Altered precipitation and root herbivory affect the productivity and composition of a mesic grassland.

BACKGROUND: Climate change models predict changes in the amount, frequency and seasonality of precipitation events, all of which have the potential to affect the structure and function of grassland ecosystems. While previous studies have examined plant or herbivore responses to these perturbations, few have examined their interactions; even fewer have included belowground herbivores. Given the ecological, economic and biodiversity value of grasslands, and their importance globally for carbon storage and agriculture, this is an important knowledge gap. To address this, we conducted a precipitation manipulation experiment in a former mesic pasture grassland comprising a mixture of C4 grasses and C3 grasses and forbs, in southeast Australia. Rainfall treatments included a control [ambient], reduced amount [50% ambient] and reduced frequency [ambient rainfall withheld for three weeks, then applied as a single deluge event] manipulations, to simulate predicted changes in both the size and frequency of future rainfall events. In addition, half of all experimental plots were inoculated with adult root herbivores (Scarabaeidae beetles). RESULTS: We found strong seasonal dependence in plant community responses to both rainfall and root herbivore treatments. The largest effects were seen in the cool season with lower productivity, cover and diversity in rainfall-manipulated plots, while root herbivore inoculation increased the relative abundance of C3, compared to C4, plants. CONCLUSIONS: This study highlights the importance of considering not only the seasonality of plant responses to altered rainfall, but also the important role of interactions between abiotic and biotic drivers of vegetation change when evaluating ecosystem-level responses to future shifts in climatic conditions.

Drought negates growth stimulation due to root herbivory in pasture grasses.

Predicted increases in extreme weather are likely to alter the interactions between organisms within ecosystems. Whilst many studies have investigated the impacts of climate change on aboveground plant-insect interactions, those belowground remain relatively unexplored. Root herbivores can be the dominant taxa in grasslands, potentially altering plant community dynamics. To better predict the impact of climate change on grasslands, we subjected four Australian pasture grasses (Cynodon dactylon, Paspalum dilatatum, Microlaena stipoides and Lolium perenne) to contrasting rainfall regimes [a press drought (i.e. sustained, moderate water stress), a pulse drought (water stress followed by periodic, infrequent deluge event) and a well-watered control], with and without root herbivores; a manual root cutting treatment was also included for comparison. Plant growth, rooting strategy, phenology and biochemistry were measured to evaluate above and belowground treatment responses. Watering treatments had a larger effect on plant productivity than root damage treatments: press drought and pulse drought treatments reduced biomass by 58% and 47%, respectively. Root herbivore damage effects were species dependent and were not always equivalent to root cutting. The combination of pulse drought and root herbivory resulted in increased root:shoot ratios for both P. dilatatum and L. perenne, as well as decreased biomass and delayed flowering time for P. dilatatum. Plant biomass responses to root damage were greatest under well-watered conditions; however, root damage also delayed or prevented investment in reproduction in at least one species. Our findings highlight the important role of soil-dwelling invertebrates for forecasting growth responses of grassland communities to future rainfall regime changes.

Ode to Ehrlich and Raven or how herbivorous insects might drive plant speciation.

Fifty years ago, Ehrlich and Raven proposed that insect herbivores have driven much of plant speciation, particularly at tropical latitudes. There have been no explicit tests of their hypotheses. Indeed there were no proposed mechanisms either at the time or since by which herbivores might generate new plant species. Here we outline two main classes of mechanisms, prezygotic and postzygotic, with a number of scenarios in each by which herbivore-driven changes in host plant secondary chemistry might lead to new plant lineage production. The former apply mainly to a sympatric model of speciation while the latter apply to a parapatric or allopatric model. Our review suggests that the steps of each mechanism are known to occur individually in many different systems, but no scenario has been thoroughly investigated in any one system. Nevertheless, studies of Dalechampia and its herbivores and pollinators, and patterns of defense tradeoffs in trees on different soil types in the Peruvian Amazon provide evidence consistent with the original hypotheses of Ehrlich and Raven. For herbivores to drive sympatric speciation, our findings suggest that interactions with both their herbivores and their pollinators should be considered. In contrast, herbivores may drive speciation allopatrically without any influence by pollinators. Finally, there is evidence that these mechanisms are more likely to occur at low latitudes and thus more likely to produce new species in the tropics. The mechanisms we outline provide a predictive framework for further study of the general role that herbivores play in diversification of their host plants.

DRI-Grass: A New Experimental Platform for Addressing Grassland Ecosystem Responses to Future Precipitation Scenarios in South-East Australia.

