Field evaluation of two microsporidian pathogens, an entomopathogenic nematode, and carbaryl for suppression of the Mormon cricket, Anabrus simplex Hald. (Orthoptera: Tettigoniidae)

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2, 59-65 (19%)

Field Evaluation of Two Microsporidian Pathogens, an Entomopathogenic Nematode, and Carbatyl for Suppression of the Mormon Cricket, Anabrus simplex Hald. (Orthoptera: Tettigoniidae) CHARLES M. MACVEAN*ANDJOHN L. CAPINERA~ *Institute of Research, Universidad de1 Valle de Guatemala, Aptdo. Postal 82, Guatemala, Guatemala; and fDepartment of Entomology and Nematology, 3103 McCarty Hall, University of Florida, Gainesville, Florida 32611 Received June 10, 1991; accepted February 26, 1992

biological agents for cricket control: two species of microsporidia, Nosema locustae Canning and an undescribed species of Vairimorpha, and the nematode Steinernema carpocapsae (Weiser). These agents were compared to a standard carbaryl treatment. Mormon crickets are remarkably free of insect parasites or predators amenable to testing (MacVean, 1987), but were reported to be a natural host to N. Zocustae (Henry and Oma, 1981). This microsporidium occurs commonly in many orthopterans (Henry, 1969; Henry and Oma, 1981; Henry and Onsager, 1982a) and is registered by the U.S. Environmental Protection Agency (EPA) for use against grasshoppers on rangeland. A large-scale field test by Henry and Onsager (198213) suggested that this pathogen might provide density reductions in Mormon cricket populations, although the lack of a controlled design precluded testing this hypothesis. We reevaluated N. locustae under controlled conditions, as well as a species of Vairimorpha, a microsporidium which we discovered in crickets near Dinosaur National Monument.’ The effects of these pathogens on survival and growth of Mormon crickets were obtained in laboratory and field evaluations; laboratory studies are presented in MacVean and Capinera (1991). The broad host range and high virulence of Steinernema carpocapsae (Laumond et al., 1979) make it an obvious candidate for evaluation. Since a primary route of infection for S. carpocapsae is by host ingestion, baits facilitate both infection and protection of the infective juvenile. Preliminary laboratory tests with individual sixth to seventh instar Mormon crickets showed that they were susceptible to the nematode. The fourth agent chosen for evaluation was a bait formulation of carbaryl on wheat bran. Insecticidal bait

In field enclosures, the microsporidium, Vairimorpha sp., produced significant reductions in survival (>60%) of Mormon crickets treated as first to third instars with bran bait ( 1012 spores/kg). This pathogen offers promise as a biological control agent for Mormon crickets. Reductions in survival attributable to Vairimorpha became statistically significant only after accounting for differential predation among treatment groups by the ant Formica criniventris Wheeler and Vesper sparrows. Nosema locustae Canning did not infect Mormon crickets or significantly reduce survival, despite high spore concentrations (101’ spores/kg) in the bran bait and cannot contribute to Mormon cricket management. The nematode Steinernema carpocapsae (Weiser) failed to infect or to reduce survival of Mormon crickets. Low palatability of nematode bait capsules contributed to the lack of pathogenic effects. Carbaryl bait, highly effective in reducing cricket density, can be applied at low rates of active ingredient per area for cricket suppression on rangeland or for immediate protection of crop fields. 0 1992 Academic Press, Inc. KEY WORDS: Insecta; Mormon cricket; Anabrus simplex; microsporidia; Nosema locustae; Vairimorpha sp.; nematode; Steinernema carpocapsae; biological control; carbaryl.

INTRODUCTION

During recent outbreaks of Mormon crickets in western Colorado and northeastern Utah, concern by ranchers and federal agencies for loss of rangeland forage has focused on devising management programs for crickets in their high-altitude (above 1800 m) permanent breeding grounds. These areas are primarily the sagebrush-dominated rangelands in and around Dinosaur National Monument. Given the U.S. National Park Service’s restrictions on chemical control measures within Dinosaur National Monument, we designed studies to evaluate the potential role of three

i Description of this species by Drs. John Henry and Douglas Street is in progress at the ARS Rangeland Insect Laboratory, Bozeman, Montana. It exhibits dimorphic development, with both binucleate and uninucleate spores present together in the same host; it will be placed in the genus Vairimorpha.

