Elsevier

Biological Control

Volume 59, Issue 3, December 2011, Pages 373-383
Biological Control

The effect of temperature and exposure to Beauveria bassiana on tarnished plant bug Lygus lineolaris (Heteroptera: Miridae) population dynamics, and the broader implications of treating insects with entomopathogenic fungi over a range of temperatures

https://doi.org/10.1016/j.biocontrol.2011.08.004Get rights and content

Abstract

Tarnished plant bugs, Lygus lineolaris (Palisot de Beauvois) (Heteroptera, Miridae) are a major pest of cotton in most cotton growing regions of the Southern US. Studies were conducted to investigate how temperature and Beauveria bassiana (Balsamo) Vuilllemin infection impacted L. lineolaris fecundity and longevity, with the goal of determining what temperatures optimized B. bassiana’s control potential. B. bassiana-treated adult females and controls were maintained at constant 18 °C, 21 °C, 25 °C, 30 °C or 32 °C. The number of eggs laid was determined daily until death. B. bassiana caused large reductions in the total number of eggs laid (45–76%) at all temperatures; however, there was no effect of infection on the daily rate of egg production. There was not a sub-lethal effect of infection on egg production on the last full day of life. Intrinsic rates of natural increase and population doubling times were marginally affected by treatment with B. bassiana; doubling times increased with treatment a mean of 3.5 days (range 0.5–7.7 days). There was a temperature dependent trend in the length of the preoviposition period and the days to death after treatment with B. bassiana. As temperature increased from 18 °C to 32 °C, the number of days to death converged on the preoviposition period. The maximum difference was observed at 18 °C (5.3 days different) compared to 30 °C and 32 °C (0.3 days). These results strongly suggested that treatment of tarnished plant bugs with B. bassiana should be performed when plant bugs are in diapause or when temperatures are cool to minimize reproduction during the disease incubation period.

Highlights

Beauveria bassiana reduced Lygus lineolaris egg laying by 45–76% at temps between 18 °C and 32 °C. ► B. bassiana had little impact on life table parameters including rm, R0, DT, and GT. ► Days-to-death of treated bugs converged on the preoviposition period as temp increased. ► B. bassiana treatments should be performed against bugs in diapause or at cool temps.

Introduction

Tarnished plant bugs, Lygus lineolaris (Palisot de Beauvois) (Heteroptera, Miridae) are a major pest of cotton and many fruit, seed, forage and vegetable crops grown in the United States. The development of resistance by tarnished plant bugs to many of the major classes of insecticides (Snodgrass and Scott, 2002, Hollingsworth et al., 1997, Snodgrass, 1996, Snodgrass et al., 2009) has prompted research into alternative methods of tarnished plant bug management. One such alternative that has received attention is entomopathogenic fungi like Beauveria bassiana (Balsamo) Vuillemin, which has been found infecting field-collected lygus (Leland and Snodgrass, 2004, McGuire, 2002).

B. bassiana isolates from field-collected L. lineolaris and L. hesprus Knight have been shown in laboratory studies to be virulent against adult tarnished plant bugs (Leland, 2005, Leland et al., 2005, McGuire et al., 2005), but field tests targeting tarnished plant bugs with B. bassiana have had mixed results. Noma and Strickler (2000) treated plots of alfalfa, Medicago sativa L. infested with lygus during pre-bloom and bloom. Despite infection rates ranging from approximately15% to 90% in both the nymphal and adult stages, there was a significant population reduction in only one of three pre-bloom trials and no reduction in any of the three bloom trials. Steinkraus and Tugwell (1997) showed that large percentages (75–100%) of field-collected adult tarnished plant bugs died within 5–7 days when they were caged on cotton plants and treated directly with B. bassiana or when tarnished plant bugs were caged on pre-treated cotton plants. Similarly, they showed high levels of control (85–92%) when field-collected tarnished plant bugs were caged and treated on canola; control at the population scale was not investigated. Leland and McGuire (2006) tested three isolates of B. bassiana against L. lineolaris in pigweed (Amaranthus spp.). They did not find significant population reductions relative to controls. McGuire et al. (2006) tested the same three isolates as Leland and McGuire (2006) against L. hesprus in alfalfa and despite high levels of infection three days post-treatment (76–82%), reductions in the adult population were not observed until 10 days post-treatment (33–42% reduction). There was no detectable effect of treatment with any of the fungal isolates tested against nymphs.

