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Keywords:

  • epidemiology;
  • Fusarium verticillioides;
  • insect vector;
  • mycotoxins;
  • Zea mays

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Field experiments were conducted in California and Hawaii in order to investigate the relationships between thrips feeding in maize ears and fusarium ear rot and silk-cut symptoms. Half the plots in each experiment were treated with insecticides following pollination. Thrips populations within ears were enumerated at six stages of ear development. Grain was examined microscopically and the percentages of kernels with silk-cut and ear rot symptoms were quantified by weight. Fumonisin B1 contamination in grain was measured by ELISA. Immature stages of thrips predominated, and maximum thrips populations occurred 21 days after pollination. Insecticides reduced thrips numbers, as well as silk-cut, ear rot symptoms and fumonisin B1 contamination. Immature thrips populations were more strongly correlated with silk-cut/ear rot symptoms (= 0·75) and fumonisin B1 accumulation (= 0·53), than were adult thrips (= 0·48 and 0·36, respectively). Silk-cut kernels all had ear rot symptoms and the percentage of kernels with symptoms was highly correlated with fumonisin B1 contamination (= 0·84). Results suggest that thrips are not occasional feeders, but can complete a substantial portion of their life cycle on maize ears. The results also indicate that thrips activity may be a cause of silk-cut symptoms, and this may be the mechanism that connects thrips activity with fusarium ear rot and fumonisin contamination of grain.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Fusarium ear rot, caused by Fusarium verticillioides and other species of Fusarium, is the most common and widespread mycotoxin-associated disease of maize (Logrieco et al., 2002; Munkvold, 2003b). Fumonisins are the most important mycotoxins associated with this disease. Fusarium verticillioides produces 18 or more fumonisin analogues (Rheeder et al., 2002); fumonisin B1 is the most prevalent and toxic, and thus the most thoroughly studied (Munkvold & Desjardins, 1997; Marasas et al., 2000). Fumonisin B1 production is promoted by environmental conditions that favour the growth of the pathogen (Miller, 2001), and the accumulation of fumonisins in maize kernels is highly correlated with fungal biomass in the kernels (Waalwijk et al., 2008).

Many insect species are associated with fusarium ear rot. Insects serve as vectors and create wounds that become infection sites for fungi that cause the disease (Smeltzer, 1959; Dowd, 1998; Payne, 1999; Sobek & Munkvold, 1999; Avantaggiato et al., 2002). Associated insects include European corn borer (Ostrinia nubilalis), corn earworm (Helicoverpa zea) (Munkvold et al., 1999; Dowd, 2000; Clements et al., 2003), the nitidulid beetle complex (Carpophilus spp.; Glischrochilus quadrisignatus) (Windels et al., 1976; Bartelt & Wicklow, 1999), and others (Dowd, 1998). In addition, Farrar & Davis (1991) determined that severity of fusarium ear rot in California was highly correlated with intra-ear incidence of western flower thrips (Frankliniella occidentalis).

Both the western flower thrips and the corn thrips (Frankliniella williamsi) have been reported on maize (Godfrey et al., 2006). Frankliniella occidentalis is polyphagous, with 244 host species from 62 different plant families, including tree and vine crops, field crops and ornamentals (EPPO, 1989). It is native to North America, and was detected internationally from 1980 (EPPO, 1989). It has since been reported globally, and is distributed throughout the USA, including Hawaii and Alaska. Frankliniella williamsi has been reported throughout most USA maize-producing regions and Hawaii. The two species are very similar in morphology (Reed et al., 2006).

Thrips feed by a ‘pierce and suck’ (Hunter & Ullman, 1992) or ‘punch and suck’ (Moritz, 1982; Heming, 1993) mechanism, typically damaging epidermal cells and consuming sap. Host plant tissues may also be damaged by the female’s saw-like ovipositor, as she deposits eggs into tender vegetative or floral tissues (Lublinkhof & Foster, 1977; Moritz, 1997). First instars emerge from eggs, and within hours moult to second instars, the primary immature feeding stage. Immature instars are flightless. Following the second instar are the quiescent, non-feeding propupal and pupal stages (Gaum et al., 1994), completed either within protective host tissues or soil. Adults can live from 30 to 60 days, depending on temperature and availability of host tissue. The life cycle for F. occidentalis, from egg to egg, ranges from 15 days at 30°C, to 40 days or more at 15°C (Lublinkhof & Foster, 1977).

For maize, the most widely reported thrips damage occurs at the early vegetative crop stage. Populations grow on early developing weed or crop hosts such as alfalfa in the spring, and then move to maize when these alternate hosts are cut or senesce (Hudson, 1999). Thrips feeding can stunt the development of young maize plants, and severe feeding damage is recognizable by browning and cupping of young leaves. Most seedlings outgrow this damage and develop normally (Godfrey et al., 2006). Yield impacts of damage at this stage are unknown, but generally presumed to be minimal in grain production fields (Hudson, 1999).

