Host range and risk assessment of Zygogramma bicolorata,a defoliating agent released in South Africa for the biological control of Parthenium hysterophorus

Parthenium hysterophorus (parthenium) is a weed of international importance and is spreading rapidly in sub-Saharan Africa. Consequently, it has been targeted for biocontrol in South Africa since 2003. Based on precedents elsewhere in the world, the defoliating beetle Zygogramma bicolorata was prioritised as a candidate agent. Although no-choice tests, involving some 48 test plant species, indicated a significant preference for parthenium, significantly reduced feeding and oviposition was recorded on some species. Multiple-choice tests resolved many of these non-target results; however, Helianthus annuus (sunflower) was still selected for oviposition and feeding. Of the 12 sunflower cultivars tested, four were selected for oviposition, while two were selected for oviposition and feeding. These six cultivars were then subjected to larval development trials, together with three native and two weed species (in the Asteraceae). These trials showed high levels of complete development on parthenium, significantly reduced development on sunflower cultivars, and partial development on only one of the weed species. Finally, a risk assessment was conducted on the six sunflower cultivars to quantify Z. bicolorata feeding and reproductive performance. Feeding risk calculations revealed these cultivars to have an extremely low risk (<0.2%) of supporting Z. bicolorata feeding and development. Similarly, reproductive risk calculations showed a very low risk (<0.16%) of supporting viable Z. bicolorata populations. These data are supported by findings from both the native (Mexico) and introduced ranges (Australia, India) of Z. bicolorata, where it has never been recorded as a pest of sunflower. These considerations were accepted by the regulatory authorities and in August 2013, Z. bicolorata became the second insect agent to be released in South Africa for the biocontrol of parthenium.     

Post introductory risk assessment studies on Zygogramma bicolorata (Coleoptera: Chrysomelidae), a classical biological control agent of Parthenium hysterophorus (Asteraceae) in India

Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae), a biological control agent of Parthenium hysterophorus L. (Asteraceae), was feeding on leaves of Helianthus annuus in India, raising concerns of its host range. Based on the age grading technique, it was shown that the majority of Z. bicolorata on sunflower plants at any time were reproductively immature. This establishes that Z. bicolorata does not pose any risk to sunflower in India.     

Pre-release evaluation of absolute spillover impact risk of Physonota maculiventris (Chrysomelidae: Cassidinae) on non-target plant species Helianthus annuus (Asteraceae) and Zea mays (Poaceae) in South Africa

The tortoise beetle, Physonota maculiventris (Coleoptera: Chrysomelidae), a candidate biological control agent of Tithonia diversifolia (Hemsl.) A. Gray (Asteraceae) was screened for spillover risks on non-target plant species in South Africa. Studies were conducted to measure the absolute feeding damage and reproductive performance of P. maculiventris on non-target plant species, Helianthus annuus L. (Asteraceae) and Zea mays L. (Poaceae). The influence of spillover on generational build-up performance on the non-target plant species was also investigated. Adult female beetles were switched from T. diversifolia at 14 (actively feeding colony) or 24 (gravid colony) days to the non-target species. Likewise, as a backup or control, female beetles were exposed to H. annuus in a no-choice situation and switched to T. diversifolia and Z. mays. Feeding damage, adult longevity and egg production of P. maculiventris were significantly lower on H. annuus, compared to those metrics on T. diversifolia. Gravid P. maculiventris adults switched from T. diversifolia on the 14th day after emergence laid a few egg batches on the leaf surfaces of Z. mays, but no signs of feeding were observed. Furthermore, the population of P. maculiventris significantly increased by 11.7 fold (26.8–312.5 adults) between the first (F1) and second (F2) generations on T. diversifolia, while on the non-target, H. annuus, it decreased from 6.3 to zero (0). The study concludes that P. maculiventris will sustain its populations entirely on the target, T. diversifolia population stands associated with or without H. annuus and Z. mays cultivations at different scales in South Africa.     

Complementing biological control with plant suppression: Implications for improved management of parthenium weed (Parthenium hysterophorus L.)

Parthenium hysterophorus L. is a weed of global significance that has become a major weed in Australia and many other parts of the world. A combined approach for the management of parthenium weed using biological control and plant suppression, was tested under field conditions over a two-year period in southern central Queensland. The six suppressive plant species, selected for their demonstrably suppressive ability in earlier glasshouse studies, worked synergistically with the biological control agents (Epiblema strenuana Walker, Zygogramma bicolorata Pallister, Listronotus setosipennis Hustache and Puccinia abrupta var. partheniicola) present in the field to reduce the growth (above ground biomass) of parthenium weed, by between 60–86% and 47–91%, in Years 1 and 2, respectively. The biomass of the suppressive plants was between 6% and 23% greater when biological control agents were present than when the biological control agents had been excluded. This shows that parthenium weed can be more effectively managed by combining the current biological control management strategy with selected sown suppressive plant species, both in Australia and elsewhere.     

