Influence of weed communities in corn plantings on parasitism of Ostrinia nubilalis (Lepidoptera: Pyralidae) by Eriborus terebrans (Hymenoptera: Ichneumonidae)

BIOLOGICAL

CONTROL

2,312-316

(1992)

Influence of Weed Communities Ostrinia nubilalis (Lepidoptera: (Hymenoptera: DANIEL

of Entomology,

Department

Ohio

Agricultural

in Corn Plantings on Parasitism of Pyralidae) by Eriborus terebrans Ichneumonidae)

M. PAVUK’ AND BENJAMIN R. STINNER Research

and Development

Center,

Received July 20, 1992; accepted November

Parasitism of second generation European corn borer, Ostrinia nubilalis (Hubner), larvae by parasitoids was examined in corn (Zea mays) plantings having different weed communities. Treatments were corn without weeds, corn principally with broadleaf weeds, corn principally with grassy weeds, and corn with a mixture of broadleaves and grasses. 0. nubilalis larvae were collected and maintained on artificial diet under constant environmental conditions in the laboratory to determine levels of parasitization. The ichneumonid, Eriborus terebrans (Gravenhorst), was the only parasitoid species reared, with the exception of a single tachinid, tentatively identified as Lydella thompsoni. Neither broadleaf nor grassy weeds had significant influences on parasitization of larvae during the study. Parasitism was positively correlated with host density (number of larvae per plant) in the corn-broadleaf weed community in 1988. Parasitism was greater in all treatments in 1989 than in 1988, ranging from 2.1 to 5.6% in 1988 and from 20.0 to 29.1% in 1989. The results were inconclusive as to whether weeds within corn plantings augment parasitism of 0. nubilalis larvae by E. terebrans or by other parasitoids. c 1992 Academic

Press,

Inc.

KEY WORDS: Insecta; Ostrinia ebrans; parasitoids; vegetational weed communities.

nubilalis; Eriborus terdiversity; Zea mays;

The European corn borer, Ostrinia nubilalis (Hubner) (Lepidoptera: Pyralidae), is a widespread and significant pest of both field and sweet corn in the United States (Showers et al., 1989). Because this insect is not native to North America, it received attention as a likely candidate for a classical biological control program. Between 1920 and 1938, 23 parasitoid species were intro-

’ Present address: Department Granville, OH 43023.

of Biology,

1049.9644/92 $5.00 Copyright 0 1992 by Academic Press, Inc. All rights

of reproduction

in any

form

reserved.

Denison

University,

312

The

Ohio

State

University,

Wooster,

Ohio

44691

23, 1992

duced into the United States from Europe and the Orient (Baker et al., 1949). In the North Central region, the introduced parasitoids which were most commonly recovered in European corn borer surveys were Lydella thompsoni Herting (Diptera: Tachinidae), Macrocentrus grandii Goidanich (Hymenoptera: Braconidae), and Eriborus terebrans (Gravenhorst) (Hymenoptera: Ichneumonidae). In addition, a number of native parasitoids have been identified as using 0. nubilalis as a host, including Trichogramma spp. and species of Tachinidae, Braconidae, and Ichneumonidae; however, parasitization by these native parasitoids is usually low (Baker et al., 1949). The presence of various weedy species in and around crop fields has been shown to have positive effects on parasitoids and predators in many situations (e.g., Leuis, 1967; Smith, 1969; Root, 1973; Speight and Lawton, 1976; Altieri and Whitcomb, 1980; Horn, 1981). Such vegetation provides additional pollen and nectar sources, more abundant prey and alternate hosts for predators and parasitoids (van Emden, 1963,1965), and ameliorated microhabitats (Root, 1973). Increasing the vegetational diversity of corn fields may have numerous benefits for the parasitoids of the European corn borer. However, presence of weeds in cornfields is a factor that increases attractiveness of those fields to the second flight of 0. nubilalis (Showers et al., 1976,198O). Caffrey and Worthley (1927) noted that adult 0. nubilalis aggregate in grassy habitats along edges of cornfields. Showers et al. (1976) demonstrated that areas of dense, grassy vegetation around cornfields are preferred mating habitats for 0. nubilalis, because free water that collects in the grass from rain and dew is used as a source of drinking water by the moths (DeRozari et al., 1977). Thus, presence of weeds, particularly grasses, in and peripheral to cornfields can result in more egg masses being deposited on corn in those situations (Derrick and Showers, 1990). We investigated the influences of manipulated weed communities within Zea mays plantings on parasitiza-

