Abundance, Distribution, and Availability of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) Hosts in a Soybean Agricultural System in Southeastern Queensland

Biological Control 18, 120 –135 (2000) doi:10.1006/bcon.2000.0827, available online at http://www.idealibrary.com on

Abundance, Distribution, and Availability of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) Hosts in a Soybean Agricultural System in Southeastern Queensland A. D. Loch 1 Department of Entomology, The University of Queensland, Brisbane, Queensland 4072, Australia Received November 24, 1998; accepted January 17, 2000

Seasonal patterns of abundance and distribution of all life stages of known Trissolcus basalis (Wollaston) host species on different plant species in a soybean agricultural system in southeastern Queensland, Australia are reported. In particular, the seasonal phenology of different bug species is described with emphasis on periods of oviposition. Twelve hosts for T. basalis were identified, with three pentatomid bugs, green vegetable bug, green stink bug, and horehound bug, predominating. These three species appear to undergo at least three generations per year with mating and oviposition occurring during all months between September and April but mainly during October and January–April. Horehound bug is the only known T. basalis host that does not diapause during winter and continues to oviposit during winter at low levels. These results suggest that T. basalis is not host limited temporally except during winter when hosts are scarce. Results also show that T. basalis hosts are spatially aggregated at a number of levels, but how this affects T. basalis and the subsequent degree of biological control has yet to be investigated. © 2000 Academic Press Key Words: Trissolcus basalis; Nezara viridula; Plautia affinis; Agonoscelis rutila; Piezodorus grossi; Cuspicona simplex; egg parasitoid; temporal distribution; spatial distribution; alternative host; host plant; biological control.

INTRODUCTION

In Australia, the egg parasitoid Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) has been regarded as a highly successful biological control agent of the green vegetable bug, Nezara viridula (L.) (Hemiptera: Pentatomidae) (Wilson, 1960; Ratcliffe, 1 Current address: CSIRO Entomology, c/o Department of Conservation and Land Management, Brain Street, Manjimup, Western Australia 6258, Australia. Fax: (618) 9777-1183. E-mail: a.loch@ ccmar.csiro.au.

1049-9644/00 $35.00 Copyright © 2000 by Academic Press All rights of reproduction in any form reserved.

1965; Waterhouse and Wilson, 1968; Caltagirone, 1981; Waterhouse and Norris, 1987; DeBach and Rosen, 1991; Waterhouse, 1998). This widely accepted view has been questioned on the basis of the weakness of the supporting evidence (Clarke, 1990, 1992b, 1993). Recent grower surveys and field studies have demonstrated that the green vegetable bug persists as a pest throughout much of eastern Australia (Clarke, 1992b), where recorded parasitism rates are low (Forrester, 1979; Titmarsh, 1979; Kelly, 1987; Clarke, 1992a; Clarke and Walter, 1993a; Seymour and Sands, 1993; Velasco et al., 1995). In southeastern Queensland, the green vegetable bug completes two principal generations each year (Velasco et al., 1995). The first generation occurs in spring, primarily on variegated thistle, Silybum marianum (L.) Gaertn., turnip-weed, Rapistrum rugosum (L.) All, and wild radish, Raphanus raphanistrum L., with the second generation, in autumn, concentrated on soybean, Glycine max (L.) Merr. (Clarke and Walter, 1993a,b; Velasco et al., 1995). During summer, densities of all stages of the green vegetable bug are low, probably because host plants suitable for adult reproduction and nymphal development are unavailable (Velasco and Walter, 1992; Velasco et al., 1995). Survival rates of adult T. basalis are lowest during summer (Clarke and Walter, 1993a), when green vegetable bug egg masses are scarce (Velasco et al., 1995). Clarke and Walter (1993a) therefore hypothesized that the poor survival rate of T. basalis over summer, coupled with the scarcity of green vegetable bug hosts during summer in southeastern Queensland, may be limiting populations of T. basalis and thus reducing its impact as a biological control agent. They assumed, tacitly, that during summer other host species are unavailable for maintenance of T. basalis populations. In Australia, T. basalis has been recorded parasitizing at least 25 species of bugs from the families Pentatomidae, Scutelleridae, Alydidae, and Coreidae (Table 1). In the soybean agricultural system on the Darling Downs,

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ABUNDANCE AND DISTRIBUTION OF Trissolcus basalis HOSTS

TABLE 1 Bug Species Recorded as Laboratory and Field Hosts for Trissolcus basalis in Australia Source Family species Pentatomidae *Green vegetable bug, Nezara viridula (L.) *Horehound bug, Agonoscelis rutila (F.)