Thrips infestation of maize ears has been reported only in the central valley of California in the USA (Farrar & Davis, 1991); however, this report did not specify which thrips stages were infesting maize ears, or whether oviposition and subsequent development was occurring on the maize plants. It has been unclear whether adult thrips use maize ears solely as a food source, or also as a host on which to complete, or partially complete, their developmental cycle. Under the hot, dry conditions that persist in the long Californian growing season, irrigated cornfields may be an ideal refuge for thrips, as alternative weed and early season or unirrigated crop hosts senesce.

Thrips infest developing maize ears after pollination and cause wounds on immature kernels by feeding or oviposition (Farrar & Davis, 1991). These minor injuries to young kernels are not believed to directly impact yield or grain quality, but disruption of the pericarp may provide infection sites for fungal pathogens. Farrar & Davis (1991) reported a strong association between thrips populations and fusarium ear rot. Fumonisins are usually associated with fusarium ear rot, and the relationship between thrips and fumonisins was recently described (Parsons & Munkvold, 2010).

The silk-cut symptoms described by Odvody et al. (1997) are associated with fungal ear rots of maize, including fusarium ear rot. Silk-cut is characterized by microscopic or macroscopic lateral splits in the pericarp that expose the underlying immature endosperm to fungal colonization by airborne or vector-transported fungal propagules. Splits of the silk-cut type are, by definition, perpendicular to the embryo axis. The silk-cut phenotype has been reported in the literature only from southern Texas (Odvody et al., 1997), although it has been observed sporadically in grain from Hawaii, California and Georgia, and in other parts of the USA (unpublished data). Host genotypes with a predisposition for silk-cut symptoms are at greater risk of infection by F. verticillioides (Odvody et al., 1997). Silk-cut is most prevalent on maize hybrids with loose husks and open ear tips, a characteristic that also favours greater insect infestation (Farrar & Davis, 1991; Dowd, 1998). This suggests a relationship between insect vulnerability and silk-cut prevalence in maize, which has not been described previously.

The objectives of this research were: (i) to identify the developmental stage(s) of thrips associated with maize ear infestations and subsequent fusarium ear rot and fumonisin B1 contamination; and (ii) to determine the relationship, if any, between intra-ear thrips infestations of maize ears and silk-cut of maize kernels.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Experimental conditions

Field experiments were conducted during the 2002 and 2003 growing seasons at the Pioneer Hi-Bred research center at Woodland, Yolo County, California (CA), and the 2002/2003 winter season at the Pioneer Hi-Bred nursery and research seed facility at Waimea, Kauai County, Hawaii (HI). A Pioneer brand maize hybrid that was known to be susceptible to fusarium ear rot was sown for all plots in both locations. From previous studies, this hybrid was known to display silk-cut symptoms in some environments, including Woodland and Waimea. Planting at Woodland in 2002 and 2003 was on 25 May and 23 May, respectively. These planting dates were later than normal for the region, and May planting dates historically are associated with significant fusarium ear rot disease on susceptible hybrids. Plots in Waimea were planted on 2 December 2002. This is also considered a late planting date for winter nurseries on Kauai, historically associated with higher levels of ear rot, including fusarium, in seed production fields and nurseries on the island. Soil fertility, herbicide application and seedbed preparation followed standard maize production practices for each region. Plots at both locations were drip-irrigated, with irrigation applied to limit visible symptoms of moisture stress in the crop, such as afternoon leaf rolling and lower leaf firing.

The experiments were planted in a randomized complete block design, with four blocks in both locations, and each open-pollinated plot measured two rows (1·5 m) by 3·0 m. Planting density was 74 000 plants per hectare. Four rows (3·0 m) of the test hybrid were planted as buffer on the outside and between the treatments to minimize edge effects and interplot interference. Within each block (replication) were two insecticide treatments: treated and untreated. The first insecticide application was made when approximately 50% of plants had silks that extended approximately 2·5 cm beyond the end of the husk leaves. The second application was made 7 days after the first, and the third application 14 days after the first. The insecticide treatment was a mixture of a contact insecticide, lambda cyhalothrin (Warrior T®; Syngenta Crop Protection) and a systemic insecticide, dimethoate (Dimethoate 2·67 EC® Drexel Chemical), applied at 0·035 and 0·56 kg active ingredient ha−1, respectively, and sprayed in solution at a rate of 93·5 L ha−1 at Woodland, and to the point of spray runoff from maize ears in Waimea.

