences deviennent significatives lorsque l'on utilise le nombre de jours depuis la contamination. Des paramètres fiables sont nécessaires pour prédire la présence des différentes stades de cet insecte. En dépit des différentes conditions imposées pour cette étude, la méthode la moins capricieuse pour prédire l'apparition d'un stade larvaire et l'émergence des adultes est la somme de températures avec une base de 11°C.

     

Factors influencing the aggregative response of the blue willow beetle, Phratora vulgatissima

Crop rotation has traditionally been a valuable method for managing pests, but now a serious insect pest of maize (Diabrotica virgifera virgifera LeConte [Coleoptera: Chrysomelidae]) has developed behavioral resistance to rotation. A simple model of adult behavior and population genetics can explain how this resistance may have developed. This general model indicates that evolution may be caused by selection on a single gene for adult movement and that behavioral resistance only develops at high levels of rotation (>80% of plant landscape). In less diverse landscapes, crop rotation selects for the expansion of host preferences (polyphagy) by adults. More diverse landscapes may delay the evolution of resistance to crop rotation depending on the fitness costs and the nature of the genetic system.     

Impact of cysteine proteinase inhibition in midgut fluid and oral secretion on fecundity and pollen consumption of western corn rootworm (Diabrotica virgifera virgifera)

Cysteine proteinases predominate in the midgut fluid (MF) and oral secretion (OS) of adult western corn rootworm (WCR) based on their mild acidic pH optima (pH 6.0), enhanced activities after treatment with thiol reducing agents, and inhibition by selective cysteine proteinase inhibitors (PIs). Four cysteine PIs including E-64, calpeptin, calpain inhibitor II, and leupeptin (also a serine PI) strongly inhibited azocaseinolytic activity in a dose-dependent manner in both the MF and OS. The most significant effect on adult female WCR of cysteine PI consumption with corn pollen was the reduction in fecundity, but female survival was not apparently affected. Mean fresh weights for all PI-fed females were also lower than control groups. All PI-fed groups [E-64, calpain inhibitor I (Cal I) and leupeptin] had a significantly lower daily egg production than respective corn pollen-fed controls. E-64 was more potent than leupeptin and Cal I on inhibiting fecundity, which correlates with their relative anti-proteinase potency in vitro. E-64, Cal I, and leupeptin at 1.5-2 nmol/beetle/day reduced fecundity down to 25-45% of control values. Reduced egg production by PI-fed beetles results from a combination of the direct inhibition of protein digestion and a post-ingestive negative feedback mechanism, which reduces food intake. The supplement of ten essential amino acids into the E-64-treated pollen enhanced up to 3.7-fold the number of eggs laid compared to the E-64-fed group without these amino acids, suggesting that egg production is dependent on the supply of essential amino acids from corn pollen proteolysis.     

Whorl and pollen-shed stage application of Beauveria bassiana for suppression of adult western corn rootworm

The corn rootworm complex is the most damaging insect pest of corn (Zea mays L.). This study was conducted to determine the efficacy of whorl and pollen-shed stage applications of a granular formulation of Beauveria bassiana (Balsamo) Vuillemin for control of adult western corn rootworm (Diabrotica virgifera virgifera Le Conte). The effect of application time (whorl-stage, pollen-shed) and plant surface exposed (leaves and leaf collars; silks; leaves, leaf collars, and silks) on level of beetle fungal infection were investigated. In addition, the number of colony forming units of B. bassiana in the corn leaf collar area was quantified. In the three years (1998–2000) of the study, application of B. bassiana at whorl-stage did not significantly increase beetle fungal infection. Beauveria bassiana applied to plants at pollen-shed in 1998 resulted in a significant increase in beetle infection with 51% of beetles from treated plants infected and 6.0% from control plants. Similar applications at pollen-shed in 1999 and 2000 resulted in very low infection levels. Beauveria bassiana application at pollen-shed stage significantly increased the number of colony forming units per leaf collar during all years of the study. Beetle infection with B. bassiana did not differ consistently among plant surface to which beetles were exposed for either application. Increased fungal load in leaf collars was not correlated with increased levels of adult infection. Increased rates of B. bassiana and application when beetles are present on the plants are likely needed to significantly increase infection rates.     