Laboratory host

Field host

Kelly, 1987; Clarke, 1992a; Loch and Walter, 1999 Kelly, 1987

*Green stink bug, Plautia affinis (Dallas) *Green potato bug, Cuspicona simplex Walker Cuspicona forticornis Breddin Cuspicona sp. Spined citrus bug, Biprorulus bibax Breddin Plorscha spp. Dictyotus inconspicuus Dallas *Brown shield bug, Dictyotus caenosus (Westwood) Piezodorus spp. *Ricespotting bug, Eysarcoris trimaculatus (Distant) *Redbanded shield bug, Piezodorus grossi Staddon *Predatory shield bug, Cermatulus nasalis (Westwood) *Predatory shield bug, Oechalia schellenbergii (Gue´rin-Me´neville) Alciphron glaucus (F.) Anaxarchus reyi (Montrouzier) Menestheus brevis Van Duzee Unidentified species A Unidentified species B Unidentified species C Alydidae *Podsucking bug or brown bean bug, Riptortus serripes (F.) *Podsucking bug or brown bean bug, Melanacanthus scutellaris (Dallas) Scutelleridae Cotton harlequin bug, Tectocoris diophthalmus (Thunberg) Coreidae Fruit spotting bug, Amblypelta nitida Stål Unidentified family *Unidentified species

S. A. Khan, unpublished data S. A. Khan, unpublished data

Strickland, 1979; Kelly, 1987; Clarke, 1992a; Loch and Walter, 1999 Noble, 1937; Kelly, 1987; Clarke, 1992a; Field et al., 1998; Loch and Walter, 1999 Coombs and Khan, 1998; Loch and Walter, 1999 Loch and Walter, 1999 Noble, 1937

Noble, 1937 Kelly, 1987 Kelly, 1987 Forrester, 1979

Forrester, 1979; Loch and Walter, 1999

Kelly, 1987 Strickland, 1979 Forrester, 1979 Forrester, 1979; Kelly, 1987 Forrester, 1979; Kelly, 1987

S. S. S. S. S. S.

A. A. A. A. A. A.

Khan, Khan, Khan, Khan, Khan, Khan,

unpublished unpublished unpublished unpublished unpublished unpublished

Forrester, 1979; Strickland, 1979; Loch and Walter, 1999 Forrester, 1979; Awan, 1989; Loch and Walter, 1999 Forrester, 1979; Strickland, 1979; Awan, 1989; Clarke, 1992a; Field et al., 1998; Loch and Walter, 1999

data data data data data data Strickland, 1979

Forrester, 1979

Strickland, 1979

Strickland, 1979

S. A. Khan, unpublished data Loch and Walter, 1999

Note. An asterisk (*) before a bug species denotes those species surveyed in this study.

southeastern Queensland, an area where the green vegetable bug is a serious pest (Clarke, 1990, 1992b; Velasco et al., 1995; Waterhouse, 1998), at least 12 host species are available to T. basalis (Table 1, Loch and Walter, 1999). I investigated the temporal and spatial availability of T. basalis host species in the soybean agricultural system on the Darling Downs in southeastern Queensland, Australia. Specifically, I asked whether

green vegetable bug eggs are scarce during summer and, if so, whether eggs of other host species are available to T. basalis then. Because many T. basalis host species are phytophagous and dependent on host plant availability, understanding the phenology of phytophagous bug species in relation to host plants is fundamental to understanding host availability for T. basalis. I conducted field surveys to quantify the seasonal patterns of abundance of all

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TABLE 2 Plant Species from Which Each of Nine Phytophagous Bug Species Was Recorded during Field Surveys on the Darling Downs from September 1996 to April 1998 Bug species b Family plant species a Amaranthaceae Amaranthus spp. Asteraceae Variegated thistle, Silybum marianum (L.) Gaertn. Spear thistle, Cirsium vulgare (Savi) Ten. Brassicaceae Turnip-weed, Rapistrum rugosum (L.) All. Buchan weed, Hirschfeldia incana (L.) Lagreze-Fossat Wild radish, Raphanus raphanistrum L. Caesalpiniaceae Bird of paradise tree, Caesalpinia gilliesii (Hook.) Dietr. Chenopodiaceae Prickly roly poly, Sclerolaena muricata (Moq.) Domin Fabaceae Spurred vetch, Vicia monantha Retz. Hexham scent, Melilotus indicus (L.) All. Bokhara clover, Melilotus albus Medik Mungbean, Vigna radiata (L.) Wilezek Soybean, Glycine max (L.) Merr. Lucerne, Medicago sativa L. Green bean, Phaseolus spp. Lamiaceae Mintweed, Salvia reflexa Hornem. Horehound, Marrubium vulgare L. Malvaceae Bladder ketmia, Hibiscus trionum L. Onagraceae Clockweed, Gaura parviflora Hook. Solanaceae Glossy nightshade, Solanum americanum Miller Blackberry nightshade, Solanum nigrum L. Wild gooseberry, Physalis spp. Verbenaceae Purpletop, Verbena bonariensis L.

GVB

GSB

⻫*

⻫*

⻫* ⻫*

⻫* ⻫*

⻫* ⻫* ⻫*

⻫

⻫*

⻫

HB

RSB

GPB

BSB

RB

PB

⻫

⻫*

⻫*

⻫

⻫

⻫

⻫ ⻫

⻫ ⻫

⻫ ⻫

⻫* ⻫*

⻫ ⻫

⻫ ⻫ ⻫* ⻫* ⻫* ⻫* ⻫ ⻫*

⻫*

⻫* ⻫*

⻫* ⻫*

⻫ ⻫ ⻫* ⻫* ⻫*

⻫ ⻫* ⻫*

⻫

⻫*

⻫* ⻫*

⻫*

⻫* ⻫* ⻫

⻫* ⻫*

⻫*

⻫*

⻫* ⻫*

Note. A tick (⻫) indicates that the bug species was recorded from that plant species, whereas a blank space indicates those plants from which that bug was never recorded. An asterisk (*) beside a tick indicates that at least one egg mass of that bug species was collected from that plant species. a Plants sampled that yielded no bugs included sorghum, Sorghum bicolor (L.) Moench, barley, Hordeum vulgare L. (Poaceae), and sunflower, Helianthus annuus L. (Asteraceae). b GVB, green vegetable bug; GSB, green stink bug; HB, horehound bug; RSB, redbanded shield bug; GPB, green potato bug; BSB, brown shield bug; RB, ricespotting bug; and PB, two podsucking bug species, Riptortus serripes and Melanacanthus scutellaris.