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1049-9644192 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.

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applications, heavily utilized during the 1920s to 1930s (Cowan, 1929; Wakeland, 1959), are now the subject of renewed interest due to lower impact on nontarget species than aerial sprays. Furthermore, comparison of biological agents with traditional chemical control measures can sometimes aid in estimating the acceptance of the biological agent by the user community. These four control agents were evaluated in bait formulations applied to field enclosures to determine their impact on Mormon cricket survival and the ability of the biological agents to infect this host.

METHODS AND MATERIALS

Sixteen 10 X 10-m pens were built in 1985 in a 4 X 4 array in Dinosaur National Monument (0.5 km west of the Echo Park Overlook, Moffat Co., CO) and were used for field experiments with all control agents from 1985 to 1987. In addition, 21 smaller circular pens, 2-m’ area, were constructed for additional tests with nematodes. Crickets were observed to engage in normal behaviors within the pens as in natural bands (e.g., feeding, molting, basking, mating). Pens were constructed of 36-cm high galvanized tin supported upright by steel fence posts. The upper edge of the tin barrier was folded inward at a 90” angle to prevent crickets from climbing out of the enclosure. To prevent invasion from the outside, tangletrap was applied to the sheet metal in a band around the entire pen. However, the 1987 study was cut short 27 days posttreatment by massive invasion of all pens by a band of crickets. The experimental site was located at 2300 m in grazed sagebrush (Artemisia trident&u Nutt.)-dominated grassland characterized by abundant arrowleaf balsamroot (Balsumorhiza sag&&a (Pursh) and grasses such as Sandberg bluegrass (Poe secunda Presl.), western wheatgrass (Agropyron smithii Rydb.), needle-andthread (Stipa comuta Trin. and Rupr.), and junegrass (Koeleriu cristutu (L.)) (see MacVean (1989) for biomass estimates of grasses vs. forbs). Evaluations were conducted over the course of three field seasons, 1985 to 1987, with different treatments in each. Progressively younger age groups of Mormon crickets were tested each year, e.g., sixth to seventh instars in 1985, fourth to fifth instars in 1986, and first to third instars in 1987. This sequence paralleled laboratory studies that were conducted concurrently (MacVean and Capinera, 1991). Details on handling and processing of spores, spraying bran with spores (or carbaryl), as well as comparative infectivity of spores from the Rangeland Insect Laboratory, Bozeman, Montana, andEvans BioControl, Broomfield, Colorado (no significant differences), were published in MacVean and Capinera (1991).

CAPINERA

Experimental design. A complete randomized block design with four blocks and four levels of the controlagent factor was used for all years. Blocks were established on the basis of the abundance of arrowleaf balsamroot within the pens. This species, a preferred food plant of the Mormon cricket (Swain, 1944), could affect acceptance of a bait. Also, the broad surface area covered by the leaves of this plant could conceal crickets and thereby affect cricket census data taken to evaluate the effects of the control agents on survival. A count of the number of arrowleaf balsamroot plants in all pens suggested four distinct categories which were maintained over the course of the studies (MacVean, 1989). All statistical analyses were conducted with SPSS/PC+ version 3.0 (SPSS, 1988). Insect collection. Crickets were collected from moving aggregations (bands) in the vicinity of Dinosaur National Monument by funneling the band into aluminum-screen cages (MacVean, 1989). Crickets were counted as they were released into each pen. In 1985, the starting population in each pen was 800 sixth to seventh instars. This number provided a density of 8/m’, the empirical economic threshold density used by the Animal and Plant Health Inspection Service (USDA, APHIS). However, because of rapid mortality due to ant (Formica criniventris Wheeler) and bird (primarily Vesper sparrows, Pooecetes grumineus) predation within the pens, this initial population was increased to 1600 in the 1986 and 1987 studies, with fourth to fifth and first to third instars, respectively. Starting density in the 2-m2 pens was 50 crickets. Measurement of survival. Cricket survival following bait application was estimated by taking a census of each pen periodically (periods of 4 days or less) up to 4-6 weeks post-treatment. A census was performed by recording each cricket seen in the outer 2-m perimeter of the pen, hereafter referred to as an “edge count.” Each pen contained a 1 X l-m grid of nylon string (100 squares). The outer 2-m area (64% of the total pen area) was chosen for two reasons: (a) crickets were observed to spend most of their active daily period (feeding, walking, mating, and molting between 0900 and 1800 h) in the outer 2-m area of the pens; and (b) preliminary census experiments revealed a near-perfect 1:l correlation between the census value for the edge count and a whole-pen count based on walking transects through the interior of the same pen (Fig. 1). Census values were used to describe survival curves for each replicate with no curve-fitting or smoothing procedures. The area under the survival curve was then calculated (Southwood, 1978; Redak, 1988) and treatment effects were examined through analysis of variance with cricket days as the dependent variable. Measurement of infection. Within 24 h post nematode treatment, determinations of infection were made