Influence of adult diet on the reproductive biology and survival of the western corn rootworm,Diabrotica virgifera virgifera

Adult corn rootworm beetles,Diabrotica virgifera virgifera LeConte, were maintained on three dietary regimes which mimicked the progression of corn tissues that would be available in the field for beetles eclosing when corn was in the following growth stages: (A) after tassels had emerged but prior to silking and pollen shed; (B) while plants were silking and shedding pollen; and (C) after pollination was complete and silks had turned brown. A fourth regime (D) was established in which green corn silks, pollen, and leaves were provided throughout the study. The mean number of eggs laid per female over the 12-week duration of the study was 125, 235, 179, and 441 for regimes A, B, C, and D, respectively. Median length of life was 7.2, 7.2, 6.7, and 8.8 weeks for regimes A, B, C, and D respectively. Beetles in regime A laid a greater proportion of their eggs at an older age than did beetles from regimes B and C. To further investigate the influences on survival of changes in food quality of corn as plants and beetles aged, newly-eclosed beetles and beetles that had been maintained in caged plots of corn growing in a greenhouse for various lengths of time were caged on corn at different stages of growth, and the proportion of beetles surviving for 48 h was determined. Survival decreased as plants aged for both groups of beetles, but decreased at a faster rate for old than for young beetles.

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Influence de l'alimenation sur la reproduction et la survíe deDiabrotica virgifera virgifera

Résumé D. virgifera virgifera LeConte a été placé sur des régimes nutritifs mimant l'évolution des tissus du maïs disponsibles dans le champ lorsque les insectes éclosent est aux stades suivants du maïs: 1) après émergence de l'épi mâle, mais avant l'apparition des barbes et l'émission du pollen; 2) lors de la présence de barbes et de l'émission de pollen; 3) après la pollinisation et quand les barbes ont bruni. Un quatrième régime a été fourni pendant toute l'expérience comprenant des barbes vertes, du pollen et des feuilles. Les pontes moyennes des femelles pendant les 12 semaines de l'étude on été 125, 235, 179 et 441 pour les régimes 1, 2, 3 et 4. Les dates de mort de la moitié des adultes a été 7,2, 7,2, 6,7 et 8,8 semaines pour respectivement les mêmes régimes. Les femelles du régime 1 pondent à un âge plus avancé que les femelles des régimes 2 et 3. L'influence des changements de la qualité alimentaire du maïs au fur et à mesure du vieillissement des plantes et deDiabrotica, a été déterminée par la survie au bout de 48 heures d'insectes éclos depuis peu et d'autres maintenus en cage sur des lots de maïs à différents stades poussant en serre depuis des temps plus ou moins longs. Plus les plantes sont âgées, plus la survie des 2 groupes deDiabrotica diminue, mais plus vite chez les lots d'insectes âgés.

     

Polymorphic microsatellite loci from the western corn rootworm (Insecta: Coleoptera: Chrysomelidae) and cross‐amplification with other Diabrotica spp

Corn rootworms (Diabrotica spp.) make up the major insect pest complex of corn in the US and Europe, and there is a need for molecular markers for genetics studies. We used an enrichment strategy to develop microsatellite markers from the western corn rootworm (Diabrotica virgifera virgifera). Of 54 loci isolated, 25 were polymorphic, and of these, 17 were surveyed for variability in 59 wild individuals. In addition, the potential for cross‐amplification of these microsatellites was surveyed for Mexican, northern, and southern corn rootworms. Nine microsatellite loci showed Mendelian inheritance and are likely to be useful in population genetics studies.     

Entomopathogenic fungi in cornfields and their potential to manage larval western corn rootworm Diabrotica virgifera virgifera

Entomopathogenic ascomycete fungi are ubiquitous in soil and on phylloplanes, and are important natural enemies of many soil-borne arthropods including larval western corn rootworm, Diabrotica virgifera virgifera, which is a major pest of corn. We measured the prevalence of Beauveria bassiana and Metarhizium anisopliae sensu lato in ten cornfields in Iowa, USA by baiting with larval insects. B. bassiana and M. anisopliae s.l. were present in 60% ± 6.3% and 55% ± 6.4% of soil samples, respectively. Subsequent laboratory bioassays found that some M. anisopliae s.l. strains collected from cornfields killed a greater proportion of D.v. virgifera larvae than a standard commercial strain.     