life stages of known T. basalis host species on different plant species. I also quantified aspects of the spatial patterns of abundance of each bug species within and across patches of each plant species. Host plant species that supported high densities of bugs and high rates of mating and oviposition of each bug species are identified. The seasonal phenology of different bug species is described with particular reference to periods of oviposition. The discussion translates the multispecies patterns of egg abundance, across both space and time, into patterns of host availability for T. basalis in the field. More robust interpretations about the ecology of T. basalis and

the biological control of green vegetable bug can thus be made. MATERIALS AND METHODS

Field Survey Monthly surveys for all life stages of T. basalis hosts were conducted across two summers on the Darling Downs between September 1996 and April 1998 in an area circumscribed by a 50-km radius from Pittsworth (27° 43⬘S, 151° 38⬘E). Plants sampled (Table 2) included previously recorded hosts for the green vegeta-

ABUNDANCE AND DISTRIBUTION OF Trissolcus basalis HOSTS

ble bug (Velasco, 1989; Velasco and Walter, 1992; Clarke and Walter, 1993b; Velasco et al., 1995) and other plants on which I recorded bugs that are parasitized by T. basalis (see Table 1). Bug abundance on individual plants of each species was determined by visually scanning mature fruiting plants of each species on each sampling occasion and counting the number of egg masses, nymphs (categorized into two groups: instars 1–3 and instars 4 –5), adults, and mating pairs of each bug species. The number of plants of each species sampled on each sampling occasion was not fixed because most plants sampled were weeds, which vary in their seasonal availability and abundance. Therefore, as many plants of each species as possible were sampled on each sampling occasion to provide the most accurate representation of the abundance and distribution of each bug species (see Figs. 1, 3, 5, 7, and 9 for mean ⫾ SE number of plants sampled). Individual plants of each species were sampled haphazardly because of differences in plant patch size and distribution. Whenever possible, bugs were sampled from the same species of host plant in two or more discontinuous patches on each sampling occasion. Adults and nymphs of each species collected were identified using the keys of Gross (1975, 1976) and Larivie`re (1995) and/or by comparison with specimens housed in The University of Queensland Insect Collection. Egg masses of the different bug species proved easy to distinguish in the field. In addition, all egg mass identifications were confirmed by comparing them to egg masses laid in the laboratory by different species of adult bugs collected in the field. All bug egg masses found were returned to the laboratory to assess for parasitism by T. basalis (Loch, 1999; Loch and Walter, 1999). Bug species were classed as hosts for T. basalis if adults of T. basalis emerged successfully from egg masses. Voucher specimens of T. basalis from the different host species are housed in The University of Queensland Insect Collection. Statistical Analysis G tests were employed to test the independence of mating frequencies of each bug species over time and across plant species. Data were analyzed as counts of the number of mating and nonmating bugs. Data were pooled for analyses over time because sample sizes were too small to permit a valid statistical analysis of mating across months. Data were pooled in two ways. First, mating data for the months September–November, December–February, March–May, and June–August were pooled across years as spring, summer, autumn, and winter mating data, respectively. The second pooling method grouped mating data into seasons as above, but maintained seasons in different years separately.

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RESULTS

Twelve T. basalis hosts were recorded during the monthly surveys (Table 1). The list includes seven phytophagous pentatomids, namely green vegetable bug, green stink bug, horehound bug, redbanded shield bug, green potato bug, brown shield bug, and ricespotting bug. The remaining hosts included two predatory pentatomids, O. schellenbergii and C. nasalis, two species of podsucking alydids, M. scutellaris and R. serripes, and one unidentified species from an unidentified family. The green vegetable bug, green stink bug, and horehound bug predominated during surveys. These three species are treated individually below with the results for each species presented in three sections: (1) temporal distribution on plant species (Figs. 1–10), (2) spatial distribution within and across plant patches (Figs. 1–10), and (3) mating frequency (Tables 3 and 4). The other species were present on the surveyed plants in only low numbers and irregularly, and they are treated together in a single section. Green Vegetable Bug (Nezara viridula) Temporal distribution on plant species. Green vegetable bug was sampled from over 20 species of plants (Table 2). Adults and nymphs were less abundant on most sampled plant species during 1997/1998 than 1996/1997 (Fig. 1). However, bug abundance was higher on mungbean (Fig. 1k) and soybean (Fig. 1l) during 1997/1998 than 1996/1997. Adults were first present on plants during August and September, mainly on turnip-weed (Fig. 1a), buchan weed (Fig. 1b), and variegated thistle (Fig. 1c). During September low numbers of adults were collected from spurred vetch but no mating or egg masses were recorded. Low numbers of bugs and egg masses were recorded on wild radish during September and October. Egg masses were commonly found during October, predominantly on turnip-weed (Fig. 2a), buchan weed (Fig. 2b), variegated thistle (Fig. 2c), and horehound (Fig. 2d). Consequently, nymphal instars 1–3 were common during October on the above hosts, as well as on glossy nightshade (Fig. 1e) and hexham scent (Fig. 1f). While the abundance of bugs began to decrease on senescing spring weeds (turnip-weed, buchan weed, variegated thistle, and hexham scent) during November and December, the number of adults and nymphal instars 4 –5 began to increase on mintweed (Fig. 1g), spear thistle (1996/1997 only; Fig. 1h), clockweed (Fig. 1i), and bird of paradise tree. More than 200 adults and nymphal instars 4 –5 were also collected from one prickly roly-poly plant in December 1996, but all other prickly roly-poly plants yielded low bug densities, with more than 95% of them having no bugs. By January 1997, only 2% of prickly roly-poly plants sampled had