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800 rz0.99

E : 0 s e a,

CONTROL

P
600 l

400

0

0a.

l

0

a

0

200

ok, 0

200

400

600

Edge Count (outer 2 m)

600

, r

FIG. 1. Correlation between edge counts (outer 2-m perimeter or each pen) and whole-pen counts for determination of Mormon cricket populations in experimental enclosures.

by collecting 50 and 15 crickets from each large and each small pen, respectively. The crickets were held in laboratory cages until death, then placed individually on emergence traps (Dutky et al., 1964). Infection by N. locustae and Vairimorpha sp. was determined in 20-30 crickets collected from the pens 17 to 26 days post-treatment, transported to the laboratory, and frozen for later microscopic examination. In 1985 and 1986, crickets were held in cages for oviposition measurements until death, then frozen. Thus, most samples were frozen ~20 days and >26 days post-treatment. In 1987, crickets were collected and frozen 17 days posttreatment, shortly after which the invasion of foreign crickets occurred. All microsporidian infection determinations were based on spore morphology using phase-contrast examination of wet smears at 400 X (MacVean and Capinera, 1991). For N. locustae, midgut homogenates were examined, while Vairimorpha diagnosis was based on wholeinsect homogenates. Since Vairimorpha occurs naturally and could affect susceptibility to Nosema, levels of Vairimorpha were recorded from whole-insect homogenates for the Nosema treatments and controls, after midgut dissection. Infection levels were scored from 0 to 5 using the procedure of Henry (1971), then further grouped into broader frequency categories as described in MacVean and Capinera (1991). Where possible (i.e., when infection categories other than zero were obtained), this frequency tabulation was then analyzed with log-linear models for multiway contingency tables (Fienberg, 1980), with block and treatment as classification variables and infection considered a dependent variable (MacVean and Capinera, 1991). 1985 studies. Three control agents were tested against sixth to seventh instars in the large pens, with

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four replicates of each. Nematodes were formulated in a water-retaining calcium alginate capsule (Kaya and Nelsen, 1985) by Plant Genetics Inc. (Davis, CA) with 400 juveniles/capsule, or 7 juveniles/mg. Capsules contained 5% ground wheat bran incorporated into the calcium alginate. Frozen aqueous suspensions of N. locustae spores, obtained from the USDA/ARS Rangeland Insect Laboratory, were formulated on flaky wheat bran at a concentration of 2.5 X lO’O/kg. Carbaryl bait was prepared by spraying undiluted Sevin-4-Oil onto wheat bran using the same procedures as for N. locustue spores. Foster et al. (1979) found that mortality in cage studies with Mormon crickets using a 2% active ingredient (AI) carbaryl bran bait was not significantly lower than with the usual 5% AI commercial bait formulations; therefore, we utilized a 2% concentration (by weight) in our tests. Control bran was sprayed with distilled water. Large-pen populations received baits applied by hand using a 500-ml cup with a perforated lid during the crickets’ peak feeding period at mid-morning (see MacVean (1987) on June 15, at a rate of 15 kg/ha. This rate was calculated to provide bait ad lib for 2 days after application, and was based on consumption rates given by Cowan and Shipman (1947) and an expected 2-day longevity for the capsules. Despite the apparently high application rate of 15 kg/ha, the resulting distribution of capsules was sparse compared with the distribution of bran particles, due to the high mass of the nematode capsules. Since our principal interest was to determine whether nematode infection could occur under favorable conditions (not necessarily economical ones), a second evaluation of the nematode was conducted on August 3, using the 2-m’ pens with seven replicates. Capsules were applied at the rate of 765 kg/ha in two partial applications, one in the evening (1930 h), coinciding with the second feeding period (MacVean, 1987), and one the following morning (0700 h) preceding high temperatures. In addition to the nematode treatment, 2% AI carbaryl was retested in the small pens at the reduced rate of 5 kg/ha. Control pens received untreated bran at the same rate. Concurrent with this second field test, we conducted a laboratory infection test in which five replicates of 10 crickets each were held in 29 X 29 X 29-cm cages and fed nematode capsules ad lib for 48 h. Controls were fed untreated wheat bran. After this inoculation period, crickets were maintained on a diet of rye sprouts, dry bran, water, and clippings of native food plants (see MacVean, 1987). As crickets died, they were placed on traps for nematode emergence. Lastly, we compared palatability of wheat bran vs. calcium alginate capsules in simultaneous choice tests in the laboratory with individual, field-collected, unstarved adult crickets held in 15 X 15 X 15-cm aluminum screen cages (n = 21). We measured feeding activ-