Climate models predict shifts in the amount, frequency and seasonality of rainfall. Given close links between grassland productivity and rainfall, such changes are likely to have profound effects on the functioning of grassland ecosystems and modify species interactions. Here, we introduce a unique, new experimental platform - DRI-Grass (Drought and Root Herbivore Interactions in a Grassland) - that exposes a south-eastern Australian grassland to five rainfall regimes [Ambient (AMB), increased amount (IA, +50%), reduced amount (RA, -50%), reduced frequency (RF, single rainfall event every 21 days, with total amount unchanged) and summer drought (SD, 12-14 weeks without water, December-March)], and contrasting levels of root herbivory. Incorporation of a belowground herbivore (root-feeding scarabs) addition treatment allows novel investigation of ecological responses to the twin stresses of altered rainfall and root herbivory. We quantified effects of permanently installed rain shelters on microclimate by comparison with outside plots, identifying small shelter effects on air temperature (-0.19°C day, +0.26°C night), soil water content (SWC; -8%) and photosynthetically active radiation (PAR; -16%). Shelters were associated with modest increases in net primary productivity (NPP), particularly during the cool season. Rainfall treatments generated substantial differences in SWC, with the exception of IA; the latter is likely due to a combination of higher transpiration rates associated with greater plant biomass in IA and the low water-holding capacity of the well-drained, sandy soil. Growing season NPP was strongly reduced by SD, but did not respond to the other rainfall treatments. Addition of root herbivores did not affect plant biomass and there were no interactions between herbivory and rainfall treatments in the 1st year of study. Root herbivory did, however, induce foliar silicon-based defenses in Cynodon dactylon and Eragrostis curvula. Rapid recovery of NPP following resumption of watering in SD plots indicates high functional resilience at the site, and may reflect adaptation of the vegetation to historically high variability in rainfall, both within- and between years. DRI-Grass provides a unique platform for understanding how ecological interactions will be affected by changing rainfall regimes and, specifically, how belowground herbivory modifies grassland resistance and resilience to climate extremes.

Altered Precipitation Impacts on Above- and Below-Ground Grassland Invertebrates: Summer Drought Leads to Outbreaks in Spring.

Climate change is predicted to result in altered precipitation patterns, which may reshape many grassland ecosystems. Rainfall is expected to change in a number of different ways, ranging from periods of prolonged drought to extreme precipitation events, yet there are few community wide studies to accurately simulate future changes. We aimed to test how above- and below-ground grassland invertebrate populations were affected by contrasting future rainfall scenarios. We subjected a grassland community to potential future rainfall scenarios including ambient, increased amount (+50% of ambient), reduced amount (-50% of ambient), reduced frequency (no water for 21 days, followed by the total ambient rainfall applied in a single application) and summer drought (no rainfall for 13 weeks during the growing season). During Austral spring (September 2015), we sampled aboveground invertebrates, belowground macro invertebrates and nematodes. Aboveground communities showed a significant response to altered rainfall regime with the greatest effects observed in summer drought plots. This was mostly due to a large increase in sucking herbivores (658% higher than ambient plots). Plots experiencing summer droughts also had higher populations of parasitoids, chewing herbivores and detritivores. These plots had 92% more plant biomass suggesting that primary productivity increased rapidly following the end of the summer drought 5 months earlier. We interpret these results as supporting the plant vigor hypothesis (i.e., that rapid plant growth is beneficial to aboveground invertebrates). While belowground invertebrates were less responsive to altered precipitation, we observed a number of correlations between the abundances of above- and below-ground invertebrate groups under ambient rainfall that dissipated under altered rainfall regimes. Mechanisms underpinning these associations, and reasons for them to become decoupled under altered precipitation regimes (we term this 'climatic decoupling'), remain speculative, but they provide the basis for formulating hypotheses and future work. In conclusion, we predict that shifts in rainfall patterns, especially summer drought, will likely have large, but probably short-term, impacts on grassland invertebrate communities. In particular, sucking herbivores show sensitivity to precipitation changes, which have the potential to cascade through the food chain and affect higher trophic levels.

Grasslands, Invertebrates, and Precipitation: A Review of the Effects of Climate Change.

Invertebrates are the main components of faunal diversity in grasslands, playing substantial roles in ecosystem processes including nutrient cycling and pollination. Grassland invertebrate communities are heavily dependent on the plant diversity and production within a given system. Climate change models predict alterations in precipitation patterns, both in terms of the amount of total inputs and the frequency, seasonality and intensity with which these inputs occur, which will impact grassland productivity. Given the ecological, economic and biodiversity value of grasslands, and their importance globally as areas of carbon storage and agricultural development, it is in our interest to understand how predicted alterations in precipitation patterns will affect grasslands and the invertebrate communities they contain. Here, we review the findings from manipulative and observational studies which have examined invertebrate responses to altered rainfall, with a particular focus on large-scale field experiments employing precipitation manipulations. Given the tight associations between invertebrate communities and their underlying plant communities, invertebrate responses to altered precipitation generally mirror those of the plants in the system. However, there is evidence that species responses to future precipitation changes will be idiosyncratic and context dependent across trophic levels, challenging our ability to make reliable predictions about how grassland communities will respond to future climatic changes, without further investigation. Thus, moving forward, we recommend increased consideration of invertebrate communities in current and future rainfall manipulation platforms, as well as the adoption of new technologies to aid such studies.

Belowground Ecology of Scarabs Feeding on Grass Roots: Current Knowledge and Future Directions for Management in Australasia.