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FIG. 1. Mean ⫹ SE density of green vegetable bug adults and nymphs (instars 1–3 and 4 –5) on different plant species and the percentage (x) of individual plants of each species infested with green vegetable bug from September 1996 to April 1998 on the Darling Downs. The dotted line above each bar chart indicates the main period when each plant species is mature, the dashed line indicates when each plant species was sampled, n is the mean ⫾ SE number of plants of each species sampled each sampling month, and p is the mean ⫾ SE number of discontinuous plant patches sampled each sampling month.

bugs present, and at no other time were bugs recorded from this plant. Egg masses and early stage nymphs were never collected from prickly roly-poly. In December, virtually all bugs sampled from turnip-

weed, buchan weed, variegated thistle, horehound, glossy nightshade, hexham scent, mintweed, and spear thistle were adults. During January, egg masses were commonly collected, mainly from horehound (Fig. 2d),

ABUNDANCE AND DISTRIBUTION OF Trissolcus basalis HOSTS

125

FIG. 1—Continued

mintweed (Fig. 2e), spear thistle (Fig. 2f), bokhara clover (Fig. 2g), and mungbean (Fig. 2h). Nymphal instars 1–3 predominated during January on the above hosts and by February, adults were the most common stage on these plant species (Fig. 1). Low bug numbers were also present on bladder ketmia, purpletop, lucerne, Amaranthus, blackberry nightshade, wild gooseberry, green bean, and turnip-weed (Fig. 1a).

Egg masses were collected during February and March principally from mintweed (Fig. 2e), spear thistle (Fig. 2f), bokhara clover (Fig. 2g), mungbean (Fig. 2h), and soybean (Fig. 2i). Nymphal instars 4 –5 were the most common stage on many hosts during March (Fig. 1). By April, most bugs were on soybean (Fig. 1l), mungbean (Fig. 1k), clockweed (Fig. 1i), mintweed (Fig. 1g), and spear thistle (1996/1997 only; Fig. 1h).

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FIG. 2. Mean ⫹ SE density of green vegetable bug egg masses on different plant species and the percentage (x) of individual plants of each species infested with egg masses from September 1996 to April 1998 on the Darling Downs.

More than 50% of bugs sampled from mungbean and soybean were nymphal instars 1–3. Some oviposition occurred in April on soybean (Fig. 2j), mungbean (Fig. 2i), and spear thistle (1996/1997 only; Fig. 2g). By May, green vegetable bug was absent on most available hosts, with only low numbers of adults recorded on turnip-weed (Fig. 1a), horehound (Fig. 1d), and bokhara clover (Fig. 1j). No bugs were recorded over winter, except during August.

Spatial distribution within and across plant patches. On most sampling occasions, less than 30% of plants of all species hosted bugs (Fig. 1) and less than 5–10% had egg masses (Fig. 2). The distribution of the green vegetable bug across plant patches could be evaluated only for those plant species where multiple patches were sampled. The bugs had an aggregated distribution with some patches hosting no bugs and other patches with bug densities varying by a factor of 10 or

ABUNDANCE AND DISTRIBUTION OF Trissolcus basalis HOSTS

127

Mating frequency. Variation in the percentage of green vegetable bug adults mating was recorded across plant species (Table 3) and over time (Table 4). Green vegetable bug adults were recorded mating on most plant species from which they were collected (Table 3). Plants from which few adults were recorded, such as hexham scent and purpletop, had no mating pairs, and there were none on horehound, although 48 adults were recorded from this plant. Significantly higher percentages of adults were recorded mating on turnipweed, buchan weed, bokhara clover, mungbean, and soybean than on other hosts (G ⫽ 81.71, df ⫽ 9, P ⬍ 0.0001; Table 3). Mating adults were recorded during all sampling months, from September to April (Table 4). Of the adults recorded each month, the percentage that was mating usually ranged between 15 and 60%, although much lower percentages were recorded during November 1996 and April 1997. When pooled across seasons, the percentage of adults mating was highest in summer and lowest in spring (G ⫽ 149.72, df ⫽ 2, P ⬍ 0.0001). When pooled across season and year, the percentage of adults mating was highest during autumn 1998 and lowest during spring 1996 and summer 1997/1998 (G ⫽ 368.92, df ⫽ 5, P ⬍ 0.0001). Green Stink Bug (Plautia affinis)

FIG. 2—Continued

more. For example, in April 1997, five discontinuous patches of soybean yielded mean ⫾ SE densities of 1.74 ⫾ 0.36, 1.26 ⫾ 0.51, 0.83 ⫾ 0.45, 0.05 ⫾ 0.02, and 0 ⫾ 0 bugs (adults and nymphs) per plant, respectively. Egg masses were collected from only one of the above five patches. The percentage of soybean plants in a patch infested with all stages of bugs at the same time varied from 0 to 45%.