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ity by recording the amount of time each insect spent L controls 250 feeding on bran vs. capsules. This was determined by * Nosema direct observation over a l-h period. Total times for each type of food were then compared with a paired t .-F 200 4 nematodes test. .; +~ carbatyl 3 150 1986 studies. N. locustae spores from Evans BioControl Inc. were tested against fourth to fifth instars at I two concentrations, 10” spores/kg bran, hereafter 3: 100 called low, and 1012 spores/kg, hereafter called high, > 5 with four replicates of each. In addition to the standard = 50 controls, a set of controls for bird predation was included in which pens (four replicates) were covered with 0 0 5 10 15 20 25 30 35 4 I orchard bird netting (2.5cm-square openings) and received untreated wheat bran. Many species of birds are Days Post Treatment known to feed on Mormon crickets (Knowlton, 1948; FIG. 2. Mean survival of Mormon crickets treated as sixth to Wakeland, 1959) and we commonly saw Vesper seventh instars (1985) with wheat-bran baits: untreated bran (consparrows taking crickets from the pens. The bird-net- trols); N. locustae at 2.5 x 10”’ spores/kg; Steinernema carpocapsae at ting treatment was included to determine to what ex- 9.3 X lo6 juveniles/kg; carbaryl 2% AI; all baits applied at 15 kg/ha. tent the rapid declines in cricket populations seen in 1985 were attributable to bird predation and could precricket days. Cricket-days data were log,, transformed clude detecting slow declines due to pathogens. All baits were applied by hand on May 24 at the recommended to stabilize variances. A significant treatment effect was rate of 2 kg/ha by Henry et al. (1973) and Henry and obtained (controls vs. treatments, F = 23.12, P = O.OOl), Onsager (1982a). This rate provided the maximum due almost entirely to the carbaryl treatment. Carbaryl bait produced rapid and significant mortality, and difamount that could be consumed by fourth to fifth infered significantly from the biologicals (F = 178.13, P < stars in a 24-hr period. This time period was chosen because the 1985 study suggested that bran particles O.OOl), which did not differ among themselves (F = 0.3, were available to crickets for no more than about 24 h. P = 0.596) nor from the controls (F < 0.005, P > 0.99, The bait was depleted via consumption by target and nonorthogonal contrasts) (Fig. 2). The effectiveness of carbaryl was not surprising and nontarget organisms, blown away by wind, or pummeled corroborates the potential of this bait treatment for by rain. 1987 studies. A final test with N. locustae and a first rapid population suppression. Wheat bran was readily field test with the recently discovered Vairimorpha sp. consumed despite an abundance of preferred food were conducted with first to third instars during the plants. The small-pen trial produced 90% mortality spring of 1987. Baits were applied May 13 at 2 kg/ha, after 48 h, after adjusting for control mortality (Henwith the same concentrations for N. locustae (10” and derson and Tilton, 1955). Thus, effective control of adult Mormon crickets at a density of 20/m” is feasible 10” spores/kg), but only at 1Ol2 spores/kg for Vairimorpha. Controls received untreated bran. Based on the with an application rate as low as 5 kg/ha. Our results agree well with the findings of Foster et al. (1979). How1986 study, all pens were covered with bird netting. Ant predation by Formica criniventris on crickets was ever, mortality in a confined population is not entirely observed in all 3 years of study. The initial introduction indicative of the control one would obtain with the typiof hundreds of crickets into each pen triggered high cal application of bait in the path of a moving band of crickets. Bait is rapidly depleted by the leading segment rates of attack by workers, but within 12-24 h ant predation subsided to an apparently much lower rate of the band, precluding any exposure to the control throughout the rest of the experiment. To account for agent by the remainder of the insect aggregation. Either this effect, we utilized the initial cricket population total coverage of the area occupied by the band of crick(census taken l-2 days after introducing crickets into ets or repeated applications in its path would be rethe pens and just prior to application of baits) as a co- quired to obtain uniformly high mortality rates. S. carpocapsae appears to hold little promise for Morvariate in analysis of variance (MacVean, 1989; Snedemon cricket control, despite the use of a protective forcar and Cochran, 1967; Steel and Torrie, 1980). mulation. Contrary to the preliminary data from an earlier laboratory inoculation, no infection by nematodes was obtained from either the large-pen test (n = 195) or RESULTS AND DISCUSSION the laboratory trial (n = 50), and only 4% infection was 1985 studies. Differences among treatments were obtained in the small-pen trial (n = 138). High soil surtested through contrasts in the analysis of variance on face temperatures (40-50”(Z) and cricket hemocoel tem-