INFLUENCE

OF

WEEDS

ON

PARASITISM

tion of 0. nubilalis larvae. We anticipated that at least the generalist parasitoids would be influenced positively by the increased vegetational diversity because of the presence of possible alternate hosts. In addition, both generalist and specialist species would be expected to benefit from additional nectar sources as well as improved microhabitats. MATERIALS

AND

METHODS

Research was conducted during 1988 and 1989 at The Ohio Agricultural Research and Development Center, Ohio State University, Wooster, Ohio. The four treatments were: (1) corn without weeds, (2) corn principally with broadleaf weeds, (3) corn principally with grassy weeds, (4) corn with a mixture of broadleaf and grassy weeds. The experiment was a 2 x 2 factorial (two factors, broadleaf weeds and grassy weeds, and two levels, present or absent); treatments were replicated four times and arranged in a randomized complete block design. The same plots were used in both years. Each plot measured 18.3 m by 18.3 m. A 3.1-m border around each plot contained naturally occurring vegetation that was mowed periodically. Surrounding areas were planted in conservation and conventional tillage corn fields. No insecticides were used, but herbicides were applied at the following rates to manipulate naturally occurring weed populations: corn without weeds-cyanazine (E.I. DuPont de Nemours, Wilmington, DE), 3.36 kg(AI)/ha; alachlor (Monsanto, St. Louis, MO), 3.36 kg(AI)/ha; and paraquat (ICI Americas, Inc., Wilmington, DE), 0.56 kg(AI)/ha; corn principally with broadleaf weedsalachlor, 2.24 kg(AI)/ha; corn principally with grassy weeds-cyanazine, 2.80 kg(AI)/ha and2,4-D amine (Riverside-Terra Corp. Sioux City, IA), 0.56 kg(AI)/ha; corn with both broadleaf and grassy weeds-cyanazine, 1.68 kg(AI)/ha; alachlor, 2.24 kg(AI)/ha; and paraquat, 0.28 kg(AI)/ha. Herbicides were applied at low rates to the mixed weeds treatment to prevent rapid establishment of early season weeds and to provide corn with a competitive advantage over the weeds. The herbicides did not seem to affect the development of the mid- to late summer weed community, which was of primary interest in this study. All plots were minimally tilled (disked once before planting) and corn was planted with a no-till planter. In 1988, “Pioneer 3780” was planted 12 May. Due to discontinuation of “Pioneer 3780” after 1988, “Pioneer 3352” was planted 19 May 1989. We assumed this change would have no significant effect on infestation of corn plants by European corn borer larvae, because neither cultivar shows resistance to first generation larvae. Plots were hoed during the season to maintain the intended treatment floristic combinations. Beginning in late May, monthly surveys were conducted to determine the principal plant species in each plot containing weeds.

OF

0.

nubilalis

BY

E.

terebrans

313

From 3 August to 18 September 1988, and from 1 August to 12 September 1989, corn plants were selected from four random locations in each plot on each sampling date (two plants from each location for a total of eight plants per plot). Sampling started in early August and continued into mid-September in order to assess how second generation larval densities changed over time in the plots, and also to determine if any parasitoid species were emerging from third and fourth instar larvae. Plants were removed at 2- to 14-day intervals in 1988, at approximately 7-day intervals in 1989, and were not taken from the edges of plots to avoid edge effects. A total of 64 and 40 plants per plot were sampled during 1988 and 1989, respectively. Extended plant height was measured, and plants were dissected in the laboratory to determine if larvae were present. The number of 0. nubilalis tunnels per plant was also recorded at the time of dissection. Larvae were held under constant conditions (16:8 L:D, 25”C, 70-80% RH) in the laboratory on a pinto bean-wheat germ diet until they pupated or parasitoids emerged. Infestation data were transformed by log(y + l), and percentage parasitization data were transformed by arcsine (square root of y), to stabilize the variances. Parasitization data were pooled, because on some sampling dates, no larvae were collected in some of the plots, and therefore no data were obtained from those dates in terms of parasitism. The data were subjected to a two-way analysis of variance. Orthogonal contrasts were used to compare treatments with and without broadleaf weeds, and treatments with and without grassy weeds. Spearman’s rank correlation coefficient was used to determine if a significant relationship existed between percentage parasitism and larval density in each treatment. A significance level of (Y = 0.05 was used for all statistical tests. RESULTS