Insecticide applications in Waimea were made with a standard horticultural backpack hand-pump sprayer, with spray directed to the silks and husk leaves of the treated ears. All ears in prescribed plots were treated. At Woodland, insecticide was applied to all the plants in each plot by a high-clearance overhead sprayer (Hagie Manufacturing Company). The wheeled legs of the sprayer were extended an additional 0·60 m beyond the factory specification to allow sufficient clearance to make applications to full-height hybrid maize in California (>3·66 m) without damaging the crop canopy. Drop nozzle assemblies were fitted on the spray boom to direct the insecticide application on the foliage, stalk and ear tissue in each plot, covering the zone extending from approximately 0·60 m above to 0·60 m below the primary ear. The spray boom was manually controlled by the operator to maintain the spray focus on this zone of the canopy.

Thrips infestation and infection by F. verticillioides were the result of naturally occurring populations. Fusarium verticillioides is reported to be ubiquitous in Californian maize fields (Farrar & Davis, 1991). Air sampling performed in both locations has indicated that microconidia of F. verticillioides are a major component of the airborne microflora (unpublished data) and the fungus is known to be a predominant contaminant of maize residues in the soil (Leslie et al., 1990). Spores and other propagules are deposited on maize ears by rain or settling from the air, wind-blown soil particles (Ooka & Kommedahl, 1977; Munkvold, 2003a) or by insect vectors (Dowd, 1998). Inoculum was not controlled, but it was assumed that all plants in the study areas had an equal probability of exposure to F. verticillioides inoculum.

Evaluation of thrips populations

Ears were evaluated for thrips populations six times: at 50% silking (0 days after pollination; DAP) and 7, 14, 21, 28 and 35 DAP. At each sampling interval, two representative ears were manually removed from every plot, labelled, placed in sealed plastic bags and immediately chilled on ice. Upon completion of field sampling, ears were refrigerated overnight at 2°C. The following day, while still chilled, husk leaves and silks were carefully removed, and each ear was inspected under a × 15 dissection stereoscope. Thrips were counted and recorded for each ear. Representative specimens were identified to species (F. occidentalis or F. williamsi), but thrips species were not enumerated separately. Mature thrips were counted separately from immatures, although there was no attempt to differentiate among the larvae, propupae or pupae. Counts from ears within plots were averaged to provide an estimate of the number of insects per ear for each plot.

Evaluation of disease and fumonisin B1

At the typical harvest time (<20% grain moisture), five representative ears per plot were manually harvested and shelled with a single-ear mechanical research sheller (Agriculex Corporation), and a representative 454-g sample was retained. The sample was then dried below 15% (if necessary), packaged, labelled, and stored at 10°C and 50% humidity for subsequent kernel symptom assessments, mycotoxin analysis and fungal isolations.

Each kernel of a 30-g subsample from each 454-g plot grain sample was assessed in the laboratory for fusarium ear rot symptoms. Each kernel of the subsample was inspected at ×15 magnification to determine if it showed silk-cut symptoms. Virtually all kernels of this hybrid exhibiting silk-cut symptoms were visibly mouldy, with symptoms consistent with F. verticillioides or sometimes other fungi. All kernels with fusarium ear rot symptoms also had silk-cut symptoms. The silk-cut/ear rot fraction was then weighed and the percentage of the subsample (by weight) with symptoms was calculated as the incidence of silk-cut.

Representative kernels from plot grain samples were cultured to confirm association of visible ear rot symptoms with F. verticillioides infection. Kernels (10 per plot) were surface-sterilized for 2 min in a dilute bleach solution, dried, and cultured on Nash-Snyder semiselective medium (Nash & Snyder, 1962). After incubation for 5 days under ambient conditions in the laboratory, any growth was transferred aseptically by hyphal tip to carnation leaf agar and incubated until sporulation. Each culture was then observed under magnification for purity, growth habit, spores and morphological characteristics of conidiophores (Leslie & Summerell, 2006).

From each grain sample, approximately 400 g were analysed for fumonisin B1 by the Pioneer Hi-Bred Grain Analysis Laboratory (Pioneer Hi-Bred International). Samples were finely ground and a 3-g subsample was extracted for analysis by enzyme-linked immunosorbent assay (ELISA). The ELISA was a competition format constructed with proprietary antibodies to fumonisin B1. Pre-coated, stabilized plates were prepared by Beacon Analytical Systems, Inc. Maize extract samples and fumonisin B1 conjugated to horseradish peroxidase were co-incubated at 20–25°C for 60–62 min with shaking in the dark. Substrate was added following washing of the plates. The substrate reaction was allowed to proceed for 30–32 min at 20–25°C with shaking in the dark. The reaction was stopped and the resulting color intensity of the wells was read at 450 nm. The amount of fumonisin B1 present in a sample was inversely proportional to the colour intensity in the assay well. Detection limits of the fumonisin ELISA ranged from 0·8 to 2000 mg kg−1. This method has been validated in comparison to HPLC (Kulisek & Hazebroek, 2000), using AOAC-approved methods (Rice et al., 1995). Mean recovery of fumonisin B1 from spiked samples was 92·1% (Kulisek & Hazebroek, 2000).