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peratures (34-37°C) at the time of application are undoubtedly involved in the failure of the nematodes to infect Mormon crickets (MacVean, 1989). Infection by nematodes might be more likely in early spring soon after cricket hatch (MacVean, 1987), when snowmelt would ensure lower ground and air temperatures, and probably lower hemocoel temperatures. Spring conditions might also provide the moisture needed to facilitate infection by encapsulated nematodes, as suggested by Kaya and Nelsen (1985). They showed that nematodes in capsules were only able to infect lepidopteran insects feeding in a moist environment. The study suggested that nematodes must first be released from the capsules into a moist environment before they can successfully attack the host insect. However, Capinera and Hibbard (1987) obtained significant reductions in densities of grasshoppers treated with nematode capsules in a dry environment. Palatability of the protective calcium alginate capsules was low, presenting a major obstacle to infection. Little feeding on the capsules was observed in the pens, whereas wheat bran was rapidly consumed. These observations were supported by the laboratory preference test, in which the mean time spent feeding on bran exceeded the time spent feeding on capsules by a mean of 18 min (t = 3.33, df = 20, P = 0.003). The addition of feeding stimulants could improve ingestion, although the wheat bran incorporated into the capsule did not elicit the strong feeding response typical of wheat bran alone. No infection by N. locwstae was found in crickets collected from the pens, either in those treated with Nosema (n = 67) or controls (n = 70). These results, as well as the lack of effects on survival, are in agreement with the results of laboratory experiments with the same pathogen treatments in this age group (MacVean and Capinera, 1991). 1986 studies. No significant treatment effects were obtained in the unadjusted analysis of variance (F = 1.3, P = 0.33), but a difference between bird exclosures and the standard controls was apparent (F = 13.5, P = 0.006) when differences in pretreatment population levels were accounted for by analysis of covariance. Nosema applications produced no significant reductions in cricket days relative to controls (F = 0.32, P = 0.586) nor did the low and high rates differ from each other (F = 0.17, P = 0.691) (Fig. 3). The bird-netting effect indicates significant bird predation which, like ant predation, could confound the evaluation of biological control agents in the field if not accounted for in the analysis. No infection by N. locustae was found (n = 81,84, and 85 for controls, Nosema low, and Nosema high, respectively). As with the 1985 data, these results match those obtained in corresponding laboratory tests (MacVean and Capinera, 1991).

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0 0

1 10

,

/ 20

30

40

Days Post Treatment F I G . 3 . Mean survival of Mormon crickets treated as fourth to fifth instars (1986) with wheat-bran baits: untreated bran (controls and bird exclosures): N. locustae at 10” and 10” spores/kg; all baits applied at 2 kg/ha.