Stage specific feeding attributes and mobilization of nutrients in Mexican beetle,Zygogramma bicolorata Pallister on Parthenium hysterophorus L.

Parthenium hysterophorus L. (Asteraceae) is a toxic weed of agricultural farms, pastures and wastelands with a pan-tropical distribution. The weed causes a reduction in crop production of agricultural fields and severe health problems in humans. The Mexican beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae) is among the most promising candidates for the weed biocontrol. However, no previous study has evaluated assimilation of nutrients in this beetle. In the present study, feeding attributes and assimilation of nutrients by larvae of Z. bicolorata were assessed on the weed. Results revealed that the first larval instars of Z. bicolorata exhibited lowest consumption rates, and accumulated minimum concentrations of glucose, proteins and triglycerides in their body. They showed compensatory feeding, and displayed highest food utilization efficiencies and developmental rates. In contrast, the fourth larval instars exhibited higher food consumption rates and conversion efficiencies, but displayed lowest developmental rates. Accumulation of food reserves was also recorded maximum for the fourth larval instars. Overall, the findings may aid current mass-rearing efforts for Z. bicolorata in laboratories, but field trials are still needed to strengthen the present findings.     

Impact of defoliation by the biocontrol agentZygogramma bicolorataon the weed Partheniumhysterophorus in Australia

The leaf-feeding beetle Zygogrammabicolorata Pallister was introduced from Mexico intoAustralia in 1980 as a biocontrol agent for the weedParthenium hysterophorus L. (Asteraceae). Z. bicolorata became abundant in 1990, and since 1992there has been regular outbreaks resulting in thedefoliation of the weed in central Queensland. In thisstudy we evaluated the impact of defoliation by Z. bicolorata on P. hysterophorus from 1996 to1998. Z. bicolorata caused 91–100% defoliationresulting in reductions in weed density by 32–93%,plant height by 18–65%, plant biomass by 55–89%,flower production by 75–100%, soil seed-bank by13–86% and seedling emergence in the following seasonby 73–90%. At sites with continued outbreaks ofZ. bicolorata, it is expected that the existing soilseed-bank will be minimised, resulting in reduceddensity of parthenium in 6 to 7 years.     

Rearing the Mexican beetle Zygogramma bicolorata (Chrysomelidae: Coleoptera) on a semi-synthetic diet

A semi-synthetic diet utilising parthenium leaf powder was evaluated for rearing the Mexican beetle Zygogramma bicolorata Pallister under in vitro conditions at 26±1°C, 65% RH. Significant differences were observed in the biological parameters of the beetle viz., the grub survival (54.3%), pupation (47.2%), fecundity (54.6/day) and total developmental period (37.7 days), when reared on the semi-synthetic diet compared to those when reared on natural parthenium leaves (91.5, 85.5, 74.8 and 29.8, respectively). The feasibility of utilising the semi-synthetic diet for mass production of the beetle is discussed.     

Pollen beetle (Meligethes aeneus) oviposition and feeding preference on different host plant species

The oviposition and feeding preferences of the pollen beetle, Meligethes aeneus, were determined in choice and no-choice tests in field, semi-field and greenhouse trials. Plant species used were Brassica napus, B. campestris, B. juncea, B. nigra, B. carinata, Sinapis alba and Crambe abyssinica. With respect to number of eggs laid, S. alba and C. abyssinica were inferior to the other species. Pollen beetles laid fewer eggs on B. nigra than on the other Brassica spp. in no-choice tests, however this difference was partly due to fewer eggs laid per bud rather than fewer buds used for oviposition. Most eggs, for all plant species, were deposited in buds sized 2–3 mm. Feeding damage on all plant species was relatively similar. Pollen beetles seem to have a wider host range for feeding than for oviposition. There was good agreement in plant species ranking as oviposition hosts between the field, semi-field and greenhouse trials.     