Characterizing laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae) selected for survival on maize containing event DAS-59122-7

Event DAS‐59122‐7 is a novel transgenic trait designed to protect the roots and yield potential of maize from the insect pest corn rootworm Diabrotica spp. (Col.: Chrysomelidae). The increased pest status of corn rootworm, exceptional efficacy of this trait, and anticipated increases in farm efficiency and grower and environmental safety will drive adoption of this trait. Strong grower acceptance of this trait highlights the importance of science‐based and practical resistance management strategies. A non‐diapause trait was introgressed into two laboratory colonies of Diabrotica virgifera virgifera collected from geographically distinct locations: Rochelle, IL and York, NE. Both colonies were divided and each reared on maize containing event DAS‐59122‐7 or its near isoline. Selected and unselected colonies were evaluated for phenotypic change in larval development, injury potential and survival to adulthood during 10 and 11 generations. The F1 generation of both selected colonies displayed increased larval development, survivorship and measurable, but economically insignificant increases in injury potential on DAS‐59122‐7 maize. Survival rates of 0.4 and 1.3% in F1 generations of both selected colonies corroborate field estimates of survival on DAS‐59122‐7 maize. Over later generations, total phenotypic variation declined gradually and irregularly. Despite the absence of random mating, the tolerance trait could not be fixed in either population after 10 or 11 generations of selection. An allele conferring major resistance to DAS‐59122‐7 was not identified in either selected colony. The assessment also concluded that major resistance gene(s) are rare in populations of D. v. virgifera in the United States, and that a minor trait(s) conferring a low level of survival on DAS‐59122‐7 maize was present. The tolerance trait identified in this study was considered minor with respect to its impact on DAS‐59122‐7 maize efficacy, and the role this trait may play in total effective refuge for major resistance genes with recessive inheritance is the basis of future work.     

Assessing host specificity of a classical biological control agent against western corn rootworm with a recently developed testing protocol

Celatoria compressa (Wulp) (Diptera: Tachinidae), a parasitoid of adult chrysomelid beetles in the subtribe Diabroticina in North America, has been selected as a candidate for classical biological control of the alien invader, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae: Galerucinae), into Europe. We conducted host specificity testing to evaluate the fundamental host range of C. compressa and potential risks to native European coleopteran species. Nine potential non-target beetles were tested for host selection with D. v. virgifera in no-choice tests, sequential no-choice tests, choice tests and sequential choice tests in small experimental arenas in a quarantine laboratory. The nine representative non-target species were selected for experimentation based on (1) ecological host range information of C. compressa, (2) ecological similarities to D. v. virgifera, (3) close phylogenetic/taxonomic relationships, (4) safeguard considerations, (5) morphological similarities, geographical distributions, overlap of temporal occurrences with D. v. virgifera and C. compressa, and (6) accessibility and availability. Of the potential nine non-target hosts tested, gravid C. compressa only parasitized a few red pumpkin beetles, Aulacophora foveicollis (Chrysomelidae: Galerucinae), regardless of the presence or absence of D. v. virgifera. However, C. compressa significantly preferred D. v. virgifera (44.6% parasitized) over A. foveicollis (2.7%) in choice tests. Of the 1110 A. foveicollis tested among all experiment types, only 23 were parasitized and only one C. compressa successfully developed from the parasitism, demonstrating that A. foveicollis is a poor host. In conclusion, C. compressa has a fundamental host range restricted to the subtribes Diabroticina and Aulacophorina, and would therefore be unlikely to have a direct impact on indigenous species in Europe.     

The contribution of prehatch and posthatch development to protandry in the chrysomelid Diabrotica virgifera virgifera

Laboratory tests with eggs of Diabrotica virgifera virgifera LeConte showed that during a 10-day hatching period, hatch of male eggs predominated on the first and second days, eggs of mixed sex, with ca. 1:1 ratio, hatched on the third and fourth days, and eggs hatching from the fifth to the tenth days were nearly all female. Overall, female eggs hatched a mean of 2.9 days later than male eggs. Not only did female eggs hatch later, but the time for posthatch development to the adult stage was 1.8 days longer for females. The later egg hatch and longer posthatch development for females resulted in female adults emerging a mean of 4.7 days later than male adults. Total adult emergence lasted 14 days; of this, males predominated during the first 5 days, and females predominated during the last 9 days. Males of D. v. virgifera appear to have evolved protandry (the tendency for males to emerge before females) by developing both a postdiapause embryonic stage and a combined larval and pupal stage of shorter duration.