Temporal distribution on plant species. Green stink bugs were recorded from a wide range of plant species (Table 2), although all stages were largely concentrated on horehound (Figs. 3a and 4a), glossy nightshade (Fig. 3b), mintweed (Fig. 3c), spear thistle (Fig. 3d), clockweed (Fig. 3e), and purpletop (Fig. 3f). The abundance of green stink bug on the above species in 1996/1997 was approximately the same as in 1997/ 1998. However, no green stink bugs (Fig. 3d) were recorded from spear thistle in the 1997/1998 period, although fruiting plants were available. Egg masses were surveyed during all sampling months between September 1996 and April 1997 and between September 1997 and December 1997 (Fig. 4). Most egg masses were recorded on horehound, with 85% (n ⫽ 308) of total egg masses collected being recorded from horehound. The abundance of egg masses on horehound per month is given in Fig. 4. During October and November, when oviposition was relatively high, nymphs were present on horehound (Fig. 3a), glossy nightshade (Fig. 3b), and mintweed (Fig. 3c). By December, most bugs were adults. In January egg masses and nymphal instars 1–3 predominated, mainly on horehound (Figs. 3a and 4), glossy nightshade (Fig. 3b), mintweed (Fig. 3c), and spear thistle (1996/1997 only). Egg masses were collected from February–April 1997 on the above plants and

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FIG. 3. Mean ⫹ SE density of green stink bug adults and nymphs (instars 1–3 and 4 –5) on different plant species and the percentage (x) of individual plants of each species infested with green stink bug from September 1996 to April 1998 on the Darling Downs. The dotted line above each bar chart indicates the main period when each plant species is mature, the dashed line indicates when each plant species was sampled, n is the mean ⫾ SE number of plants of each species sampled each sampling month, and p is the mean ⫾ SE number of discontinuous plant patches sampled each sampling month.

purpletop and clockweed. All stages of green stink bug were present in approximately equal proportions on all plants from February to April. During May and June, low numbers of adults and nymphs were supported on

horehound, which fruits throughout the year (Fig. 3a). By July, adults were the only stage recorded on horehound, and at low densities. No mating adults or egg masses were recorded from horehound over winter.

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FIG. 4. Mean ⫹ SE density of green stink bug egg masses on horehound and the percentage (x) of individual horehound plants infested with egg masses from September 1996 to April 1998 on the Darling Downs.

FIG. 6. Mean ⫹ SE density of horehound bug egg masses on horehound and the percentage (x) of individual plants infested with egg masses from September 1996 to April 1998 on the Darling Downs.

Spatial distribution within and across plant patches. Between spring 1996 and autumn 1997, green stink bug adults and nymphs were usually present on 20 – 40% of horehound plants sampled. During spring 1997 approximately 30% of horehound plants were infested, before this dropped dramatically in 1998 to less than 5% (Fig. 3a). On other plant species, a lower percentage of plants tended to be infested, with the exception of purpletop, which never had less than 20% of plants infested (Fig. 3f). The percentage of horehound plants with egg masses was usually less than 5%, although

this climbed to 30% in November 1997 (Fig. 4). Horehound was the only plant for which the distribution of green stink bug across patches could be quantified. Mean ⫾ SE densities across three horehound patches in October 1996 were 0.05 ⫾ 0.05, 0.79 ⫾ 0.21, and 5.21 ⫾ 3.04 bugs (adults and nymphs) per plant. Corresponding egg mass densities were 0 ⫾ 0, 0.25 ⫾ 0.11, and 0.86 ⫾ 0.43 egg masses per plant. Between 5 and 20% of plants in patches were infested with bugs and eggs. Mating frequency. Although most green stink bug adults (68%, n ⫽ 1083) were recorded from horehound, the percentage of adults that were mating when sampled was lowest on horehound and highest on variegated thistle, from which only 25 adults were recorded (G ⫽ 39.97, df ⫽ 4, P ⬍ 0.0001; Table 3). On glossy nightshade, mintweed, clockweed, and purpletop an intermediate mating frequency of approximately 10% was recorded. The percentage of green stink bug adults mating during each sampling month ranged from 0 to 35% (Table 4). No adults were recorded mating during September 1996, January–March 1997, May–July 1997, and January–February 1998. When pooled across seasons, there was no significant difference in the percentage of adults mating (G ⫽ 0.91, df ⫽ 2, P ⫽ 0.63). When pooled across season and year, the percentage mating was significantly higher during autumn 1998 than at any other time (G ⫽ 23.70, df ⫽ 5, P ⫽ 0.0002; Table 4).

FIG. 5. Mean ⫹ SE density of horehound bug adults and nymphs (instars 1–3 and 4 –5) on horehound and the percentage (x) of individual plants infested with horehound bug from September 1996 to April 1998 on the Darling Downs. The dotted line above the figure indicates the main period when horehound is mature, the dashed line indicates when plants were sampled, 131 ⫾ 12 (mean ⫾ SE) plants were sampled each sampling month, and 3.50 ⫾ 0.20 discontinuous horehound patches were sampled each sampling month.