Temperature and altitude modulate feeding attributes of Mexican beetle,Zygogramma bicolorata Pallister on Parthenium hysterophorus

Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae) is an effective biocontrol agent of Parthenium hysterophorus L. which is an alien invasive herbaceous weed with a pan-tropical distribution. The present study aimed to assess the effects of temperature and altitude on feeding attributes (consumption rate, conversion efficiency and growth rate) of adults from the wild populations of Z. bicolorata inhabiting India and Nepal. Results revealed that adults inhabiting areas of low temperature (24°C ‒ 25°C) and high altitude (415 m ‒1400 m) were large and had higher food consumption rates. In contrast, those inhabiting areas of high temperature (34°C ‒ 36°C) and low altitude (81 m ‒ 229 m) were smaller and had higher food utilization efficiencies. In all the eco-climatic regions, females were larger than males and had higher feeding attributes than their counterparts. Temperature between 27°C and 30°C was found optimal for Z. bicolorata adults to convert and utilize the food biomass to body mass. Above the optimal temperature the feeding attributes decreased. Present results suggest that there exists a possibility for decrease in body size, and thereby weed biocontrol efficiency of Z. bicolorata adults with an increase in temperature due to global climate change.     

Benefits of polyandry in Parthenium beetle,Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae)

The influence of polyandry on the reproductive performance of females and on offspring fitness in Zygogramma bicolorata Pallister was investigated using four experimental treatments, viz. (A) monandrous, limited mating, (B) monandrous, unlimited mating, (C) polyandrous, no-choice limited mating, and (D) polyandrous, mate choice unlimited mating. Polyandrous females had higher reproductive performance than monandrous ones. Monandrous females subjected to unlimited matings had higher egg viability than those subjected to limited matings, but fecundity did not differ significantly. In polyandrous females, the freedom to choose mates did not affect reproductive performance. However, offspring of polyandrous females allowed mate choice developed fastest and had the highest survival at 25, 27, and 30 °C. Thus, polyandry in Z. bicolorata appears to provide both direct (material) and indirect (genetic) benefits resulting in better reproductive performance and increased adaptability of the offspring to counter environmental stresses. The present study not only adds to the knowledge of reproductive biology of Z. bicolorata but it could also be of economic value as it may help in the mass rearing of Z. bicolorata and in the management of Parthenium hysterophorus.     

Biology and host range of Mada polluta,a potential biological control agent of Tecoma stans in South Africa

The host range of Mada polluta Mulsant (Coleoptera:Coccinnellidae) was studied to assess its suitability as a biological control agent of Tecoma stans (L.) Juss ex Kunth var stans (Bignoniaceae), an invasive weed in South Africa. Biology of M. polluta and its host range were determined in the laboratory using no-choice and multi-choice feeding, oviposition and larval survival tests. Out of 36 plant species from 12 plant families (Bignoniaceae, Acanthaceae, Asteraceae, Verbenaceae, Lamiaceae, Oleaceae, Cucurbitaceae, Fabaceae, Scrophulariaceae, Solanaceae, Apiaceae, Chenopodiaceae and Poaceae) within the order Lamiales that were tested during the host specificity testing, M. polluta showed a very strong preference for T. stans, depositing its eggs on T. stans and none on non-target plant species. In no-choice tests, an average of 246 eggs was laid on T. stans, and from these, 133 larvae developed to adulthood. The beetle also showed very promising biological attributes that will contribute to its success as a biological control agent of T. stans. These attributes include highly damaging larvae and adults, high fecundity (532 eggs/female) and a short life cycle (four weeks). The short life cycle will enable multiple generations per year and rapid population increase in the field. It is concluded that M. polluta is sufficiently host-specific to be released against T. stans in South Africa. It is, therefore, strongly recommended that permission be granted to release this beetle from quarantine for biological control of T. stans in South Africa.     

Does parasitoid state affect host range expression?

The pre-release risk assessment of parasitoids for classical biological control generally involves non-target testing to define the agent’s host range. To ensure that no suitable host species are falsely rejected in these tests, it has been suggested that the physiological and informational state of parasitoids be manipulated to enhance their “motivation to oviposit”. However, the effects of such factors on host acceptance are not consistent across parasitoid species, making it laborious to identify the conditions necessary to maximise host acceptance. Our objective was to determine whether changes in parasitoid state could alter host acceptance behaviour sufficiently to affect host range expression. In addition, we tested the assumption that a state-dependent shift in motivation to oviposit on the target host will translate to a similar change in responsiveness to lower-ranked host species. Three-day-old and 10-day-old females of the candidate classical biological control agent, Diadromus pulchellus, were offered 12 non-target species of varying relatedness to the target pest, Acrolepiopsis assectella, in a series of no-choice and choice oviposition trials. Younger D. pulchellus females had previously demonstrated greater motivation to oviposit in the target pest and were, therefore, predicted to express a broader host range than older females. Parasitoid age had a minor effect on host range expression that was contrary to expectations. Older females more readily attacked one of the non-target species in no-choice tests and inflicted higher mortality in one of the choice tests. Ultimately however, young and old parasitoids still attacked the same four non-target species and their offspring emerged from the same three. There was an interaction between the effects of parasitoid condition and experimental design on responsiveness to low-ranked hosts: increasing non-target density in choice tests significantly altered attack rates by 10-day-old, but not by 3-day-old, parasitoids. The implications of these findings for host specificity testing depend largely on the specific aims of a host range assessment. Parasitoid state influenced the frequency of non-target attack but did not affect which non-target species were attacked.     