Statistical analyses

Data were analysed using the mixed linear model function ‘fit model-standard least squares’ and ‘multivariate’ procedures in the jmp 7 software application (SAS Institute). Analysis of residuals indicated the need for data transformation for some variables. The ‘square root of the square root’ transformation gave the best improvement for incidence of silk-cut, fumonisin B1 (mg kg−1), intra-ear adult and immature thrips populations. For each combination of year (2002, 2003) and location (Woodland, Waimea) analysis of variance (anova) was completed for the transformed intra-ear adult and immature thrips populations. Model effects were insecticide treatment, sampling time, the interaction of insecticide and sampling time, and the random block effect (replication).

One-way anova was used to analyse silk-cut incidence and fumonisin B1. For each year (2002, 2003) and location (Woodland, Waimea), separate analyses were conducted to determine the effect of the insecticide treatment (applied, not applied) upon the response variables. Means comparisons were made using Student’s t-test ( 0·05), with transformed data. Untransformed mean and standard error values are reported in all tables.

The jmp 7 ‘multivariate’ correlation method was used to quantify the associations of intra-ear adult and immature thrips population with silk-cut incidence, and to quantify the association of ear rot severity with fumonisin B1. For all correlation analyses, data were transformed by the ‘square root of the square root’ transformation and were pooled across locations, years and insecticide treatments.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Insecticide treatment on thrips populations

Across years and locations, insecticide treatment had a significant effect on immature and adult intra-ear thrips populations, which fluctuated over sampling times (Table 1). Two-way interactions between insecticide treatment and sampling time (DAP) were also significant, except for adult intra-ear thrips populations in Waimea during 2002. The insecticide treatment was a strongly significant effect of percentage of silk-cut kernels and fumonisin B1 in all locations and years (Table 2). There was some injury to ears as a result of corn earworm feeding, but this was not associated with silk-cut symptoms.

Table 1.   Analysis of variance (anova) for 2002 and 2003 Waimea, HI and Woodland, CA, USA immature and adult intra-ear thrips (Frankliniella spp.) data from maize, grouped by year and location and transformed by the ‘square root of the square root’ method to meet the assumptions of the anova
YearLocationSourceImmature thrips (#)cAdult rhrips (#)d
d.f.F RatioProb > Fd.f.F RatioProb > F
  1. aPlots were either sprayed with insecticide three times (at pollination and 7 and 14 days after pollination), or were not sprayed.

  2. bTwo representative ears were harvested from each plot at 0, 7, 14, 21, 28 and 35 days after pollination; immature and adult intra-ear thrips were counted for each ear, and counts averaged to estimate of the number of immature and adult intra-ear thrips per plot.

  3. c‘Immature thrips’ included first and second instars, propupae and pupae.

  4. d‘Adult thrips’ included only winged, mature adult thrips.

2002WaimeaInsecticide treatmenta128·1<0·00115·50·024
Days after pollinationb530·2<0·001512·1<0·001
Insecticide treatment × Days after pollination53·50·01150·80·528
2002WoodlandInsecticide treatment131·6<0·00119·30·005
Days after pollination530·9<0·001512·3<0·001
Insecticide treatment × Days after pollination54·70·00253·60·011
2003WoodlandInsecticide treatment125·8<0·001114·90·001
Days after pollination521·2<0·00158·4<0·001
Insecticide treatment × Days after pollination56·3<0·00153·10·021
Table 2.   Analysis of variance (anova) for 2002 and 2003 Waimea, HI and Woodland, CA, USA silk-cut and fumonisin B1 data from maize, grouped by year and location. Percentages of silk-cut kernels and fumonisin B1 concentrations were transformed by the ‘square root of the square root’ method to meet the assumptions of the anova
YearLocationSourceSilk-cut kernels (%)bFumonisin B1 (mg kg−1)c
d.f.F RatioProb > Fd.f.F RatioProb > F
  1. aPlots were either sprayed with insecticide three times (at pollination and 7 and 14 days after pollination), or were not sprayed.

  2. bEach kernel of a representative 30-g subsample of grain from each plot was categorized as silk-cut or not silk-cut, and the weight of silk-cut kernels was expressed as a percentage of the total subsample weight for each plot.

  3. cA 400-g mature grain sample from each plot, was ground, and subjected to analysis by ELISA to quantify fumonisin B1 concentration.

