Parasitoid Gonatocerus Ashmeadi Research Articles

Feeding and Development of the Glassy-Winged Sharpshooter, Homalodisca vitripennis, on Australian Native Plant Species and Implications for Australian Biosecurity

In any insect invasion the presence or absence of suitable food and oviposition hosts in the invaded range is a key factor determining establishment success. The glassy-winged sharpshooter, Homalodisca vitripennis, is an important insect vector of the xylem-limited bacterial plant pathogen, Xylella fastidiosa, which causes disease in numerous host plants including food and feedstock crops, ornamentals and weeds. Both the pathogen and the vector are native to the Americas and are considered to be highly invasive. Neither has been detected in Australia. Twelve Australian native plant species present in the USA were observed over two years for suitability as H. vitripennis feeding, oviposition and nymph development hosts. Hosts providing evidence of adult or nymph presence were Leptospermum laevigatum, Acacia cowleana, Eremophila divaricata, Eucalyptus wandoo, Hakea laurina, Melaleuca laterita and Swainsona galegifolia. An oviposition-suitability field study was conducted with citrus, a favoured oviposition host, as a positive control. Citrus and L. laevigatum, A. cowleana, B. ericifolia×B. spinulosa, C. pulchella, E. divaricata, E. wandoo, H. laurina, and S. galegifolia were found to be oviposition hosts. Egg parasitism by the mymarid parasitoid Gonatocerus ashmeadi was observed on all Australian plants. A number of Australian plants that may facilitate H. vitripennis invasion have been identified and categorised as ‘high risk’ due to their ability to support all three life stages (egg, nymph and adult) of the insect in the field (L. laevigatum, A. cowleana, E. divaricata, H. laurina, and S. galegifolia). The implications of these host status and natural enemy research findings are discussed and placed in an Australian invasion context.

Predicting the distribution of Gonatocerus ashmeadi, an egg parasitoid of glassy winged sharpshooter, in New Zealand

The mymarid egg parasitoid Gonatocerus ashmeadi is a potential candidate for classical biological control of glassy winged sharpshooter (GWSS; Homalodisca vitripennis), should the pest arrive in New Zealand. However, the climate in the parasitoid's native range in the southern USA is considerably warmer than that in New Zealand, which may pose an obstacle to establishment. Although G. ashmeadi is a very effective biocontrol agent in Florida, Hawaii and Western Polynesia, it appears currently to be limited by cooler climate in central and northern California – regions that typically have climates more similar to those in New Zealand. A CLIMEX model was used to predict the survival of G. ashmeadi in New Zealand by comparison with known parameters in the USA and western Pacific Islands. The model indicates that the establishment and distribution of G. ashmeadi is likely to be limited by the climate in New Zealand, although it will probably persist in warmer parts of the North Island. These predictions indicate that biocontrol of GWSS in New Zealand using G. ashmeadi will also require active management through varying regional integrated pest management programmes. Should GWSS arrive in New Zealand, G. ashmeadi should be selected from a population that has adapted to cooler parts of California. However, such a population is not known at present, so preventing GWSS from establishing in New Zealand remains a crucial strategy.