Horehound Bug (Agonoscelis rutila) Temporal distribution on plant species. Horehound bug was recorded almost exclusively from horehound (Table 2). Whereas adults were present only at low

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gated. For example, in October 1996, mean ⫾ SE horehound bug densities in three horehound patches were 0 ⫾ 0, 1.06 ⫾ 0.60, and 2.79 ⫾ 1.75 bugs (adults and nymphs) per plant and 0 ⫾ 0, 0.23 ⫾ 0.07, and 0.79 ⫾ 0.39 egg masses per plant, respectively. The percentage of plants in horehound patches infested with horehound bug in October 1996 varied from 0 to 20%. Mating frequency. Horehound bug adults were recorded mating only on horehound and mintweed (Table 3). Adults were recorded mating on most sampling occasions, although little or no mating was recorded during winter. The percentage of adults recorded mating was significantly higher during spring and summer than autumn (G ⫽ 21.21, df ⫽ 3, P ⬍ 0.0001; Table 4), with the lowest mating frequency in autumn 1997 (G ⫽ 20.71, df ⫽ 6, P ⫽ 0.002). Other Species

FIG. 7. Mean ⫹ SE density of redbanded shield bug adults and nymphs (instars 1–3 and 4 –5) on different plant species and the percentage (x) of individual plants of each species infested with redbanded shield bug from September 1996 to April 1998 on the Darling Downs. The dotted line above each figure indicates the main period when each plant species is mature, the dashed line indicates when each plant species was sampled, n is the mean ⫾ SE number of plants of each species sampled each sampling month, and p is the mean ⫾ SE number of discontinuous plant patches sampled each sampling month.

densities (Fig. 5), egg masses were relatively abundant at all times of the year except during winter (Fig. 6). Very low densities of bugs and egg masses were occasionally found on mintweed (Table 2). Egg masses were recorded during all months between spring and autumn and were especially prevalent during October, January, and March (Fig. 6). At other times adults and nymphal instars 4 –5 predominated. During winter (June–August), the adult stage was the predominant one and they continued to oviposit, albeit rarely. Spatial distribution within and across plant patches. Between 10 and 20% of horehound plants were usually infested with horehound bug, although in 1998 up to 50% were infested (Figs. 5 and 6). The distribution of horehound bug across horehound patches was aggre-

Redbanded shield bug was recorded mainly during autumn when it was reproductively active on mungbean and soybean (Figs. 7 and 8, Tables 3 and 4). At other times of the year, this species was recorded only in low numbers, from lucerne, variegated thistle, hexham scent, and bokhara clover. Green potato bug was recorded predominantly from glossy nightshade (Figs. 9a and 10a), with low numbers of bugs also being collected from horehound (1996/1997 only; Figs. 9b and 10b) and blackberry nightshade. Green potato bug adults were recorded mating only on glossy nightshade, and only during October 1996 and November 1997. Egg masses of green potato bug were collected mainly during October and from January to April (Figs. 10a and 10b). Brown shield bug and ricespotting bug were present in low numbers on mungbean, soybean, mintweed, and horehound, and some egg masses

FIG. 8. Mean ⫹ SE density of redbanded shield bug egg masses on soybean and the percentage (x) of individual plants infested with egg masses from September 1996 to April 1998 on the Darling Downs.

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131

small area of southeastern Queensland, but this is justified by patterns of host plant availability and host plant use, at least by the green vegetable bug, being fairly constant across southeastern Queensland (Velasco et al., 1995). Hosts of T. basalis are spatially and temporally aggregated and this must affect the ecology of T. basalis and the subsequent degree of biological control. Below, the importance of temporal and spatial host availability to T. basalis is discussed in relation to biological control of the green vegetable bug. Temporal Availability of Hosts for Trissolcus basalis Hosts for T. basalis were most abundant during October and again between January and April (Figs. 2, 4, 6, 8, and 10). This may suggest that T. basalis is host limited at other times of the year, but egg masses of the three most commonly recorded species were collected during all months between September and April of 1996/1997 and/or 1997/1998. Although the preference

FIG. 9. Mean ⫹ SE density of green potato bug adults and nymphs (instars 1–3 and 4 –5) on different plant species and the percentage (x) of individual plants of each species infested with green potato bug from September 1996 to April 1998 on the Darling Downs. The dotted line above each figure indicates the main period when each plant species is mature, the dashed line indicates when each plant species was sampled, n is the mean ⫾ SE number of plants of each species sampled each sampling month, and and p is the mean ⫾ SE number of discontinuous plant patches sampled each sampling month.

of the former species were collected mainly from horehound in late spring–summer during 1997/1998 (Table 2). The predatory shield bugs O. schellenbergii and C. nasalis were only occasionally recorded. All stages of these two species were present on a number of plants, but mainly turnip-weed, lucerne, mungbean, and soybean. Low numbers of M. scutellaris and R. serripes were recorded from mungbean, soybean, and bird of paradise tree but no eggs were collected (Table 2). DISCUSSION

Host availability for T. basalis can be viewed with respect to time (temporal) and geographical space (spatial). The spatial scale covered here was restricted to a

FIG. 10. Mean ⫹ SE density of green potato bug egg masses on different plant species and the percentage (x) of individual plants of each species infested with egg masses from September 1996 to April 1998 on the Darling Downs.