2002WaimeaInsecticide treatmenta1153·4<0·001149·00·001
2002WoodlandInsecticide treatment136·30·00119·20·023
2003WoodlandInsecticide treatment136·3<0·001199·70·001

In 2002 at Waimea, the highest adult thrips populations occurred between 14 and 28 DAP (Fig. 1). Immature thrips populations were highest at 21 DAP (Fig. 2), and plots treated with insecticide had significantly fewer immature thrips than untreated plots (Table 1; Fig. 2). Immature thrips were generally much more numerous than adults (Figs 1 and 2).

image

Figure 1.  Number of adult intra-ear thrips (Frankliniella spp.) on maize by sampling time and insecticide treatment, from Woodland, CA (2002 and 2003) and Waimea, HI (2002). Insecticide treatment consisted of three weekly applications of lambda-cyhalothrin and dimethoate applied to ear tissue starting at 50% silk emergence. Two representative ears were harvested from each plot at 0, 7, 14, 21, 28 and 35 days after pollination; immature and adult intra-ear thrips were counted for each ear, and counts averaged to estimate of the number of immature and adult intra-ear thrips per plot. ‘Adult thrips’ included only winged, mature adult thrips. Bars represent standard error.

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image

Figure 2.  Number of immature intra-ear thrips (Frankliniella spp.) on maize by sampling time and insecticide treatment, from Woodland, CA (2002 and 2003) and Waimea, HI (2002). Insecticide treatment consisted of three weekly applications of lambda-cyhalothrin and dimethoate applied to ear tissue starting at 50% silk emergence. Two representative ears were harvested from each plot at 0, 7, 14, 21, 28 and 35 days after pollination; immature and adult intra-ear thrips were counted for each ear, and counts averaged to estimate of the number of immature and adult intra-ear thrips per plot. ‘Immature thrips’ included first and second instars, propupae and pupae. Bars represent standard error.

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In 2002 at Woodland, the highest populations of adult thrips occurred at 21 DAP, and insecticide-treated plots had significantly lower populations than untreated plots (Fig. 1). The same pattern was also true for immature thrips in 2002, where the highest numbers were seen at 21 DAP, and populations in untreated plots were higher than from treated plots (Fig. 2). In 2003, adult thrips first appeared at 21 DAP, although there was little difference among sampling points and between insecticide regimes (Fig. 1). Immature thrips in 2003 peaked at 21 DAP, and were significantly higher in untreated plots than in treated plots (Fig. 2). In 2002 and 2003, immature thrips were far more numerous than adults (Figs 1 and 2).

Insecticide treatment on disease parameters

Silk-cut/ear rot incidence was significantly higher in untreated plots than in insecticide-treated plots for each experiment (Table 3). Fumonisin B1 contamination was also significantly higher (approximately 10-fold) in untreated plots than in insecticide-treated plots for each experiment (Table 3). Fusarium ear rot symptoms co-occurred with silk-cut, whereas intact kernels did not have fusarium ear rot symptoms.

Table 3.   Incidence of maize kernels with silk-cut and fusarium ear rot (Fusarium verticillioides) symptoms (%) and concentration of fumonisin B1 (mg kg−1) in mature grain samples from field experiments in Woodland, CA and Waimea, HI, USA in 2002 and 2003
YearLocationInsecticide treatmentaSilk-cut/Ear rot (% by weight)bSEFumonisin B1 (mg kg−1)cSE
  1. Values are least square means (n = 4), followed by standard error estimates (SE); percentages of silk-cut kernels and fumonisin B1 concentrations were transformed by the ‘square root of the square root’ method to meet the assumptions of the anova. Means within columns and locations not followed by the same letter significantly differ (Tukey’s HSD,  0·05)

  2. aPlots were either sprayed with insecticide three times (at pollination and 7 and 14 days after pollination), or were not sprayed.

  3. bEach kernel of a representative 30-g subsample of grain from each plot was categorized as silk-cut or not silk-cut, and the weight of silk-cut kernels was expressed as a percentage of the total subsample weight for each plot.

  4. cA 400-g mature grain sample from each plot, was ground, and subjected to analysis by ELISA to quantify fumonisin B1 concentration.

2002WaimeaYes8·2A2·722·5A29·3
No75·0B220·3B
WoodlandYes10·2A5·014·8A32·8
No48·6B125·1B
2003WoodlandYes14·5A3·139·6A42·5
No75·7B495·2B

Thrips populations and fumonisin B1

Across locations and years, peak immature intra-ear thrips populations (21 DAP) were more strongly correlated with percentage of silk-cut kernels (= 0·75) and fumonisin B1 levels (= 0·53), than were peak adult intra-ear thrips populations (21 DAP) (= 0·48 and 0·36, respectively) (Table 4). The percentage of silk-cut kernels in a harvested grain sample was highly correlated with the concentration (mg kg−1) of fumonisin B1 in the sample (= 0·84).

