How Nutrients Mediate the Impacts of Global Change on Locust Outbreaks.

Locusts are grasshoppers that can migrate en masse and devastate food security. Plant nutrient content is a key variable influencing population dynamics, but the relationship is not straightforward. For an herbivore, plant quality depends not only on the balance of nutrients and antinutrients in plant tissues, which is influenced by land use and climate change, but also on the nutritional state and demands of the herbivore, as well as its capacity to extract nutrients from host plants. In contrast to the concept of a positive relationship between nitrogen or protein concentration and herbivore performance, a five-decade review of lab and field studies indicates that equating plant N to plant quality is misleading because grasshoppers respond negatively or neutrally to increasing plant N just as often as they respond positively. For locusts specifically, low-N environments are actually beneficial because they supply high energy rates that support migration. Therefore, intensive land use, such as continuous grazing or cropping, and elevated ambient CO2 levels that decrease the protein:carbohydrate ratios of plants are predicted to broadly promote locust outbreaks.

High carbohydrate consumption increases lipid storage and promotes migratory flight in locusts.

Migration allows animals to track favorable environments and avoid harmful conditions. However, migration is energetically costly, so migrating animals must prepare themselves by increasing their energy stores. Despite the importance of locust migratory swarms, we still understand little about the physiology of locust migration. During long-distance flight, locusts rely on lipid oxidation, despite the fact that lipids are relatively rare in their leaf-based diets. Therefore, locusts and other insect herbivores synthesize and store lipid from ingested carbohydrates, which are also important for initial flight. These data suggest that diets high in carbohydrate should increase lipid stores and the capacity for migratory flight in locusts. As predicted, locust lipid stores and flight performance increased with an increase in the relative carbohydrate content in their food. However, locust flight termination was not associated with complete lipid depletion. We propose potential testable mechanisms that might explain how macronutrient consumption can affect flight endurance.

Nutrient supply and accessibility in plants: effect of protein and carbohydrates on Australian plague locust (Chortoicetes terminifera) preference and performance.

In contrast to predictions from nitrogen limitation theory, recent studies have shown that herbivorous migratory insects tend to be carbohydrate (not protein) limited, likely due to increased energy demands, leading them to preferentially feed on high carbohydrate plants. However, additional factors such as mechanical and chemical defenses can also influence host plant choice and nutrient accessibility. In this study, we investigated the effects of plant protein and carbohydrate availability on plant selection and performance for a migratory generalist herbivore, the Australian plague locust, Chortoicetes terminifera. We manipulated the protein and carbohydrate content of seedling wheat (Triticum aestivum L.) by increasing the protein:carbohydrate ratio using nitrogen (N) fertilizer, and manipulated the physical structure of the plants by grinding and breaking down cell walls after drying the plants. Using a full factorial design, we ran both choice and no-choice experiments to measure preference and performance. We confirmed locust preference for plants with a lower protein-carbohydrate ratio (unfertilized plants). Unlike previous studies with mature wild grass species, we found that intact plants supported better performance than dried and ground plants, suggesting that cell wall removal may only improve performance for tougher or more carbohydrate-rich plants. These results add to the growing body of evidence suggesting that several migratory herbivorous species perform better on plants with a lower protein:carbohydrate ratio.

Field bands of marching locust juveniles show carbohydrate, not protein, limitation.

Locusts are grasshoppers that migrate en masse and devastate food security, yet little is known about the nutritional needs of marching bands in nature. While it has been hypothesized that protein limitation promotes locust marching behavior, migration is fueled by dietary carbohydrates. We studied South American Locust (Schistocerca cancellata) bands at eight sites across Argentina, Bolivia, and Paraguay. Bands ate most frequently from dishes containing carbohydrate artificial diets and minimally from balanced, protein, or control (vitamins and salts) dishes-indicating carbohydrate hunger. This hunger for carbohydrates is likely explained by the observation that local vegetation was generally protein-biased relative to locusts' preferred protein to carbohydrate ratio. This study highlights the importance of studying the nutritional ecology of animals in their environment and suggests that carbohydrate limitation may be a common pattern for migrating insect herbivores.

High carbohydrate diet ingestion increases post-meal lipid synthesis and drives respiratory exchange ratios above 1.

