Immune system modulation & virus transmission during parasitism identified by multi-species transcriptomics of a declining insect biocontrol system.

BACKGROUND: The Argentine stem weevil (ASW, Listronotus bonariensis) is a significant pasture pest in Aotearoa New Zealand, primarily controlled by the parasitoid biocontrol agent Microctonus hyperodae. Despite providing effective control of ASW soon after release, M. hyperodae parasitism rates have since declined significantly, with ASW hypothesised to have evolved resistance to its biocontrol agent. While the parasitism arsenal of M. hyperodae has previously been investigated, revealing many venom components and an exogenous novel DNA virus Microctonus hyperodae filamentous virus (MhFV), the effects of said arsenal on gene expression in ASW during parasitism have not been examined. In this study, we performed a multi-species transcriptomic analysis to investigate the biology of ASW parasitism by M. hyperodae, as well as the decline in efficacy of this biocontrol system. RESULTS: The transcriptomic response of ASW to parasitism by M. hyperodae involves modulation of the weevil's innate immune system, flight muscle components, and lipid and glucose metabolism. The multispecies approach also revealed continued expression of venom components in parasitised ASW, as well as the transmission of MhFV to weevils during parasitism and some interrupted parasitism attempts. Transcriptomics did not detect a clear indication of parasitoid avoidance or other mechanisms to explain biocontrol decline. CONCLUSIONS: This study has expanded our understanding of interactions between M. hyperodae and ASW in a biocontrol system of critical importance to Aotearoa-New Zealand's agricultural economy. Transmission of MhFV to ASW during successful and interrupted parasitism attempts may link to a premature mortality phenomenon in ASW, hypothesised to be a result of a toxin-antitoxin system. Further research into MhFV and its potential role in ASW premature mortality is required to explore whether manipulation of this viral infection has the potential to increase biocontrol efficacy in future.

The conserved and high K-to-Na ratio in sunflower pollen: Possible implications for bee health and plant-bee interactions.

Sodium (Na) concentrations are low in plant tissues, and its metabolic function in plants is minor; however, Na is a key nutrient for plant consumers. Previous studies have thus far focused on Na concentration. Nevertheless, a balanced potassium (K) to Na ratio (K:Na) is more important than Na concentration alone since food with high K:Na has detrimental effects on consumers irrespective of Na concentration. Therefore, plants may actively regulate K:Na in their tissues and products, shaping plant-insect interactions. Studies considering nutritional aspects of plant-insect interactions have focused on nonreproductive tissues and nectar. In this study, we consider pollen as serving a primary reproductive function for plants as well as a food of pollinivores. Plants might regulate K:Na in pollen to affect their interactions with pollinivorous pollinators. To investigate whether such a mechanism exists, we manipulated Na concentrations in soil and measured the proportion of K, Na, and 13 other nutrient elements in the pollen of two sunflower (Helianthus annuus) cultivars. This approach allowed us to account for the overall nutritional quality of pollen by investigating the proportions of many elements that could correlate with the concentrations of K and Na. Of the elements studied, only the concentrations of Na and K were highly correlated. Pollen K:Na was high in both cultivars irrespective of Na fertilization, and it remained high regardless of pollen Na concentration. Interestingly, pollen K:Na did not decrease as pollen increased the Na concentration. We hypothesize that high K:Na in pollen might benefit plant fertilization and embryonic development; therefore, a tradeoff might occur between producing low K:Na pollen as a reward for pollinators and high K:Na pollen to optimize the plant fertilization process. This is the first study to provide data on pollen K:Na regulation by plants. Our findings broaden the understanding of plant-bee interactions and provide a foundation for a better understanding of the role of the soil-plant-pollen-pollinator pathway in nutrient cycling in ecosystems. Specifically, unexplored costs and tradeoffs related to balancing the K:Na by plants and pollinivores might play a role in past and current shaping of pollination ecology.

Plant-Mediated Behavioural Avoidance of a Weevil Towards Its Biological Control Agent.