1987 studies. After adjusting for the effects of ant predation, we observed the same dramatic reduction in survival of first to third instars due to Vairimorpha treatment seen in the laboratory (MacVean and Capinera, 1991). N. locustae failed to infect or to reduce the survival of even this youngest age group, which also corresponds to our laboratory findings. Survival curves following Nosema and Vairimorpha treatment are shown in Fig. 4. On one sampling date (Day 4), sampling error resulted in census values higher than the known initial population. This effect was presumed to be common to all pens and data were not modified in calculating curve areas. The curves alone did not suggest any significant treatment effects, and in fact provided no overall statistical significance in ANOVA on cricket days (F = 0.77, P = 0.538). However, initial population values in each treatment group differed widely (Fig. 4A), despite uniform introductions of crickets into each pen and were probably the result of variable ant predation (l-33 ant nests per pen). In the analysis of cricket days, initial population values were a significant covariate (F = 19.05, P = 0.002) and covariance analysis revealed highly significant treatment effects (F = 5.24, P = 0.027). For separation of pathogen effects, a set of nonorthogonal contrasts comparing each treatment to the controls was chosen since these corresponded to the questions of interest better than did orthogonal contrasts (MacVean, 1989). Nosema did not produce significant reductions in survival (controls vs. Nosema low: F = 0.57, P = 0.472; controls vs. Nosema high: F = 0.21, P = 0.662). As in previous years, no infection by Nosema was found in midguts or whole-insect homogenates (n = 240). Possible reasons for this total lack of infection are discussed in MacVean and Capinera (1991).

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In comparison, Vairimorpha produced a rapid and significant reduction (>60%) in survival relative to controls (F = 7.62, P = 0.025). These results match closely the results of laboratory tests (MacVean and Capinera, 1991), in which 90% mortality was observed 6 days post.inoculation. Infection rates of Vuirimorpha 17 days postinoculation are shown in Table 1. Since most of the mortality in the Vairimorpha treatments occurred by Day 7 postinoculation (Fig. 4B), data shown in Table 1 reflect infection in those insects surviving the high dose of Vairimorpha. In the laboratory, most of the insects inoculated at a sublethal dose of Vairimorpha became infected. Thus, the fact that few survivors in the field were infected suggests that most insects consuming the bait succumbed to it, whereas the majority of the survivors failed to ingest the bait. It appears, then, as predicted from laboratory data, that application of Vairimorpha at a high concentration in bran to early instars can provide short-term reductions in host density, but will not greatly increase prevalence or infection levels within the treated population. Lower concentrations of Vairimorpha applied in the field may increase infection levels and produce the sublethal effects (e.g., reduction in nymphal development) shown in laboratory tests. The Mormon cricket appears to be an unsuitable host for N. locustae, at least for the acridid-reared strain of

700 -,-”‘, w

8

‘,

-controls + Noeema 10 ‘O/kg +Norama lO%g -eVairlmorphs

CAPINERA

TABLE 1 Vuirimorpha Infection 17 Days Postinoculation of First to Third Instar Mormon Crickets with N. locustae (10” and 10” Spores/kg Bran) or Vairimorpha (10” Spores/kg Bran), Field Study, 1987 Percent in each category Treatment

Uninfected

Light”

Heavy”

N

Controls Nosema low Nosema high Vairimorpha

97 96 99 73

3 4 1 26

0 0 0 1

120 121 119 114

a Light infection: levels l-2 of Henry (1971), i.e., ~5 spores/field at 400 X; heavy infection: levels 3-5, i.e., >5 spores/field.

this pathogen (MacVean and Capinera, 1991). Henry and Onsager (1982b) did report spores from Mormon crickets treated with acridid-produced N. locustae, but only trace levels were found in midgut tissue (J. E. Henry, personal communication). In contrast, Henry and Oma (1981) found natural infection in Mormon crickets from Montana, with high levels of spores in the fat body. Taken together, these studies and our current findings strongly suggest strain differences. Before N. locustae can be included in cricket management plans, an appropriate strain must be selected and reared for testing. Unfortunately, to date no significant infection (e.g., in fat body) has been found in Mormon crickets since the initial field isolation in Montana, and no material from this isolation is currently available. Efforts should be made to reisolate a naturally occurring population of N. locustae on which selection experiments could be performed. Vairimorpha sp. offers greater possibilities for integration into Mormon cricket management schemes, or for improvement through genetic selection or engineering, but suffers from lack of EPA registration. Unless Mormon crickets reach the outbreak proportions and pest status achieved during the 1920s and 1930s (MacVean, 1987), it is doubtful that the limited geographic areas currently sustaining high cricket populations would ever justify the costs of commercial registration. Moreover, damage to range plants in these areas is often low (MacVean, 1989). However, perhaps special-use permits for agencies such as the National Park Service or Bureau of Land Management, allowing application of Vairimorpha to protected areas, can become an option.