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TABLE 3 Percentage of Adults of Five Bug Species Recorded Mating on Different Plant Species, from September 1996 to April 1998 on the Darling Downs a

Percentage mating

Plant species

GVB

GSB

HB

RSB

GPB

Turnip-weed Variegated thistle Glossy nightshade Horehound Buchan weed Hexham scent Bokhara clover Spear thistle Mintweed Clockweed Purpletop Mungbean Soybean Other species Grand total

28.0 (271)a 12.3 (179)b 11.8 (17) 0 (48)b 32.6 (178)a 0 (11) 34.0 (212)a 15.1 (278)b 15.6 (64)b 14.3 (56)b 0 (5) 36.7 (169)a 25.5 (251)a 1.9 (318) 20.5 (2057)

0 (2) 40 (25)a 9.0 (133)b 3.6 (732)c — — — 0 (21) 11.4 (35)b 14.0 (43)b 9.4 (85)b 0 (1) — 33.3 (6) 5.5 (1083)

— — — 14.3 (544) — — — — 31.6 (19) — — — — — 14.9 (563)

— 0 (14) — — — 28.6 (7) — — — — — 0 (10) 12.9 (31) 0 (8) 8.6 (70)

— 0 (2) 5.4 (148) 0 (2) — 0 (1) — — — — — — — 0 (12) 4.8 (165)

a Percentage mating ⫽ (number of males and females mating/total number of males and females) ⫻ 100. Numbers in parentheses ⫽ total number of males and females found. GVB, green vegetable bug; GSB, green stink bug; HB, horehound bug; RSB, redbanded shield bug; GPB, green potato bug. Column means followed by the same letter are not significantly different (G test, P ⬎ 0.05). Column means without a letter were not included in the statistical analysis because of low sample size (⬍25 adults).

and use of different host species by T. basalis is not known, the availability of a number of host species between spring and autumn suggests that T. basalis is not likely to experience a host shortage during summer in southeastern Queensland as hypothesized by Clarke and Walter (1993a). Their hypothesis was based on the results of Velasco et al. (1995), who suggested that the green vegetable bug is limited to two generations each year in southeastern Queensland as a result of host plants suitable for nymphal development and adult reproduction being unavailable, especially over summer. However, the green vegetable bug oviposits and develops on a number of plant species during summer, such as horehound, glossy nightshade, buchan weed, mintweed, and clockweed (Figs. 1 and 2, Table 3). These were not recorded by Velasco et al. (1995) in the localities that they sampled. The suitability of these newly discovered host plants of the green vegetable bug is not known. However, differences in bug abundances (Fig. 1), rates of oviposition (Fig. 2), and mating across plant species (Table 3) suggest that some of them are more suitable than others (see Velasco and Walter, 1992 on relative suitability of hosts). The green vegetable bug, green stink bug, and horehound bug appear to undergo at least three generations each year on the Darling Downs. In addition to the two generations of green vegetable bug identified by Velasco et al. (1995), there appears to be a generation in summer concentrated on horehound (Figs. 1d and 2d), glossy nightshade (Fig. 1e), mintweed (Figs. 1g and 2e), clockweed (Figs. 1i and 2g), and bokhara

clover (Figs. 1j and 2g). Two generations from late summer to autumn are also possible with mating and oviposition occurring between February and April on a number of summer weeds, mungbean, and soybean (Tables 3 and 4, Fig. 2). More intensive field surveys are required to confirm these results and provide more ecological data on the rarer bugs that host T. basalis, all of which are also likely to undergo at least three generations each year. The horehound bug differs from all the other host species of T. basalis in that it does not diapause during winter and is therefore the only known host species available to T. basalis during winter. Kelly (1987) showed that T. basalis parasitizes horehound bug eggs in winter and therefore does not appear to diapause. She stressed the importance of the availability of horehound bug eggs during winter as a reproductive refuge for T. basalis. However, the horehound bug oviposits only rarely in winter (Fig. 6), and as a result T. basalis is likely to experience a host shortage then. Whereas adult T. basalis survival rates are highest in winter in southeastern Queensland (Clarke and Walter, 1993a), the low parasitism rates achieved by T. basalis during early spring (Loch, 1999; Loch and Walter, 1999) suggest that populations of this parasitoid dwindle during winter as a result of a shortage of hosts. Because many T. basalis host species are phytophagous and dependent on plant availability, these hosts would be expected to be temporally scarce or unavailable during climatically unfavorable times. However, despite 1996/1997 being relatively “wet” in contrast to

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TABLE 4 Percentage of Adults of Five Bug Species Recorded Mating from September 1996 to April 1998, Grouped over All Plant Species on the Darling Downs Percentage mating (total adults) a Year

Month

GVB

GSB

HB

RSB

GPB

1996

Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr

21.1 (19) 37.5 (16) 1.1 (550) 29.7 (276) 28.6 (147) 41.9 (86) 14.6 (96) 2.9 (279) 0 (5) — — 100 (2) 34.9 (63) 15.7 (51) 45.2 (31) 25.0 (48) 46.9 (98) 31.0 (84) 33.6 (107) 58.6 (99)