New Zealand pastures largely comprising Lolium ryegrass species (Poales: Poaceae) are worth $19.6B and are subject to major pest impacts. A very severe pest is the Argentine stem weevil Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). This has been previously suppressed by the importation biological control agent, Microctonus hyperodae Loan (Hymenoptera: Braconidae). However, this suppression has recently declined and is subject to investigation. It has been hypothesised that grass type influences the parasitism avoidance behaviour by the weevil and thus parasitism rates. This study explored the hypothesis using three common pasture grasses: a diploid Lolium perenne x Lolium multiflorum hybrid ryegrass (cv. Manawa), a tetraploid Italian ryegrass L. multiflorum Lam. (cv. Tama), and a diploid perennial ryegrass L. perenne L. (cv. Samson). The described laboratory-based microcosm methodology determined the extent of weevil avoidance behaviour on each of these three grasses when subjected to the parasitoid. Such reaction was gauged by the extent of reduced weevil on-plant presence and feeding compared to the control populations. In the absence of the parasitoid, the hybrid cv. Manawa ryegrass is as highly favoured by the weevil as the tetraploid cv. Tama. On diploid cv. Samson, feeding is considerably less. In the presence of the parasitoid, weevils on the tetraploid cv. Tama plants showed little avoidance activity in response to the parasitoid and it can be argued that the benefits of staying on this plant outweighed the possibility of parasitism. Conversely and surprisingly, in the parasitoid's presence, weevils on diploid cv. Manawa showed very strong avoidance behaviour leading to levels of exposure similar to those found on the less-preferred diploid cv. Samson. These findings reflect how weevil parasitism rates have declined in most Lolium grasses, particularly diploids, since the 1990s, but not in the tetraploid L. multiflorum. This contribution supports the hypothesis that the decline in weevil parasitism rates has been the result of rapid evolution arising from parasitoid-induced selection pressure and the countervailing effect of the nutritional quality of the host plants.

Potential ecosystem service delivery by endemic plants in New Zealand vineyards: successes and prospects.

Vineyards worldwide occupy over 7 million hectares and are typically virtual monocultures, with high and costly inputs of water and agro-chemicals. Understanding and enhancing ecosystem services can reduce inputs and their costs and help satisfy market demands for evidence of more sustainable practices. In this New Zealand work, low-growing, endemic plant species were evaluated for their potential benefits as Service Providing Units (SPUs) or Ecosystem Service Providers (ESPs). The services provided were weed suppression, conservation of beneficial invertebrates, soil moisture retention and microbial activity. The potential Ecosystem Dis-services (EDS) from the selected plant species by hosting the larvae of a key vine moth pest, the light-brown apple moth (Epiphyas postvittana), was also quantified. Questionnaires were used to evaluate winegrowers' perceptions of the value of and problems associated with such endemic plant species in their vineyards. Growth and survival rates of the 14 plant species, in eight families, were evaluated, with Leptinella dioica (Asteraceae) and Acaena inermis 'purpurea' (Rosaceae) having the highest growth rates in terms of area covered and the highest survival rate after 12 months. All 14 plant species suppressed weeds, with Leptinella squalida, Geranium sessiliforum (Geraniaceae), Hebe chathamica (Plantaginaceae), Scleranthus uniflorus (Caryophyllaceae) and L. dioica, each reducing weed cover by >95%. Plant species also differed in the diversity of arthropods that they supported, with the Shannon Wiener diversity index (H') for these taxa ranging from 0 to 1.3. G. sessiliforum and Muehlenbeckia axillaris (Polygonaceae) had the highest invertebrate diversity. Density of spiders was correlated with arthropod diversity and G. sessiliflorum and H. chathamica had the highest densities of these arthropods. Several plant species associated with higher soil moisture content than in control plots. The best performing species in this context were A. inermis 'purpurea' and Lobelia angulata (Lobeliaceae). Soil beneath all plant species had a higher microbial activity than in control plots, with L. dioica being highest in this respect. Survival proportion to the adult stage of the moth pest, E. postvittana, on all plant species was poor (<0.3). When judged by a ranking combining multiple criteria, the most promising plant species were (in decreasing order) G. sessiliflorum, A. inermis 'purpurea', H. chathamica, M. axillaris, L. dioica, L. angulata, L. squalida and S. uniflorus. Winegrowers surveyed said that they probably would deploy endemic plants around their vines. This research demonstrates that enhancing plant diversity in vineyards can deliver SPUs, harbour ESPs and therefore deliver ES. The data also shows that growers are willing to follow these protocols, with appropriate advice founded on sound research.