Evolution and biological control

Opinions about the value of biological control are often extreme. Colloquially, biological control most often refers to classical biological control, in which one species is introduced from another region to control pests such as arthropod herbivores in agricultural systems, or weeds in managed and natural systems.1 As such, biological control has the potential to be a low-cost, chemical free, means to control pests. Numerous biological control programs have been unqualified successes (Bellows 2001), such as the control of cacti in Australia with the moth Cactoblastis cactorum (Raghu and Walton 2007), of cottony-cushion scale (Icerya purchasi) in California with the vedalia lady beetle, Rodolia cardinalis (Caltagirone and Doutt 1989), and of glassy-winged sharpshooters in French Polynesia with the egg parasitoid Gonatocerus ashmeadi (Grandgirard et al. 2009). Yet, classical biological control, as with any introduction of a species into a new area, necessarily involves the unknown and therefore carries some inherent risk (Simberloff and Stiling 1996) – what will these organisms actually do in a novel ecosystem? The most unpredictable element in biological control is the extent to which the realized niche is modified in the new environment. This effect has been responsible for some disastrous outcomes of classical biological control, many of which occurred during an era when vertebrates were being introduced around the world by Europeans for a variety of reasons (e.g., introducing the birds of Shakespeare to America, Mirsky 2008), including for biological control (Howarth 1991). The introductions as biological control agents of cane toad to Australia (Crossland et al. 2000) and mongoose to Hawaii (Hays and Conant 2007) are notorious. Introductions of generalist invertebrate agents also have had dire consequences, such as the introduction of predatory snails to French Polynesia (Murray et al. 1988; Coote 2007). In retrospect, some of the unintended consequences of biological control could have been avoided with more ecological knowledge (McEvoy and Coombs 2000) or more societal appreciation for native species (which has developed with time, Henneman and Memmott 2001), but with other introductions, it would have been impossible to know ahead of time what the risks would be (e.g., gall fly agents of knapweeds providing supplementary food to mice that harbor hantavirus, Pearson and Callaway 2006). Many of the unknown outcomes of biological control are purely ecological – what is the risk that a wasp, introduced to parasitize an agricultural pest, will also be able to feed on a native insect? Other unknowns involve evolution – will a herbivore adapt over time to be able to feed on a new nontarget host or hybridize with a closely related species? This volume explores the evolutionary aspects of biological control. Although often overlooked, evolutionary considerations are critical to all stages of classical biological control, from agent selection, to quarantine, release, establishment, and ultimately success in pest control (Ehler et al. 2004). Many questions are unresolved. For example, should agents be chosen that have a long history with the host or are ‘new associations’ more likely to succeed (Hokkanen and Pimentel 1989)? Can one improve effectiveness through artificial selection (Hopper et al. 1993)? Will postcolonization adaptation of the agent increase the likelihood of success, and/or are hosts equally likely to evolve resistance over time (Roderick 1992; Holt and Hochberg 1997; Hufbauer 2001)? Are generalist consumers more likely to survive in novel environments or are specialists more effective (Murdoch et al. 1985; Waage 1990; Brodeur 2012)? More recently, concern for the environment, as well as theory examining the reasons for success of generalist predators, prompted a shift to the release of specialized consumers typically preceded by extensive testing aimed at delimiting the host range of candidate biological control agents. While this approach has clearly made biological control more predictive ecologically, research focused on host range currently lacks measures of genetic variation in host use and responses of those hosts, and thus evolutionary uncertainties remain.

Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia

Invasive species are generally detected in new ecosystems long after their first arrival, making it difficult to elucidate pathways leading to successful invasion. In this study, the dispersal of a classical biological control agent, the mymarid egg parasitoid Gonatocerus ashmeadi, was monitored across ten islands in three major island groups in French Polynesia from the exact moment of its introduction into Tahiti to combat the invasive pest Homalodiscavitripennis. Within 10 months, the parasitoid spread quickly from Tahiti to widely separated islands (up to 1,400 km from Tahiti); presumably through the transportation of plant material containing parasitized H. vitripennis eggs. Gonatocerus ashmeadi thus functioned as a “biomarker”, providing an informal audit of the effectiveness of inter-island quarantine measures designed to curb the accidental spread of noxious organisms. Survey results suggest that invasive organisms, like deliberately released biological control agents, can be unintentionally and rapidly transmitted across vast distances by humans. Furthermore, even remote islands appear to experience relentless pressure from invasive propagules associated with human travel. Implications of survey work documenting the spread and impact of G. ashmeadi are discussed within the context of biological control programs, non-target impacts, and biosecurity initiatives.

Classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in the Society, Marquesas and Austral archipelagos of French Polynesia

The glassy-winged sharpshooter, Homalodisca vitripennis (Germar) (= H. coagulata [Say]) (Hemiptera: Cicadellidae), was a major exotic pest in French Polynesia until a classical biological control program against this pest was conducted using the host-specific egg parasitoid Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). After risk assessment studies indicated an acceptably low potential threat to non-target species, parasitoids were released on Tahiti in May 2005. One year after release, populations of H. vitripennis had decreased by more than 90% in Tahiti and nearby Moorea. Here we present results of impact studies obtained during the second post-release year for G. ashmeadi in Tahiti and Moorea; we also report for the first time on results for eight other H. vitripennis infested islands located in three different archipelagos (Society, Marquesas, and Austral) of French Polynesia. On all infested islands across the three archipelagos, arrival of G. ashmeadi slashed H. vitripennis densities by more than 95%. In Tahiti and Moorea, H. vitripennis populations were maintained at very low densities during the second post-release year. Seasonal fluctuations of H. vitripennis abundance were observed in Tahiti with pest populations being more abundant during the cooler dry season than during the warmer wet season because of lower parasitism rates. Hence, similar seasonal fluctuations of H. vitripennis abundance are expected across all infested archipelagos in French Polynesia.

Short-distance dispersal behavior and establishment of the parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae) in Tahiti: Implications for its use as a biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae)

The egg parasitoid Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae), was introduced into French Polynesia as a biological control agent to control the invasive plant feeding pest Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). The short-distance dispersal of G. ashmeadi was monitored as part of the biological control program. G. ashmeadi showed exponential dispersal capacity with 47 m/day being a minimum estimate of its natural rate of spread at high host densities (>150 nymphs per minute of sweep net sampling) in urbanized areas at sea level, which were characterized by a high diversity of exotic ornamental plants. This rate of spread contrasted starkly with almost nonexistent establishment and dispersal where host densities were very low (<2 nymphs per minute of sweep net sampling) at high elevation (800 m) with relatively undisturbed native vegetation. Survey results across different altitudes revealed an effect of vegetative diversity and host density on the measurable mobility and establishment of G. ashmeadi. In contrast, no significant influence of wind direction was found on G. ashmeadi dispersal rate or direction. Survey results for G. ashmeadi from French Polynesia suggest that the best release establishment strategies for classical biological control of H. vitripennis are: (1) many small releases where host density is high, or (2) larger and fewer releases where host densities are low.

Pre-introductory risk assessment studies of Gonatocerus ashmeadi (Hymenoptera: Mymaridae) for use as a classical biological control agent against Homalodisca vitripennis (Hemiptera: Cicadellidae) in the Society Islands of French Polynesia

Homalodisca vitripennis (Germar) (=H. coagulata [Say]) (Hemiptera: Cicadellidae) invaded French Polynesia in 1999. A classical biological control program against H. vitripennis was initiated in 2004 aiming to introduce the exotic egg parasitoid Gonatocerus ashmeadi (Girault) (Hymenoptera: Mymaridae) to the Society Islands archipelago. Prior to any release, two risks were assessed: (a) continued uncontrolled H. vitripennis spread and proliferation in French Polynesia, and (b) non-target impacts by G. ashmeadi on indigenous French Polynesian cicadellids. The primary risk of H. vitripennis is its potential to vector the lethal plant bacterium, Xylella fastidiosa. While the presence of X. fastidiosa in French Polynesia has not yet been demonstrated, the presence of uncontrolled H. vitripennis greatly elevates the risk of a disease outbreak and thus represents a major threat for numerous plant species. Assessing the risk of G. ashmeadi introduction for native cicadellids first required an inventory of the Cicadellidae of the Society Islands, resulting in at least 14 cicadellid species (nine not previously recorded). The risk to these species of attack by G. ashmeadi was assessed using four criteria: (1) their phylogenetic relationships to known hosts of G. ashmeadi, and their similarity in (2) body size, (3) egg laying biology, and (4) ecology. All indigenous cicadellid species found were considered to be at low risk of attack because they differed greatly from all known hosts for G. ashmeadi: (1) none of the indigenous species are in the tribe Proconiini, (2) all were very small and, when possible to determine, (3) lay tiny single eggs, which (4) are deposited on the undersides of leaves of trees. These results persuaded the French Polynesian Government that the benefits of establishing G. ashmeadi for H. vitripennis control outweighed the serious potential risks associated with either delaying release or not releasing G. ashmeadi in French Polynesia. Releases of G. ashmeadi in Tahiti began in May 2005.