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Résumé L'observation, au laboratoire, pendant une période d'éclosion de dix jours, des oeufs de D. v. virgifera LeConte, a montré que les oeufs mâles prédominent les deux premiers jours d'éclosion, que les oeufs des deux sexes, avec des fréquences 0,5/0,5, ont éclos les troisième et quatrième jours, et que les oeufs éclos du cinquième au dixième jour étaient presque tous femelles. Globalement, les oeufs femelles ont éclos en moyenne 2,9 jours plus tard que les oeufs mâles. De plus, la durée du développement post-embryonnaire des femelles a demandé 1,8 jour en plus. Une éclosion plus tardive et un développement post-embryonnaire plus long ont entrainé une émergence des femelles en moyenne 4,7 jours après les mâles. La période d'émergence des adultes s'est étalée sur 14 jours; les mâles ayant dominé pendant les 5 premiers jours et les femelles pendant les 9 derniers. Les mâles de D. v. virgifera semblent avoir évolué vers la protandrie en acquerant, tant une diapause post-embryonnaire que des stades de développements larvaire et nymphal plus brefs.

     

Survey for natural enemies of the invasive alien chrysomelid, Diabrotica virgifera virgifera, in Central Europe

The western corn rootworm, Diabrotica virgifera virgifera LeConte(Coleoptera: Chrysomelidae), is the mostdestructive pest of maize (Zea mays L.)in North America, and began to successfullyinvade Central Europe in the early 1990's. Thispaper reports a three-year field surveyconducted in Hungary, Yugoslavia, and Croatia,which are currently the focal points ofinvasion, with the aim to determine theoccurrence of indigenous natural enemies ofD. v. virgifera in Europe. A total of9,900 eggs, 550 larvae, 70 pupae and 33,000adults were examined for the occurrence ofparasitoids, nematodes, and fungal pathogens. It can be concluded from the survey resultsthat effective indigenous natural enemies arenot attacking any of the life stages of D.v. virgifera in Europe. The exception is theoccurrence of the fungi Beauveriabassiana (Bals.) Vuill. (Mitosporic fungi;formerly Deuteromyces) and Metarhiziumanisopliae (Metsch.) Sorok (Mitosporic fungi)attacking adults of D. v. virgifera at anextremely low level (< 1%). However no otherentomopathogenic fungal pathogens,entomopathogenic nematodes, or parasitoids werefound on eggs, larvae, pupae or adults. Whileseveral natural enemies in North and CentralAmerica are known to attack D. v.virgifera, it is apparent that indigenousnatural enemies in Europe have not adapted tothe high population density of the alieninvasive species D. v. virgifera. Classical biological control may provide anopportunity to reconstruct the natural enemycomplex of an invading alien pest, and itsapplication to manage D. v. virgiferapopulations in Europe should be considered.     

<Emphasis Type="Italic">Trichogramma Brassicae</Emphasis> and SLAM<Superscript>®</Superscript>, an Integrated Approach to Managing European Corn Borer and Corn Rootworms

European corn borer, Ostrinia nubilalis (Hübner) (Lepidoptera: Crambidae); western corn rootworm (WCRW), Diabrotica virgifera virgifera LeConte; and northern corn rootworm (NCRW), Diabrotica barberi (Smith & Lawrence) (Coleoptera: Chrysomelidae) are important pests of corn, Zea mays L., that occur simultaneously in the US Corn Belt. Areawide management strategies for northern and western corn rootworm in Iowa, Kansas, South Dakota, Illinois, and Indiana, and for the Mexican strain in Texas, use SLAM^®, which contains cucurbitacin, a feeding stimulant, and a small amount of the insecticide carbaryl. This management strategy is environmentally sound because it introduces a substantially lesser amount of chemical insecticide into the environment than prophylactic soil insecticide applications for WCRW management. To develop a management program for both corn pests, the compatibility of SLAM^® to control CRW, along with a biological agent to manage European corn borer, was investigated. Laboratory studies were conducted using the egg parasitoid Trichogramma brassicae (Bezdenko) (Hymenoptera: Trichogrammatidae). In experiments in which SLAM^® and T. brassicae were evaluated as components of a management system, SLAM^® did not affect parasitism or parasitoid emergence rates. Trichogramma brassicae displayed vigorous biotic fitness, emergence rates, sex ratios, and fecundity over the duration of the study. Data collected under these laboratory conditions indicated that SLAM^® had no adverse effect on the quality of T. brassicae, indicated by its ability to reproduce in the filial generation.     