The weed community of the broadleaf treatment was dominated during August and September by lambsquarter, Chenopodium album L., and pigweed, Amaranthus retroflexus L. The grassy weed treatment was mainly populated by giant foxtail, Setaria faberii Hermann; fall panicum, Panicum dichotomiflorum Michaux; barnyardgrass, Echinochloa crus-galli (L.) Beavois; and large crabgrass, Digitaria sanguinalis (L.) Scopoli. Combinations of these broadleaf and grass species were found in the mixed-weeds treatment. Weed densities were not determined in the plots, but grassy weeds, particularly giant foxtail, 5’. faberii, were abundant in the treatment containing grasses. Presence of S. faberii may have favored larger populations of adult moths in those plots; in fact, moths were frequently flushed from these grassy areas during the study (D. M. Pavuk, personal observation). Table 1 lists the principal weed spe-

314

PAVUK

TABLE Principal

Weed

Species

Late May to mid-July: dandelion, Taraxacum strigosus Muhlenberg Mid-July to September: pigweed, Amaranthus

._

weed

Diverse

lambsquarter, retroflexus L. weed

Treatments

35

E .$

weed

1988

aruense L.; fleabane, Erigeron

Chenopodium

album

L.;

plots

Late May to late July: Muhlenbergia frondosa (Poiret) Fernald; yellow nutsedge, Cyperus esculentus L. Late July-September: giant foxtail, Setaria jaberii Hermann; fall panicum, Panicum dichotomiflorum Michaux; barnyardgrass, Echinochloa cru.-galli (L.); large crabgrass, Digitaria sanguinalis (L.) Mixed

0

q 1989

plots

Canada thistle, Cirsium oficinale Weber; daisy

Grassy

STINNER

1

in Vegetationally Broadleaf

AND

plots

0 No Weeds

ties present in the weedy treatments from May through September. Figure 1 shows the mean numbers of European corn borer larvae collected in the four treatments during the study. Greater numbers of larvae were collected from the weedless treatment than from weedy treatments both years, and especially in 1989. In both years of the study, larval density (number of larvae per corn plant) and damage (number of tunnels per corn plant) were significantly lower in treatments with broadleaf weeds than in treatments without broadleaves. In addition, larval density was significantly lower in treatments with

50

n 1988

T

Grasses

Mixed Weed:

Treatment ‘Total

FIG. 2.

Late May to mid-July: Cirsium aruense; Taraxacum oficinale; Cyperus esculentus; Muhlenbergia frondosa; Erigeron strigosus Mid-late July to September: Setaria faberii; Panicum dichotomiflorum; Cherwpodium album; Amaranthus retrofkxus; Echinochloa crus-galli; Digitaria sanguinalis

Broadleaves

borus

Percentage

Ostrinia

nubilalis

larvae

number of larvae collected parasitized

by Eri-

terebrans.

grasses than those without grasses in 1989 (Pavuk and Stinner, 1991a). The only parasitoid reared from second generation 0. nubilalis larvae in both years was the solitary campoplegine ichneumonid, Eriborus terebrans. The single exception was a tachinid, tentatively identified as Lydella thompsoni, reared from a larva in 1988. In each treatment, percentage parasitism was considerably greater in 1989 than in 1988 (Fig. 2), and the range across treatments was also greater in the second year of the study. In terms of 0. nubilalis larval parasitism, the interaction between broadleaf and grassy weeds was not significant for either year (1988: F = 0.09, df = 1, 9, P > 0.7; 1989: F = 0.14, df = 1, 9, P > 0.7). Broadleaf weeds had no significant influence on larval parasitism either year (1988: F = 0.21, df = 1, 9, P > 0.5; 1989: F = 0.03, df = 1, 9, P > 0.8) and neither did grasses (1988: F = 0.01, df = 1, 9, P> 0.9; 1989: F = 1.4, df = 1, 9, P> 0.2). Correlation between number of larvae per plant (larval density) and percentage larvae parasitized was significant in the broadleaf weeds treatment in 1988 (n = 16,Z = 2.1, P < 0.05). There were no significant correlations in the rest of treatments in 1988, and no significant correlations were observed in the second year in any treatments. DISCUSSION

0 No Weeds

Broadleaves

Grasses

Mixed Weeds

Treatment FIG. 1

Number

of Ostrinia

nubilalis

larvae

collected.