First records of Gonatocerus dolichocerus Ashmead, Palaeoneura sp., Anagrus sp. (Hymenoptera: Mymaridae), and Centrodora sp. (Hymenoptera: Aphelinidae) in French Polynesia, with notes on egg parasitism of the glassy-winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae)

The glassy-winged sharpshooter, Homalodisca vitripennis (Germar) [= H. coagulata (Say)] (Hemiptera: Cicadellidae: Proconiini), invaded Tahiti in 1999 and at the time of writing this pest was widespread in French Polynesia being extremely abundant in Tahiti and Moorea. Homalodisca vitripennis is a major threat for agriculture and biodiversity. In 2004, a classical biological control program against H. vitripennis was initiated with the goal of introducing and establishing the exotic egg parasitoid Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae) in French Polynesia. As part of the preliminary studies for this program, a survey was conducted of existing natural enemies, in particular egg parasitoids of H. vitripennis. Pan trap surveys and monitoring parasitism of H. vitripennis egg masses was performed in Tahiti. The results of the pan trap surveys provide the first record of the presence of Gonatocerus dolichocerus Ashmead (Hymenoptera: Mymaridae) in French Polynesia, but surveys of H. vitripennis egg...

Progeny Quality of &lt;I&gt;Gonatocerus ashmeadi&lt;/I&gt; (Hymenoptera: Mymaridae) Reared on Stored Eggs of &lt;I&gt;Homalodisca coagulata&lt;/I&gt; (Hemiptera: Cicadellidae)

This study assessed the effects of refrigerated storage on the suitability of eggs of the glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae), as hosts for propagation of the parasitoid Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). Development of the host eggs was terminated by chilling at 2 degrees C for 5 d before storage was initiated at 10 degresC for up to 70 d. Parasitism, adult emergence rate, developmental time, and sex ratio were used to gauge the suitability of the eggs as hosts after storage. In addition to these measures, demographic growth parameters also were used to assess the quality of the wasp progeny through the F2 generation. Host eggs stored 20 d remained fully acceptable to the wasps for attack. Although the parasitism rate decreased with storage time, > 80% adult parasitoid emergence was realized from eggs stored 30 d. After 70 d storage, adult emergence rate was decreased by 48%, fecundity decreased by 53%, female production by 19%, developmental time was extended 3 d, and female longevity was shortened 5 d. The emergence pattern of F1 but not F2 adults varied with storage time of the parental and grandparental hosts, respectively. For the F1 generation, emergence rate, development, and sex ratio did not vary with storage time when the F1 parents parasitized fresh host eggs. Demographic parameters for the F, population showed that net reproductive rate was > 20 although it decreased significantly after their parental host eggs were stored for > 30 d. The intrinsic and finite rates of increase, population doubling time, and mean generation time decreased only after storage for 60 d. Our results show that short-term cold storage could be used for maintaining wasp populations in a mass-rearing program and that the detrimental effects of chilling host eggs in storage for over 30 d do not extend to F2 generation.