Semiochemical footprints of the predaceous coccinellid beetle,Menochilus sexmaculatus,deter Zygogramma bicolorata (Coleoptera: Chrysomelidae) from feeding on Parthenium

Present study assessed if semiochemical cues left by an aphidophagous beetle, M. sexmaculatus influenced foraging behaviour of a phytophagous beetle, Z. bicolorata on noxious weed, P. hysterophorus. The lower predation attributes of Z. bicolorata in presence of M. sexmaculatus semiochemical footprints confirms they interfere with weed biological control.     

Does Zygogramma bicolorata Pallister really affects the growth,density and reproductive performance of Parthenium hysterophorus L?

Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae) is a satisfactory potential candidate for controlling Parthenium hysterophorus L. The study was conducted in order to evaluate the bio-control potential of Z. bicolorata to satisfactory reduced the density of parthenium weed in natural field conditions. Therefore, beetles were released in the twelve study sites @ 12 adults and/or larvae/m² in their respective sites on 5th, 10th, 15th and 20th day after initial field releases. Observations were made on defoliation by the beetle, perthenium plant height, plant biomass, leaf injury rating and soil seed reservoir. Present study showed that field releases of Z. bicolorata considerably lowering down the parthenium density at all treated sites. At larval release sites by the 60th day of observation a complete defoliation was noted, however at adult release sites it took 80 days for complete defoliation. Moreover, significantly higher number of developmental stages i.e. eggs, larvae and adults were noted in the adults released sites than to larval released sites and the controls. It was also noted that plant height and its density, flowers & leaves production, biomass of parthenium plant and seed reservoir in soil was negatively affected in treated sites as compared to untreated sites. Thus, we have concluded that adults can be utilized in biocontrol program because population build-up was greater in those sites where adults were released.     

Time-dependent Changes in the Host-acceptance Threshold of Insects: Implications for Host Specificity Testing of Candidate Biological Control Agents

Commonly, insects show a progressive decrease in acceptance threshold to sensory cues associated with food or oviposition sites when they are deprived of the opportunity to feed or oviposit. Such changes have been termed time-dependent. In biological control, candidate agents are tested in a variety of cage assays in order to determine the limits of their host range. These assays commonly include choice tests including the target species, simultaneous no-choice tests, and sequential no-choice tests. We consider the possible influence of time-dependent changes in acceptance threshold on the likely outcomes of each of these kinds of tests. Results that may under-estimate the field host range of candidate agents are deemed to be most likely from choice tests that include a highly ranked host, and any no-choice assay conducted over a short period. We recommend: (i) that choice tests including the target species and sequential no-choice tests with a short period of access to non-target species, should not be employed as the only type of test, or for any initial screening; and (ii) that more attention be paid to the temporal profiles of feeding and oviposition by the candidate agent, especially in no-choice tests.     

Risk assessment of Episimus unguiculus (Lepidoptera: Tortricidae), a biological control agent of Schinus terebinthifolia (Sapindales: Anacardiaceae) in Hawaii,USA

Schinus terebinthifolia Raddi (Anacardiaceae) is an introduced ornamental tree from South America that has become one of the most invasive weeds in Hawaii and Florida, USA. Exploratory surveys in the plant’s native range from 1950 to 2014 identified several potential biological control agents. One of these is the leaflet rolling moth Episimus unguiculus Clarke (Lepidoptera: Tortricidae), previously known as Episimus utilis Zimmerman. This biological control agent was released in Hawaii in the 1950s where high densities were occasionally observed, leading to partial control of S. terebinthifolia by the 1960s. Larvae are leaf tiers capable of completely defoliating small plants. In order to investigate the release of E. unguiculus in the continental USA, a series of laboratory no- choice, and multiple-choice tests were conducted in Florida, and a preliminary open field test with a native plant in Hawaii. Under the confined laboratory conditions imposed during the no-choice tests, E. unguiculus accepted the economically important Pistacia spp. and several other non-target plants for oviposition and development. However, in the multiple-choice tests E. unguiculus exhibited a clear preference for S. terebinthifolia relative to non-target plants accepted in the no-choice tests. Overall, the results of field observations during surveys in South America and Hawaii and host range studies completed in Hawaii and Florida showed that E. unguiculus is a narrow specialist on S. terebinthifolia, its natural host plant.     