The inhibitory effects of the cysteine protease inhibitor, oryzacystatin, on digestive proteases and on larval survival and development of the southern corn rootworm (Diabrotica undecimpunctata howardi)

At least eight proteolytic activities have been identified in the midgut contents of larval Southern corn rootworm (Diabrotica undecimpunctata howardi). Around 70% of protease activity could be arrested by the cysteine protease inhibitors E-64 and chicken egg-white cystatin, while the aspartic acid protease inhibitor pepstatin caused 30% inhibition. The cysteine protease activity was found to be highly sensitive to inhibition by both chicken egg-white cystatin and the rice cystatin, oryzacystatin I. Oryzacystatin I, expressed as a fully functional fusion protein in E. coli, was found to strongly inhibit larval gut protease activity. This recombinant oryzacystatin, incorporated into artificial diet at concentrations of 10 mM and above, caused significant decreases in larval survival and weight gain. E-64 was also shown to cause a significant antimetabolic in vivo effect. These results demonstrate the great potential for cysteine protease inhibitors, such as oryzacystatin, as tools for exploitation in the control of the Southern corn rootworm.     

Comparative susceptibility of larval instars and pupae of the western corn rootworm to infection by three entomopathogenic nematodes

As a first step towards the development of an ecologically rational control strategy against western corn rootworm (WCR; Diabrotica virgifera virgifera LeConte, Coleoptera: Chrysomelidae) in Europe, we compared the susceptibility of the soil living larvae and pupae of this maize pest to infection by three entomopathogenic nematode (EPN) species. In laboratory assays using sand-filled trays, Heterorhabditis bacteriophora Poinar and H. megidis Poinar, Jackson & Klein (both Rhabditida: Heterorhabditidae) caused comparable mortality among all three larval instars and pupae of D. v. virgifera. In soil-filled trays, H. bacteriophora was slightly more effective against third larval instars and pupae, and H. megidis against third larval instars, compared to other developmental stages. In both sand and soil, Steinernema feltiae (Filipjev) (Rh.: Steinernematidae) was least effective against second instars. In conclusion, all larval instars of D. v. virgifera show susceptibility to infection by all three nematodes tested. It is predicted that early application against young larval instars would be most effective at preventing root feeding damage by D. v. virgifera. Applications of nematodes just before or during the time period when third instars are predominant in the field are likely to increase control efficacy. According to our laboratory assays, H. bacteriophora and H. megidis appear to be the most promising candidates for testing in the field. I. Hiltpold similarly contributed to this paper as the first author.     

How to measure the food utilization of subterranean insects: a case study with the western corn rootworm (Diabrotica virgifera virgifera)

To date, nutritional studies on subterranean insects have focused on qualitative aspects due to experimental limitations. We have developed a method of studying insect–plant interactions quantitatively in subterranean environments. The initial and final weights of larvae of Diabrotica virgifera virgifera LeConte (Chrysomelidae, Galeruncinae) and those of maize roots, which served as food items were determined. The difference between initial and final weight of larvae and roots allowed for the calculation of the food conversion efficiency. This can be used to portray differences in food quality and its impact on larval performance and development.     

Parasitism of Western Corn Rootworm Larvae and Pupae by Steinernema carpocapsae

Virulence and development of the insect-parasitic nematode, Steinernema carpocapsae (Weiser) (Mexican strain), were evaluated for the immature stages of the western corn rootworm, Diabrotica virgifera virgifera LeConte. Third instar rootworm larvae were five times more susceptible to nematode infection than second instar larvae and 75 times more susceptible than first instar larvae and pupae, based on laboratory bioassays. Rootworm eggs were not susceptible. Nematode development was observed in all susceptible rootworm stages, but a complete life cycle was observed only in second and third instar larvae and pupae. Nematode size was affected by rootworm stage; the smallest infective-stage nematodes were recovered from second instar rootworm larvae. Results of this study suggest that S. carpocapsae should be applied when second and third instar rootworm larvae are predominant in the field.