Parasitism of second generation 0. nubilalis larvae by E. terebrans was not significantly influenced by the presence of weeds, although there was a trend for greater parasitism in treatments with weeds than in the weedless planting (Fig. 2). E. terebrans is considered to be a specialist on 0. nubilalis (Carlson, 1979); parasitism of

INFLUENCE

OF

WEEDS

ON

PARASITISM

other Ostrinia species, such as the smartweed borer, Ostrinia obumbratalis, has been observed, but there was no emergence of parasitoid adults (Baker et al., 1949). Thus, it is unlikely that E. terebrans was using other lepidopterous larvae on the weeds as hosts. Ichneumonidae are known to feed on extrafloral nectar (Bugg et al., 1989), and Leius (1967) observed increased parasitism of codling moth and tent caterpillar larvae in orchards that had herbaceous flora consisting of various flowering species. It is possible that E. terebrans feeds on nectar of various weeds possessing extrafloral nectaries, and that such vegetation in and around corn plantings may be visited by this species. However, we did not attempt to determine utilization of the flowering weeds present by E. terebrans, and lack of significant effects of different weed types on corn borer larval parasitism indicated no apparent benefit of the weeds in the corn plantings to this parasitoid. In addition, the flowering weeds that were present may not have been preferred by, or had nectar accessible to, E. terebrans. Therefore, whether or not this species benefited from any of the weedy vegetation is speculative. The relatively small plot size may also have obscured any significant findings. Landis and Haas (1992) observed greater parasitism rates of 0. nubilalis by E. terebrans on edges of large fields than in field interiors, but in small fields no differences were noticed. E. terebrans is a strong flier, and could have easily dispersed across the plots. In addition, numerous large cornfields were close to the experimental area, and parasitoids could have dispersed from these fields into the study plots. Lack of significant correlations between host density and E. terebrans parasitism may indicate that this parasitoid is not affected by variation in host density. Baker et al. (1949) observed that E. terebrans parasitism of 0. nubilalis was not density dependent, a trend also found by Landis and Haas (1992). Density dependence may not be common for insect parasitoids (Stiling, 1987), and perhaps E. terebrans is like many other species in this regard. Although in our study parasitism of 0. nubilalis by E. terebrans was not significantly influenced by the presence of weeds, proximity to cornfields of weed species possessing nectar accessible to this parasitoid could be beneficial. Higher parasitization rates occur along edges of large cornfields bordered by woody vegetation (Landis and Haas, 1992). Weeds in or near cornfields may also harbor alternate hosts for certain European corn borer larval parasitoids (Pavuk and Stinner, 1991b). One possible study to further assess the effects of weeds on parasitism of 0. nubilalis larvae would compare large corn plantings having weeds adjacent to them with plantings lacking weeds. Because of the mobility of both 0. nubilalis and its parasitoids, distances between these study sites would have to be large, perhaps on the scale of kilometers. In addition, studies which manipulate

OF

0.

nubilalis

BY

315

E. terebruns

border vegetation of cornfields or incorporate strips of plants which have nectaries accessible to parasitoids into cornfields to determine the influences of such vegetation on parasitism of European corn borer by E. terebrans and other parasitoids could be logical steps in research on 0. nubilalis-parasitoid interactions. ACKNOWLEDGMENTS We thank D. A. McCartney and J. P. Reed for generous field assistance, B. Bishop for statistical advice, and R. W. Carlson, Taxonomic Services Unit, Systematic Entomology Laboratory, USDA-ARS, BARC, Beltsville, Maryland, for identifying Eriborw terebrans. The manuscript was greatly improved by comments from F. F. Purrington, L. R. Nault, D. J. Horn, C. W. Hoy, and two anonymous reviewers. Salaries and research support were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, Wooster, Ohio. This is manuscript number 19892.

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