Biology and host specificity of Rhinusa pilosa,a recommended biological control agent of Linaria vulgaris

Linaria vulgaris Mill. (Plantaginaceae), common or yellow toadflax, is a Eurasian short-lived perennial forb invasive throughout temperate North America. Rhinusa pilosa (Gyllenhal) (Coleoptera, Curculionidae) is a univoltine shoot-galling weevil found exclusively on L. vulgaris in Europe. Under no-choice test conditions, 13 non-native Linaria species exposed to R. pilosa were accepted for oviposition and most were found to be suitable, to varying degrees, for gall and larval development. Adult feeding and survival was minimal on native North American species in the plant tribe Antirrhineae which includes the target plant. In no-choice tests with 63 native North American species and 24 other non-target species outside Linaria, oviposition was limited to four native North American species. Only three larvae developed to the adult stage on Sairocarpus virga (A. Gray) D.A. Sutton, with no negative impact on plant growth. Risks to native flora from the release of R. pilosa are therefore expected to be minimal. The Technical Advisory Group for the Biological Control of Weeds (TAG—BCW) has recommended release of R. pilosa in September 2013.     

The double life cycle of Lepidapion argentatum,a promising candidate for the biological control of French Broom.

Lepidapion argentatum (Gerstaecker) (Brentidae) is a weevil from the Mediterranean region collected and recorded from French broom (Genista monspessulana) (L.) LAS Johnson (Fabaceae), a major invasive plant in the USA. We studied feeding and oviposition of L. argentatum under laboratory conditions. Overwintering adults can oviposit in either seed-pods or stem tips of French broom. Larvae in seed-pods consume seeds whereas those in stems develop inside a gall. The development time of L. argentatum in stem galls ranged from 34 to 40 days at mean 23.67?±?2.43°C. The double ability of L. argentatum to develop in stems and pods appears not to have been recorded in Coleoptera and rare in other phytophagous insects. Our finding increases its potential value as a biocontrol agent against French broom.     

Activity enhancement of Zygogramma bicolorata,a biocontrol agent of Parthenium hysterophorus,by temperature regulated diapause aversion

Diapause is a unique strategy of dormancy in insects to avoid unfavourable conditions. The exotic beetle Zygogramma bicolorata, is an effective biological control agent of Parthenium hysterophorus in India, Adults diapause in soil during December to May. As a result, there is delay in its effectiveness on the plant that reaches to flowering and seed production by the time the beetle is able to build up its population after emerging from diapause. Therefore, a study was conducted to explore possibilities of diapause aversion by temperature regulation. Results indicated that exposure of newly emerged adults to heat treatment of 35°C and to low temperature of 10°C could reduce diapause in Z. bicolorata. The low temperature can also be used as a medium for the storage of the mass reared beetles for a long time without having negative effect on their longevity and fecundity.     

Host specificity of Argopistes tsekooni (Coleoptera: Chrysomelidae), a potential biological control agent of Chinese privet

Chinese privet, Ligustrum sinense Lour., is a perennial semi-evergreen shrub that is a serious invasive weed in the United States. Classical biological control offers the best hope for controlling it in an economic, effective, and persistent way. Host specificity of one of the most promising biological control agents of Chinese privet, a flea beetle, Argopistes tsekooni Chen (Coleoptera: Chrysomelidae), was evaluated in China by using laboratory no-choice and choice tests on 13 species of Oleaceae and eight species in other families that have important economic value. In adult no-choice survival and oviposition tests, the flea beetle fed and survived for 30 d on Syringa oblata Lindl., Jasminum nudiflorum Lindl., and three species in the genus Ligustrum. Females also oviposited on these species, but only larvae from eggs laid on S. oblata and Ligustrum spp. developed successfully. In addition, the beetles did not feed or oviposit on the species of economic importance. In choice tests, adults preferred L. sinense for feeding and oviposition. These results show that A. tsekooni is relatively host specific and warrants further testing as a biocontrol agent of Chinese privet in the United States.