Days Post Treatment

FIG. 4. Mean survival of Mormon crickets treated as first to third instars (1987) with wheat-bran baits: untreated bran (controls); N. locustae at 10” and 10” spores/kg; Vuirimorpha sp. at 10” spores/ kg; all baits applied at 2 kg/ha. (A) Actual numbers of individuals surviving. (B) Percentage of the initial population surviving. Values greater than 100% reflect sampling error.

ACKNOWLEDGMENTS This research was supported by a grant from the National Park Service. We thank Steve Petersburg and the Resource Management group of Dinosaur National Monument for their support; Stuart Shippey, William Barnes, David Hopcia, Tom Weissling, David Hor-

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ton, Richard Redak, Boris Kondratieff, and Phillip Chapman for their invaluable assistance and many contributions to this study; BIOSYS, Catharine Mannion, and Plant Genetics, Inc. for supplying and formulating nematode bait capsules; and the Universidad de1 Valle de Guatemala for supporting publication costs.

REFERENCES

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Henry, J. E., Tiahrt, K., and Oma, E. A. 1973. Importance of timing, spore concentration, and levels of spore carrier in applications of Nosemu locustue (Microsporida: Nosematidae) for control of grasshoppers. J. Invertebr. Puthol. 21, 263-272. Kaya, H. K., and Nelsen, C. E. 1985. Encapsulation of steinernematid and heterorhabditid nematodes with calcium alginate: A new approach for insect control and other applications. Enuiron. Entomol.

14,572-574. Capinera, J. L., and Hibbard, B. E. 1987. Bait formulations of chemical and microbial insecticides for suppression of crop-feeding grasshoppers. J. Agric. Entomol. 4, 337-344. Cowan, F. T. 1929. Life history, habits, and control of the Mormon cricket. USDA Tech. Bull. 161.

Knowlton, G. F. 1948. Vertebrate animals feeding on the Mormon cricket. Am. Midl. Nat. 39, 137-138.

Cowan, F. T., and Shipman, H. J. 1947. Quantity of food consumed by Mormon crickets. J. Econ. Entomol. 40, 825-828. Dutky, S. R., Thompson, J. V., and Cantwell, G. E. 1964. A technique for the mass propagation of the DD-136 nematode. J. Insect Pathol. 6,417-422. Fienberg, S. E. 1980. “The Analysis of Cross-classified Categorical Data.” 2nd ed. MIT Press. Foster, R. N., Billingsley, C. H., Staten, R. T., and Hamilton, D. J. 1979. Field cage tests for concentrations of carbaryl in a bait and its application rates for control of Mormon cricket. J. Econ. Entomol.

MacVean, C. M. 1987. Ecology and management of Mormon cricket, Anabrus simplex Haldeman. In “Integrated Pest Management on Rangeland: A Shortgrass Prairie Perspective” (J. L. Capinera, Ed.), pp. 116-136. Westview Press, Boulder, CO.

72, 295-297. Henderson, C. F., and Tilton, E. W. 1955. Tests with acaricides against the brown wheat mite. J. Econ. Entomol. 48, 157-161. Henry, J. E. 1969. Extension of the host range of Nosema locustae in Orthoptera. Ann. Entomol. Sot. Am. 62, 452-453. Henry, J. E. 1971. Experimental application of Nosema locustae for control of grasshoppers. J. Znuertebr. Puthol. l&389-394. Henry, J. E., and Oma, E. A. 1981. Pest control by Nosema locustue, a pathogen of grasshoppers and crickets. In “Microbial Control of Pests and Plant Diseases 1970-1980” (H. D. Burges, Ed.), pp. 573586. Academic Press, New York. Henry, J. E., and Onsager, J. A. 1982a. Large-scale test of control of grasshoppers on rangeland with Nosemu locustae. J. Econ. Entomol.

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