Table 4.   Linear correlation coefficients (R) for immature intra-ear thrips (Frankliniella spp.) populations on maize at 21 days after pollination, adult intra-ear thrips populations at 21 days after pollination, percentage silk-cut kernels at harvest, and fumonisin B1 concentration at harvest
Variable 1Variable 2R
  1. Data were transformed by the ‘square root of the square root’ method and were pooled across years, locations and insecticide treatments (n = 24)

  2. aTwo representative ears were harvested from each plot at 21 days after pollination, immature intra-ear thrips (first and second instars, propupae and pupae) were counted for each ear, and counts averaged to estimate the number of immature thrips per plot.

  3. bTwo representative ears were harvested from each plot at 21 days after pollination, adult intra-ear thrips (only winged adults) were counted for each ear, and counts averaged to estimate the number of adult thrips per plot.

  4. cEach kernel of a representative 30-g subsample of grain from each plot was categorized as silk-cut or not silk-cut, and the weight of silk-cut kernels was expressed as a percentage of the total subsample weight for each plot.

  5. dA 400-g mature grain sample from each plot, was ground, and subjected to analysis by ELISA to quantify fumonisin B1 concentration.

Immature thrips (#)aSilk-cut kernels (%)0·75
Immature thrips (#)Fumonisin B1 (mg kg−1)d0·53
Adult thrips (#)bSilk-cut kernels (%)0·48
Adult thrips (#)Fumonisin B1 (mg kg−1)0·36
Silk-cut kernels (%)cFumonisin B1 (mg kg−1)0·84

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

These results confirm the important role of thrips in fusarium ear rot development in central California (Farrar & Davis, 1991; Warfield & Davis, 1996), suggest a mechanism for their involvement (by inducing silk-cut injury), and also provide new information about thrips life stages associated with maize ear rot. Control of thrips with insecticide dramatically reduced silk-cut incidence, which was closely associated with fusarium ear rot severity. Like silk-cut incidence, fumonisin B1 contamination was dramatically reduced (by ∼90%) from very high levels in untreated plots, by treatment with insecticide. The hybrid used in this study had short and loose husks, and exhibited high levels of silk-cut and fusarium ear rot severity, high intra-ear thrips populations, and high fumonisin B1 contamination in unsprayed plots at both locations, in both years. Susceptibility of a hybrid with short and loose husk morphology to fusarium kernel rot, intra-ear thrips infestation and silk-cut symptoms is consistent with past reports (Warfield & Davis, 1996; Odvody et al., 1997), although silk-cut has not been previously associated with intra-ear thrips populations. The present results indicate that thrips may be a causal factor in silk-cut symptoms, which provide an opportunity for infection by F. verticillioides, and subsequent fumonisin B1 contamination. In this study, nearly all kernels with silk-cut were visibly mouldy, and mouldy kernels nearly always had silk-cut symptoms. Conversely, kernels with intact pericarps very rarely displayed fusarium ear rot symptoms, including starburst. Ears that were not protected with insecticide exhibited silk-cut symptoms, whilst silk-cut and associated ear rot was dramatically reduced at both locations when ears were sprayed with insecticide to control thrips. This effect was evident in Woodland, CA and Waimea, HI, and warrants investigation to determine whether this insect also causes silk-cut symptoms in other corn-production regions, including Texas, where F. occidentalis is a known pest of cotton in the Corpus Christi area (Moore et al., 2003). Given the very high levels of fumonisin B1 associated with thrips-infested plots in this study, researchers and producers should evaluate risks and potential associations where similar abiotic (i.e. hot and dry conditions) and biotic (i.e. presence of F. occidentalis and/or F. williamsi) risk factors for fusarium ear rot and fumonisin contamination exist in other maize production regions of the world. Some of these regions include, but are not limited to Italy, Spain, South Africa and Australia (EPPO, 1989).

This is the first report of fumonisin contamination of hybrid maize in Hawaii. Maize grain production is essentially non-existent in the state, but the Hawaiian islands of Kauai, Oahu, Maui and Molokai are strategically important to seed and biotechnology companies, who utilize the year-round growing season to accelerate product research and development operations. The importance of Hawaii to the seed industry has grown exponentially with the development and commercialization of transgenic crops, primarily maize and soyabeans. The value of the industry on Hawaii has grown by 13 000% in the last 40 years, and was estimated in 2006 to generate $144 million annually for the state’s economy (Loudat & Kasturi, 2006). Transgenic and conventional maize production represent the majority of this investment, and loss of valuable seed to fusarium ear rot is a year-round concern for seed companies operating in Hawaii. The results of this study confirm that fusarium kernel rot is a significant disease of maize in Hawaii. Given the strong association of intra-ear thrips infestations with visible symptoms and fumonisin B1, effective scouting and control of intra-ear thrips should reduce the risk of losses of high-value research and commercial seed production in Hawaii.