Engineering an invasion: classical biological control of the glassy-winged sharpshooter, Homalodisca vitripennis, by the egg parasitoid Gonatocerus ashmeadi in Tahiti and Moorea, French Polynesia

The glassy-winged sharpshooter, Homalodisca vitripennis Germar (=H. coagulata Say) (Hemiptera: Cicadellidae), invaded Tahiti in 1999 and spread rapidly to the main island groups of French Polynesia becoming an important pest. It threatened agriculture, native biodiversity, and created serious social and recreational problems. Further, massive uncontrolled populations on Tahiti presented an elevated invasion threat to other South Pacific nations. In 2004, a classical biological control program against H. vitripennis was initiated in French Polynesia using the highly host-specific egg parasitoid Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). After risk assessment studies indicated an acceptably low level of risk to non-target species, 13,786 parasitoids were released at 27 sites in Tahiti between May and October 2005. Here we present the results of G. ashmeadi and H. vitripennis population surveys during the first year of their interaction in French Polynesia (until mid-May 2006). The impact of G. ashmeadi on H. vitripennis was extremely rapid and high. Parasitism of H. vitripennis egg masses by G. ashmeadi has averaged 80–100% in Tahiti since the introduction of the parasitoid, and populations of H. vitripennis nymphs and adults have decreased by more than 90% since December 2005. Populations of H. vitripennis have been successfully maintained at this low level for more than 1 year. The same results were obtained in nearby Moorea where the parasitoid was probably spread by the unregulated transport of plants infested with parasitized H. vitripennis eggs. Population monitoring continues in order to determine if a stable equilibrium between the pest and the parasitoid has been reached.

Lethal toxicity of systemic residues of imidacloprid against Homalodisca vitripennis (Homoptera: Cicadellidae) eggs and its parasitoid Gonatocerus ashmeadi (Hymenoptera: Mymaridae)

Abstract A study was conducted to determine the lethal effects of systemic imidacloprid against the egg stage of the glassy-winged sharpshooter Homalodisca vitripennis , and its mymarid egg parasitoid Gonatocerus ashmeadi . During the development of the sharpshooter embryo within the egg, imidacloprid did not have a lethal effect, even at very high concentrations. However, upon emergence from the egg mass, the 1st instar nymph encountered residues of imidacloprid in the surrounding leaf tissues. When mortality was assessed within 48 h of emergence, there was an excellent dose–response between the imidacloprid concentration and nymph mortality, giving an LC 50 of 39 ng imidacloprid per cm 2 leaf. In the same way, G. ashmeadi did not succumb to lethal levels of imidacloprid during its development within the sharpshooter egg. However, parasitoid adults were sensitive to imidacloprid residues during emergence from the sharpshooter egg. When mortality was assessed within 48 h of emergence, the LC 50 for the parasitoid was 66 ng imidacloprid per cm 2 leaf. In a survey of commercial citrus trees that were treated with imidacloprid, the mean residues of the insecticide within the leaves did not exceed the LC 50 concentrations for either insect. The implications of these results for the integration of biological and chemical controls are discussed.

Species identity of geographically distinct populations of the glassy-winged sharpshooter parasitoid Gonatocerus ashmeadi: morphology, DNA sequences, and reproductive compatibility

Abstract Gonatocerus ashmeadi is a common and seemingly widespread egg parasitoid of Homalodisca coagulata , the glassy-winged sharpshooter (GWSS). Location records for G. ashmeadi indicate its natural range to be the southeastern USA and northeastern Mexico (which coincides with the presumed native range of GWSS), and possibly southern and central California (CA) (the adventive range of GWSS). The purpose of our work was to determine whether G. ashmeadi in the USA and northeastern Mexico is one species or a complex of reproductively incompatible sibling species. We used three approaches to determine the species identity of different G. ashmeadi populations: (1) reassessment of key morphological features using scanning electron microscopy (SEM) to determine if subtle morphological differences exist between G. ashmeadi populations which could indicate species differences; (2) to determine if molecular differences exist between G. ashmeadi populations collected from different regions by comparing mitochondrial and ribosomal DNA sequences; (3) mating compatibility studies to determine if different populations of G. ashmeadi are reproductively isolated, or if mating occurs, whether offspring are viable thereby defining species groups on the basis of successful interbreeding. Results from these three areas (morphology, DNA sequences, and reproductive compatibility) have been evaluated collectively; leading us to the conclusion that G. ashmeadi as it is currently viewed is a valid species and not an aggregate of morphologically indistinguishable cryptic species.