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Adult Survival, Maturation, and Reproduction of the Desert Locust Schistocerca Gregaria Infected with the Fungus Metarhizium Anisopliae Var Acridum

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Adult Survival, Maturation, and Reproduction of the Desert Locust Schistocerca Gregaria Infected with the Fungus Metarhizium Anisopliae Var Acridum Journal of Invertebrate Pathology 78, 1–8 (2001) doi:10.1006/jipa.2001.5031, available online at http://www.idealibrary.com on Adult Survival, Maturation, and Reproduction of the Desert Locust Schistocerca gregaria Infected with the Fungus Metarhizium anisopliae var acridum Simon Blanford and Matthew B. Thomas Leverhulme Unit for Population Biology and Biological Control, NERC Centre for Population Biology and CABI BIOSCIENCE, Imperial College, Silwood Park, Ascot, Berkshire, SL5 7PY, United Kingdom E-mail: [email protected] Received August 2, 2000; accepted May 3, 2001; published online July 12, 2001 have also assessed the impact that infection may have Studies were conducted with two different doses of on host behaviors that contribute to the status of the Metarhizium anisopliae var acridum to examine the target insect as a pest. These include studies on effects effects on survival and reproductive potential of adult of infection on feeding (e.g., Johnson and Pavlikova, Schistocerca gregaria under conditions that either 1986), developmental time (Subrahmanyam and Ra- limited thermoregulation or enabled optimal thermo- regulation. Adult S. gregaria infected with the fungal makrishnan, 1980; Olfert and Erlandson, 1991), and pathogen showed either a rapid and high mortality at fecundity (Fargues et al., 1991; Zaki, 1998). However, relatively constant temperatures or a much reduced these studies are generally conducted under environ- mortality and lengthened survival time when allowed mentally constant regimes that are conducive for in- to thermoregulate. Mortality rate varied from >90% fection and do not consider how these behaviors and after 10 days under constant temperature conditions the overall impact of the pathogen might change under to 66% after 70 days under optimal thermoregulatory more realistic, variable conditions experienced in the conditions. Effects of infection on maturation and re- field. production depended on the age of the adults at the For example, in the LUBILOSA program (see Ac- time of inoculation, the nighttime temperature re- knowledgments), which is developing a mycoinsecti- gime, the fungal dose, and the length of time of the cide for locust and grasshopper control, previous stud- monitoring period. No difference in reproductive be- haviors in treated and control insects were found in ies have indicated that infection with the fungal ento- one experiment that utilized older adults and was con- mopathogen Metarhizium anisopliae var acridum ducted over 25 days. In a second experiment with [formerly Metarhizium flavoviride Gams and Rozsypal, newly fledged locusts, differences in maturation rates but now reclassified (Driver et al., 2000)] can reduce and total reproductive output were observed due to feeding and flight ability in the desert locust Schisto- infection. The results from these experiments are dis- cerca gregaria Forskål (Moore et al., 1992; Seyoum et cussed in terms of the potential of M. anisopliae var al., 1994). Although useful in highlighting the poten- acridum to alter the balance of insect endocrine sys- tial for such reductions, these studies were conducted tems and the importance of the assessment of behav- at constant temperatures optimal for fungal develop- ioral changes and their impact on microbial control ment and gave the pathogen maximum opportunity not agents in the long term. © 2001 Academic Press only to cause these important prelethal effects but also Key Words: Schistocerca gregaria; Metarhizium anisopliae var acridum; thermoregulation; fungal to induce high and rapid mortality. However, several pathogens; biological control; locusts; pathogenicity studies have now shown speed of kill of a range of of; bioassay. pathogens in locusts and grasshoppers to be dependent on environmental temperature and host thermal biol- ogy (Carruthers et al., 1992; Inglis et al., 1996, 1997, INTRODUCTION 1999; Blanford et al., 1998; Blanford and Thomas, 1999a,b). Accordingly, it is likely that sub- and prele- Whereas the majority of studies assessing pathogens thal effects of pathogens will also be affected with as biocontrol agents deal with their ability to produce potential considerable change in relative importance. mortality in the target pest, a considerable number Thus, there is a need to consider the impact of 1 0022-2011/01 $35.00 Copyright © 2001 by Academic Press All rights of reproduction in any form reserved. 