This is the first reported evidence of thrips life cycle progression within developing maize ears. The results suggest that thrips utilize developing maize ears not only as a food source, but also as oviposition sites for eggs and development of immature thrips. The appearance of adult thrips in the ear tissues beginning 7–14 DAP, followed by increasing numbers of immature thrips at successive stages of ear development, suggest that maize ears may be attractive oviposition sites for female thrips under some conditions. It is unclear from this study whether females deposit eggs directly into developing kernels, on ear tissues adjacent to developing kernels, or on external leaf tissues from where immature thrips migrate into the developing ear via the silk channel. The absence of detectable adult intra-ear thrips earlier than 7–14 DAP, coupled with the appearance of immature thrips at 7–14 DAP, possibly suggests oviposition by adults outside developing maize ears, with subsequent migration of immature thrips into the developing ears. In both years and both locations, eggs were observed (but not quantified) within the external surfaces of the fleshy basal portions of husk leaves from maize ears sampled soon after pollination. Though not confirmed, these findings suggest that thrips hatch and develop on maize ears.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We are grateful to Pioneer Hi-Bred Int., Inc., for supporting this research with financial and other resources. Mr Mark Mancl and other Pioneer co-workers provided instrumental help and support with experiment design, data collection and analysis. Our thanks also go to Drs Alicia Carriquiry and Petruza Caragea of Iowa State University for their guidance on statistical procedures.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Avantaggiato G, Quaranta F, Desiderio E, Visconti A, 2002. Fumonisin contamination of maize hybrids visibly damaged by Sesamia. Journal of the Science of Food and Agriculture 83, 138.
  • Bartelt RJ, Wicklow DT, 1999. Volatiles from Fusarium verticillioides (Sacc.) Nirenb. and their attractiveness to nitidulid beetles. Journal of Agricultural Food Chemistry 47, 244754.
  • Clements MJ, Campbell KW, Maragos CM et al. , 2003. Influence of cry1ab protein and hybrid genotype on fumonisin contamination and fusarium ear rot of corn. Crop Science 43, 128393.
  • Dowd PF, 1998. Involvement of arthropods in the establishment of mycotoxigenic fungi under field conditions. In: SinhaKK, BhatnagarD, eds. Mycotoxins in Agriculture and Food Safety. New York, USA: Marcel Dekker, Inc, 30750.
  • Dowd PF, 2000. Indirect reduction of ear molds and associated mycotoxins in Bacillus thuringiensis corn under controlled and open field conditions: utility and limitations. Journal of Economic Entomology 93, 166979.
  • EPPO, 1989. Data sheets on quarantine organisms no. 177, Frankliniella occidentalis. EPPO Bulletin 19, 72531.
  • Farrar JJ, Davis RM, 1991. Relationships among ear morphology, western flower thrips, and Fusarium ear rot of corn. Phytopathology 81, 6616.
  • Gaum WG, Giliomee JH, Pringle KL, 1994. Life history and life tables of western flower thrips, Frankliniella occidentalis (Thysanoptera, Thripidae), on English cucumbers. Bulletin of Entomological Research 84, 21924.
  • Godfrey LD, Wright SD, Summers CG, Frate CA, 2006. University of California Pest Management Guidelines: Corn, Thrips. Richmond, CA, USA: University of California Agriculture and Natural Resources: UC ANR Publication 3443.
  • Heming BS, 1993. Structure, function, ontogeny and evolution of feeding in thrips (Thysanoptera). In: SchaeferCW, LeschenRAB, eds. Functional Morphology of Insect Feeding. Lanham, MD, USA: Entomological Society of America, 341.
  • Hudson R, 1999. Thrips. In: SteffeyKL, RiceME, AllJ, AndowDA, GrayME, Van DuynJW, eds. Handbook of Corn Insects. Lanham, MD, USA: Entomological Society of America, 111.
  • Hunter WB, Ullman DE, 1992. Anatomy and ultrastructure of the piercing-sucking mouthparts and paraglossal sensilla of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). International Journal of Insect Morphology and Embryology 21, 1735.
  • Kulisek ES, Hazebroek JP, 2000. Comparison of extraction buffers for the detection of Fumonisin B1 in corn by immunoassay and high-performance liquid chromatography. Journal of Agricultural and Food Chemistry 48, 659.