Many scarab beetles spend the majority of their lives belowground as larvae, feeding on grass roots. Many of these larvae are significant pests, causing damage to crops and grasslands. Damage by larvae of the greyback cane beetle (Dermolepida albohirtum), for example, can cause financial losses of up to AU$40 million annually to the Australian sugarcane industry. We review the ecology of some scarab larvae in Australasia, focusing on three subfamilies; Dynastinae, Rutelinae, and Melolonthinae, containing key pest species. Although considerable research on the control of some scarab pests has been carried out in Australasia, for some species, the basic biology and ecology remains largely unexplored. We synthesize what is known about these scarab larvae and outline key knowledge gaps to highlight future research directions with a view to improve pest management. We do this by presenting an overview of the scarab larval host plants and feeding behavior; the impacts of abiotic (temperature, moisture, and fertilization) and biotic (pathogens, natural enemies, and microbial symbionts) factors on scarab larvae and conclude with how abiotic and biotic factors can be applied in agriculture for improved pest management, suggesting future research directions. Several host plant microbial symbionts, such as arbuscular mycorrhizal fungi and endophytes, can improve plant tolerance to scarabs and reduce larval performance, which have shown promise for use in pest management. In addition to this, several microbial scarab pathogens have been isolated for commercial use in pest management with particularly promising results. The entomopathogenic fungus Metarhizium anisopliae caused a 50% reduction in cane beetle larvae while natural enemies such as entomopathogenic nematodes have also shown potential as a biocontrol. Key abiotic factors, such as soil water, play an important role in affecting both scarab larvae and these control agents and should therefore feature in future multi-factorial experiments. Continued research should focus on filling knowledge gaps including host plant preferences, attractive trap crops, and naturally occurring pathogens that are locally adapted, to achieve high efficacy in the field.

Reducing rainfall amount has a greater negative effect on the productivity of grassland plant species than reducing rainfall frequency.

The productivity of semiarid Australian grassland ecosystems is currently limited by water availability and may be impacted further by predicted changes in rainfall regimes associated with climate change. In this study, we established a rainfall manipulation experiment to determine the effects of reduced frequency (RF; 8 days between water events) and reduced magnitude (RM; 50% reduction in amount) of rainfall events on the physiology and above- and below-ground growth of five grassland plant species with differing traits. Native C4 grasses exhibited the highest productivity in well watered, control (Cont) conditions, as well as in RF and RM treatments. The RF treatment generally had little effect on total biomass, rooting distributions or photosynthesis, suggesting species were relatively tolerant of reduction in the frequency of rainfall events. However, the RM treatment had a negative effect on total biomass and physiology, and generally resulted in a shift towards shallower rooting profiles. Overall, the reduction in biomass was greater in RM than RF, suggesting that rainfall magnitude may be a more important determinant of grassland productivity and composition than the frequency of rainfall events under future climates.

Invasive plant species alters consumer behavior by providing refuge from predation.

Understanding the effects of invasive plants on native consumers is important because consumer-mediated indirect effects have the potential to alter the dynamics of coexistence in native communities. Invasive plants may promote changes in consumer pressure due to changes in protective cover (i.e., the architectural complexity of the invaded habitat) and in food availability (i.e., subsidies of fruits and seeds). No experimental studies have evaluated the relative interplay of these two effects. In a factorial experiment, we manipulated cover and food provided by the invasive shrub Amur honeysuckle (Lonicera maackii) to evaluate whether this plant alters the foraging activity of native mammals. Using tracking plates to quantify mammalian foraging activity, we found that removal of honeysuckle cover, rather than changes in the fruit resources it provides, reduced the activity of important seed consumers, mice in the genus Peromyscus. Two mesopredators, Procyon lotor and Didelphis virginiana, were also affected. Moreover, we found rodents used L. maackii for cover only on cloudless nights, indicating that the effect of honeysuckle was weather-dependent. Our work provides experimental evidence that this invasive plant species changes habitat characteristics, and in so doing alters the behavior of small- and medium-sized mammals. Changes in seed predator behavior may lead to cascading effects on the seeds that mice consume.

Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics.

Despite the ubiquity of invasive organisms and their often deleterious effects on native flora and fauna, the consequences of biological invasions for human health and the ecological mechanisms through which they occur are rarely considered. Here we demonstrate that a widespread invasive shrub in North America, Amur honeysuckle (Lonicera maackii), increases human risk of exposure to ehrlichiosis, an emerging infectious disease caused by bacterial pathogens transmitted by the lone star tick (Amblyomma americanum). Using large-scale observational surveys in natural areas across the St. Louis, Missouri region, we found that white-tailed deer (Odocoileus virginianus), a preeminent tick host and pathogen reservoir, more frequently used areas invaded by honeysuckle. This habitat preference translated into considerably greater numbers of ticks infected with pathogens in honeysuckle-invaded areas relative to adjacent honeysuckle-uninvaded areas. We confirmed this biotic mechanism using an experimental removal of honeysuckle, which caused a decrease in deer activity and infected tick numbers, as well as a proportional shift in the blood meals of ticks away from deer. We conclude that disease risk is likely to be reduced when honeysuckle is eradicated, and suggest that management of biological invasions may help ameliorate the burden of vector-borne diseases on human health.