Entomopathogenic fungi are relatively slow-acting biological control agents compared to synthetic chemical pesticides. Because of this, their success depends in part on the insects’ reproductive capacity during the disease incubation period (Ugine et al., 2005). Entomopathogenic fungi, which can take several days to kill an insect, would also presumably be more effective in suppressing the population growth of insects that have long preoviposition periods such as tarnished plant bugs in cool weather (Ugine, 2011) (i.e. if they are treated early after adult eclosion). A long preoviposition period extends the window of opportunity for a fungus to kill an insect before it replaces itself via oviposition. Numerous researchers have investigated the effects of fungal infection on insect population dynamics (Blanford and Thomas, 2001, Castillo et al., 2000, Ekesi and Maniania, 2000, Fargues et al., 1991, Hsiao et al., 1992, Noma and Strickler, 2000, Ugine et al., 2006). Findings in these studies included significant reductions in lifetime fecundity, eggs per clutch, and egg viability. Other investigators have reported no significant pre-mortem effects of fungal infection on fecundity of insect hosts (Lacey et al., 1997, Lord et al., 1987, Nielsen et al., 2005, Wang and Knudsen, 1993). Temperature affects fungal growth parameters (e.g. germination/penetration speed, cell growth rate) and insect developmental and reproductive rate. Knowledge of the effect of temperature on the interaction between the fungal infection and insect reproduction will help determine the optimum temperature at which B. bassiana should be deployed against tarnished plant bug populations. Therefore, studies were conducted to determine the nature of the interaction between temperature and B. bassiana infection on L. lineolaris fecundity and longevity.

Section snippets

Liquid fermentation

B. bassiana strain TPB3 (ARSEF 8889), was grown in liquid culture for injection into barley-filled bags as follows. A conidial suspension of 106 conidia/ml in 0.02% Tween 80 was prepared, and a 100-μl aliquot was spread onto 1/2-strength Sabouraud dextrose agar (Becton, Dickinson and Co., Sparks, MD) supplemented with 1% yeast extract (SDAY). The culture was incubated at 25 °C in total darkness. When the culture was three days old, three 2-mm-diam. agar plugs supporting B. bassiana growth were

Longevity post-treatment with B. bassiana

The lifespan of female tarnished plant bugs was significantly affected by temperature in Tests 1 and 2 (Test 1: F[4, 267] = 7.4, P < 0.0001; Test 2: F[4, 171] = 10.5, P < 0.0001), and by treatment with B. bassiana (Test 1: F[1, 267] = 103.5, P < 0.0001; Test 2: F[1, 171] = 109.4, P < 0.0001), but not by the temperature × treatment interaction (Test 1: F[4, 267] = 0.77, P = 0.55; Test 2: F[4, 171] = 0.69, P = 0.60) (Table 1). Of all the insects treated with B. bassiana in Tests 1 and 2, only two did not support fungal

Discussion

Adult tarnished plant bugs treated with B. bassiana and maintained at a range of constant temperatures (18–32 °C) lived significantly shorter lives compared to their control counterparts. As expected, insects maintained at cooler temperatures lived longer than insects maintained at warmer temperatures irrespective of treatment with B. bassiana. There was also a significant effect of temperature on total egg production post-treatment in Test 1 for both treated and control tarnished plant bugs;

Acknowledgments

I would like to thank Gordon Snodgrass for sharing with me his extensive knowledge and expertise of tarnished plant bugs. I would also like to thank Tabatha Ramsey and Gerald Gibson for technical assistance, and Brenda Woods for providing me tarnished plant bug egg packs.

References (42)

  • T.A. Ugine et al.

    Development of a novel bioassay for estimation of median lethal concentrations (LC50) and doses (LD50) of the entomopathogenic fungus Beauveria bassiana, against western flower thrips, Frankliniella occidentalis

    Journal of Invertebrate Pathology

    (2005)
  • T.A. Ugine et al.

    Influences of impatiens pollen and exposure to Beauveria bassiana on bionomics of western flower thrips Frankliniella occidentalis

    Biological Control

    (2006)
  • S.P. Wraight et al.

    Pathogenicity of the entomopathogenic fungi Paecilomyces spp. and Beauveria bassiana against the silver leaf whitefly, Bemisia argentifolii

    Journal of Invertebrate Pathology

    (1998)
  • L.C. Birch

    The intrinsic rate of natural increase of an insect population

    Journal of Animal Ecology

    (1948)
  • A. Burgerjon

    Pulvérisation et poudrage au laboratoire par des préparations pathogènes insecticides

    Annales des Epiphyties

    (1956)
  • A.C. Cohen

    New oligidic production diet for Lygus hesperus Knight and L Lineolaris (Palisot de Beauvois)

    Journal of Entomological Science

    (2000)
  • W.J. Conover

    Practical Nonparametric Statistics

    (1999)
  • J.W. Debolt et al.

    Lygus hesperus

  • S. Ekesi et al.

    Susceptibility of Megalurothrips sjostedti developmental stages to Metarhizium anisopliae and the effects of infection on feeding, adult fecundity, egg fertility and longevity

    Entomologia Experimentalis et Applicata

    (2000)
  • J. Fargues et al.

    Fecundity and egg fertility in the adult Colorado beetle (Leptinotarsa decemlineata) surviving larval infection by the fungus Beauveria bassiana

    Entomologia Experimentalis et Applicata

    (1991)
  • S.J. Fleischer et al.

    Lygus lineolaris (Heteroptera: Miridae) population dynamics: nymphal development, life table, and Leslie matrices on selected weeds and cotton

    Environmental Entomology

    (1988)
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