  • Leslie JF, Summerell BA, 2006. The Fusarium Laboratory Manual. Ames, IA, USA: Blackwell Publishing.
  • Leslie JF, Pearson CAS, Nelson PE, Toussoun TA, 1990. Fusarium spp. from corn, sorghum, and soybean fields in the central and eastern United States. Phytopathology 80, 34350.
  • Logrieco A, Mulè G, Moretti A, Bottalico A, 2002. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. European Journal of Plant Pathology 108, 597609.
  • Loudat T, Kasturi P, 2006. Hawaii’s Seed Crop Industry: Growth, Current and Potential Economic and Fiscal Contributions. Washington, DC, USA: United States Department of Agriculture, National Agricultural Statistics Service.
  • Lublinkhof J, Foster DE, 1977. Development and reproductive capacity of Frankliniella occidentalis (Thysanoptera: Thripidae) reared at three temperatures. Journal of the Kansas Entomological Society 50, 3136.
  • Marasas WFO, Miller JD, Visconti A, 2000. Fumonisin B1. Environmental Health Criteria 219, 1150.
  • Miller JD, 2001. Factors that affect the occurrence of fumonisin. Environmental Health Perspectives 109, 3214.
  • Moore GC, Parker RD, Fromme DD, Knutson AE, 2003. Managing Cotton Insects in the Southern, Eastern, and Blackland Areas of Texas. College Station, TX, USA: Texas Agricultural Extension Service: Bulletin E-5.
  • Moritz G, 1982. Zur Morphologie and Anatomie des Fransenfluglers Aelothrips intermedius Bagnal, 1934 (Aeolothripidae, Thysanoptera, Inesecta) 1. Mitteilung: Der Kopf. Zoologisches Jahrbuch der Anatomie 107, 557608.
  • Moritz G, 1997. Structure, growth and development. In: LewisT, ed. Thrips as Crop Pests. Wallingford, UK: CAB International, 323.
  • Munkvold GP, 2003a. Epidemiology of Fusarium diseases and their mycotoxins in maize ears. European Journal of Plant Pathology 109, 70513.
  • Munkvold GP, 2003b. Mycotoxins in corn: occurrence, impacts, and management. In: WhiteP, JohnsonL, eds. Corn Chemistry and Technology, 2nd edn. St Paul, MN, USA: American Association of Cereal Chemists, 81181.
  • Munkvold GP, Desjardins AE, 1997. Fumonisins in maize: can we reduce their occurrence? Plant Disease 81, 55665.
  • Munkvold GP, Hellmich RL, Rice LG, 1999. Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Disease 83, 1308.
  • Nash SM, Snyder WC, 1962. Quantitative estimations by plate counts of propagules of the bean root rot Fusarium in field soils. Phytopathology 52, 56772.
  • Odvody GN, Spencer N, Remmers J, 1997. A description of silk cut, a stress-related loss of kernel integrity in preharvest maize. Plant Disease 81, 43944.
  • Ooka JJ, Kommedahl T, 1977. Wind and rain dispersal of Fusarium moniliforme in corn fields. Phytopathology 67, 10236.
  • Parsons MW, Munkvold GP, 2010. Associations of planting date, drought stress, and insects with Fusarium ear rot and fumonisin B1 contamination in California maize. Food Additives and Contaminants 27, 591607.
  • Payne GA, 1999. Ear and kernel rots. In: WhiteDG, ed. Compendium of Corn Diseases, 3rd edn. St Paul, MN, USA: APS Press, 447.
  • Reed JT, Allen C, Bagwell R et al. , 2006. A Key to Thrips on Seedling Cotton in the Midsouthern United States. Starkville, MS, USA: Office of Agricultural Communications, Mississippi State University: Bulletin 1156.
  • Rheeder JP, Marasas WFO, Vismer HF, 2002. Production of fumonisin analogs by Fusarium species. Applied and Environmental Microbiology 68, 21015.
  • Rice LG, Ross PF, DeJong J, Plattner RD, Coats JR, 1995. Evaluation of a liquid chromatographic method for the determination of fumonisins in corn, poultry feed, and Fusarium culture material. Journal of AOAC International 78, 10029.
  • Smeltzer DG, 1959. Relationship between Fusarium ear rot and corn earworm infestation. Agronomy Journal 51, 534.
  • Sobek EA, Munkvold GP, 1999. European corn borer (Lepidoptera: Pyralidae) larvae as vectors of Fusarium moniliforme, causing kernel rot and symptomless infection of maize kernels. Journal of Economic Entomology 92, 5039.
  • Waalwijk C, Koch SH, Ncube E et al. , 2008. Quantitative detection of Fusarium spp. and its correlation with fumonisin content in maize from South African subsistence farmers. World Mycotoxin Journal 1, 3947.
  • Warfield CY, Davis RM, 1996. Importance of the husk covering on the susceptibility of corn hybrids to fusarium ear rot. Plant Disease 80, 20810.
  • Windels CE, Windels MB, Kommedahl T, 1976. Association of Fusarium species with picnic beetles on corn ears. Phytopathology 66, 32831.