0 (15) 16.7 (60) 7.1 (28) 14.6 (41) 0 (39) 0 (62) 0 (107) 6.7 (89) 0 (67) 0 (31) 0 (3) 26.7 (15) 3.3 (61) 4.5 (177) 5 (120) 8.1 (124) 0 (16) 0 (11) 35.3 (17) —

14.3 (14) 32.6 (43) 0 (20) 18.2 (33) 26.7 (30) 19.5 (41) 0 (15) 0 (15) 0 (24) 0 (17) 0 (3) 25.0 (8) 0 (10) 10.3 (58) 28.6 (35) 25.4 (71) 7.1 (28) 8.0 (25) 14.0 (43) 0 (30)

— — 0 (4) — — — 0 (1) 0 (1) — — — — 18.2 (11) 0 (14) — — — 0 (9) 0 (10) 20.0 (20)

— 17.6 (34) 0 (1) 0 (4) 0 (6) 0 (38) 0 (23) 0 (16) — — — — 0 (4) 0 (24) 15.4 (13) 0 (1) — 0 (1) — —

1997

1998

a Percentage mating ⫽ (number of males and females mating/total number of males and females) ⫻ 100. Numbers in parentheses ⫽ total number of males and females found. GVB, green vegetable bug; GSB, green stink bug; HB, horehound bug; RSB, redbanded shield bug; GPB, green potato bug.

the drought conditions during 1997/1998, the patterns of abundance, distribution, and host plant use of green vegetable bug and other phytophagous species on the Darling Downs remained much the same across these two climatically contrasting periods. Most plant species, except crops such as mungbean and soybean, were less abundant in 1997/1998 and this appears to have significantly affected populations of green vegetable bug, as seen in the dramatic decrease in the abundance and distribution of this species on most plant species in 1997/1998 (Fig. 1). However, other phytophagous bug species did not exhibit similar decreases (Figs. 3, 5, 7, and 9). Whether spear thistle is a regular host plant for green vegetable bug and green stink bug is dubious because both species were absent from spear thistle during 1997/1998 (Figs. 1h, 2h, and 3d). Similarly, the presence of over 200 green vegetable bug adults on only one roly-poly plant on one occasion casts doubt on whether roly-poly is a regular host plant and stresses the need to test suspected host plants experimentally for their suitability for insect development and reproduction. Spatial Availability of Hosts for Trissolcus basalis Hosts of T. basalis are spatially aggregated at a number of levels. At the level of an individual host,

eggs of most host species are laid in compact masses. Hosts are further aggregated within plants because most eggs are laid on the underside of leaves and on fruits and flowers (A. D. Loch, personal observation). Oviposition is concentrated mainly on host plants that are suitable for bug development, with species such as green vegetable bug ovipositing on many hosts (Fig. 2), whereas green potato bug (Fig. 8) and horehound bug (Fig. 10) oviposit on only a few plant species. Egg masses are also spatially aggregated within and across plant patches, with some plants and patches having a higher host density than others. The spatial distribution of hosts must affect T. basalis in terms of movement of individuals. This is likely to impact on the subsequent degree of biological control, but how or to what degree are unknown. Future research is needed to address the host-searching behavior of T. basalis in relation to the distribution of hosts. The findings presented in this paper are applicable to the Darling Downs and, although aspects may be applicable to other areas of Australia, the situation may be vastly different even in other areas of southeastern Queensland. For example, I have observed green vegetable bug nymphs feeding on glossy nightshade, castor oil, Ricinus communis L., and siratro, Macroptilium atropurpureum (DC.) Urban, during

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winter in Brisbane. I have also observed green potato bug adults mating and ovipositing and nymphs feeding on glossy nightshade in winter. Horehound bug has been observed feeding on blue billygoat weed, Ageratum haustonianum Miller, and cobbler’s pegs, Bidens pilosa L., in Brisbane throughout the year. These examples clearly illustrate that even small changes in climate and host plant availability could lead to significant differences in the ecology of parasitoid and host species, and this may impact on the ensuing degree of biological control of green vegetable bug. CONCLUSIONS

The wide host range of T. basalis coupled with the seasonal phenology of these different host species indicates that T. basalis is unlikely to be host limited during summer in southeastern Queensland. Instead, T. basalis is more likely to be host limited in winter when horehound bug is the only known host species available. In addition to being temporally aggregated, T. basalis hosts are spatially aggregated at a number of levels. Quantifying the magnitude to which T. basalis is affected by temporal and spatial patterns of host availability requires further research. To understand how the ecology of T. basalis is affected by these patterns of host availability, future research must investigate the host preference and use by T. basalis and how the spatial availability of hosts affects the behavior and ecology of T. basalis. Such research may also provide clues to improve biological control of the green vegetable bug. ACKNOWLEDGMENTS I thank Jessie Loch for her hospitality and help during field trips, the farmers who kindly allowed me access to their fields, Gimme Walter and Tony Clarke for their supervision of this study and critical comments on the manuscript, Shama Khan and Marc Coombs (CSIRO Entomology) for their unpublished data, and Helen Nahrung for her critical comments on the manuscript. This study was supported by a Grains Research and Development Corporation Junior Research Fellowship.

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