2 BLANFORD AND THOMAS M. anisopliae var acridum infections when locusts and 9 h per day, and external lighting was switched on for grasshoppers are exposed to more realistic thermal 1.5 h at the beginning and end of this period. This gave regimes and where behavioral thermoregulation is a 12-h light period but locusts were limited in their made possible. The aim of this study, therefore, was to ability to raise internal body temperatures to 9 h per examine the effects of M. anisopliae var acridum on day. One treatment was inoculated with 1 ϫ 103 adult S. gregaria under realistic thermal regimes. Two conidia of M. anisopliae var acridum in the same man- experiments are presented in which mortality, matu- ner as that described above and the second treatment ration, and reproduction were assessed in adult locusts was left uninoculated as a control. These two treat- following infection. ments are designated as the “thermoregulation treat- ments” in future discussion. MATERIALS AND METHODS All locusts were fed an excess of cassava (Manihot esculenta), the thermoregulation treatments being reg- Experiment 1 ularly checked to ensure that fresh food was always available as the higher temperatures caused food This experiment was conducted at the International ϳ Institute of Tropical Agriculture in Benin, west Africa plants to wilt more rapidly than those in the 30°C and used 10-day-old (i.e., 10 days postfledging) adult S. treatments. gregaria taken from a long established research colony Mortality was monitored every 24 h and dead insects at the institute. Four treatments were used. For the were removed and placed in humid conditions (100% first two, 40 locusts per treatment were divided into RH) at 30°C to encourage sporulation. The cumulative four wood-framed cages (60 ϫ 60 ϫ 70 cm) with mos- mortality response across the assessment period was quito-mesh sides and roof. Each cage contained 5 male analyzed with Kaplan–Meier survival analysis in and 5 female locusts. Cages were positioned in an SPSS for Windows 6.1. open-sided, covered area. Thus, they experienced am- Maturation rate was assessed by observation of color bient daylight and temperature conditions but were change in male locusts. Each locust was given a score protected from direct sunlight, wind, and rain. Ambi- between one (immature and mostly pink) and five (ma- ent temperature in these cages ranged from 28 to 33°C ture and fully yellow) after Norris (1954). Observations and no internal light or heat source was provided in the were also made on time of first copulation and time of cage. One treatment was inoculated with M. anisopliae first oviposition. Fecundity was assessed by measure- var acridum. Insects were inoculated in a standardized ment of the number of egg pods laid, eggs per pod, and bioassay method similar to that described in Prior et al. successful eclosion from these pods. (1995). The fungal isolate was a single conidial isolate of M. anisopliae var acridum, isolate IMI 330189. Experiment 2 Conidial suspensions were formulated in groundnut oil and these suspensions were placed in a bath sonicator This second experiment used adult S. gregaria that for 1 min to break up the conidial chains, and conidial were just 3 days postfledging. Each treatment con- counts were made with a hemocytometer. Each locust tained seven male/female pairs per cage with four ␮ in the treatment groups received 1 l of conidial sus- cages per treatment. Cage size and layout were similar pension applied with a micropipette beneath the dorsal to those described above and maintained under the pronotal shield. Spore suspensions were adjusted to same light:dark regime and the same thermoregula- ϫ 3 give 1 10 conidia per insect. Control insects were tory regime (i.e., light bulbs were switched on for 9 h). left uninoculated as previous experiments have shown Temperatures in the cages ranged from 33 to 46°C no effect of the formulating oils (Blanford, 1999). These while the light bulbs were switched on. During the two treatments are designated as the “ϳ30°C treat- night temperatures were again left at ambient which, ments” in future discussion. Ϯ The remaining two treatments consisted again of 40 during the study period, averaged 20.5 0.1°C, with adult S. gregaria of the same age and sex ratio divided maximum of 27.6°C and minimum of 15.8°C. Insects between four similar cages per treatment. In these were hand-inoculated by the methodology described cages a 40-W light bulb was placed three-quarters of above. Three treatments were used. One treatment ϫ 3 ϫ 5 the way up the rear wall and a wire mesh climbing received 5 10 conidia/insect, one received 1 10 tube was fixed in front of the light bulb so that insects conidia per insect, and one was designated as an uni- could choose a variety of perching and, therefore, ther- noculated control. moregulating sites. Temperatures next to and directly Mortality, maturation rate, and observations on above the bulb reached 44–46°C while those at the mating and oviposition were monitored as above, as bottom of the cage were 31–34°C. Nighttime tempera- were egg pods laid and number of eggs per pod. tures fluctuated with ambient temperatures (29 Ϯ No assessment was made of eclosion in this experi- 2°C). Light bulbs inside the cage were switched on for ment. S. gregaria INFECTED WITH M. anisopliae VAR acridum 3 TABLE 1 Average Survival Time and Significance between Treatments for Adult Schistocerca gregaria Experiment 1 (a) Kaplan–Meier analysis of average survival time (days Ϯ SE) in SPSS for Windows Control (ϳ30°C) Treated (ϳ30°C) Control (thermoregulate) Treated (thermoregulate) AST (ϮSE) 23.45 (Ϯ0.40) 8.48 (Ϯ0.33) 24.46 (Ϯ0.19) 23.44 (Ϯ0.42) 95% Conf.
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