Locusts have been reported to elevate metabolic rate in response to high carbohydrate diets; this conclusion was based on metabolic rates calculated from CO2 production, a common practice for insects. However, respiratory exchange ratio (RER, CO2 production divided by O2 consumption) can rise above 1 as a result of de novo lipid synthesis, providing an alternative possible explanation of the prior findings. We studied the relationship between macronutrient ingestion, RER and lipid synthesis using South American locusts (Schistocerca cancellata) reared on artificial diets varying in protein:carbohydrate (p:c) ratio. RER increased and rose above 1 as dietary p:c ratio decreased. Lipid accumulation rates were strongly positively correlated with dietary carbohydrate content and ingestion. RERs above 1 were only observed for animals without food in the respirometry chamber, suggesting that hormonal changes after a meal may drive lipid synthesis. Schistocerca cancellata does not elevate metabolic rate on low p:c diets; in fact, the opposite trend was observed.

Physiological status is a stronger predictor of nutrient selection than ambient plant nutrient content for a wild herbivore.

There is generally a close relationship between a consumer's food and its optimal nutrients. When there is a mismatch, it is hypothesized that mobile herbivores switch between food items to balance nutrients, however, there are limited data for field populations. In this study, we measured ambient plant nutrient content at two time points and contrasted our results with the nutrient ratio selected by wild female and male grasshoppers (Oedaleus senegalensis). Few plants were near O. senegalensis' optimal protein:carbohydrate ratio (P:C), nor were plants complementary. Grasshoppers collected earlier all regulated for a carbohydrate-biased ratio but females ate slightly more protein. We hypothesized that the long migration undertaken by this species may explain its carbohydrate needs. In contrast to most laboratory studies, grasshoppers collected later did not tightly regulate their P:C. These results suggest that field populations are not shifting their P:C to match seasonal plant nutrient shifts and that mobile herbivores rely on post-ingestive mechanisms in the face of environmental variation. Because this is among the first studies to examine the relationship between ambient nutrient landscape and physiological state our data are a key step in bridging knowledge acquired from lab studies to hypotheses regarding the role ecological factors play in foraging strategies.

Plant carbohydrate content limits performance and lipid accumulation of an outbreaking herbivore.

Locusts are major intermittent threats to food security and the ecological factors determining where and when these occur remain poorly understood. For many herbivores, obtaining adequate protein from plants is a key challenge. We tested how the dietary protein : non-structural carbohydrate ratio (p : c) affects the developmental and physiological performance of 4th-5th instar nymphs of the South American locust, Schistocerca cancellata, which has recently resurged in Argentina, Bolivia and Paraguay. Field marching locusts preferred to feed on high carbohydrate foods. Field-collected juveniles transferred to the laboratory selected artificial diets or local plants with low p : c. On single artificial diets, survival rate increased as foods became more carbohydrate-biased. On single local plants, growth only occurred on the plant with the lowest p : c. Most local plants had p : c ratios substantially higher than optimal, demonstrating that field marching locusts must search for adequate carbohydrate or their survival and growth will be carbohydrate-limited. Total body lipids increased as dietary p : c decreased on both artificial and plant diets, and the low lipid contents of field-collected nymphs suggest that obtaining adequate carbohydrate may pose a strong limitation on migration for S. cancellata. Anthropogenic influences such as conversions of forests to pastures, may increase carbohydrate availability and promote outbreaks and migration of some locusts.

Nitrogen fertilizer decreases survival and reproduction of female locusts by increasing plant protein to carbohydrate ratio.

Nitrogen limitation theory predicts that terrestrial plants should benefit from nitrogen inputs and that herbivores should benefit from subsequent higher plant protein contents. While this pattern has generally been supported, some herbivorous insects have shown preference and higher performance on low protein (p), high carbohydrate (c) diets as juveniles. However, little is known about the effects on reproduction in adults. Using nitrogen fertilizer, we demonstrate that high plant p:c has negative effects on Senegalese locust (Orthoptera: Oedaeleus senegalensis) reproduction and survival in an agroecological setting. For this, we measured p:c in millet plants Pennisetum glaucum that received two levels of fertilizer (high and moderate) and a control, then we caged locusts on these plants for 2 weeks. In the laboratory, we gave locusts the choice between untreated millet leaves and leaves that received one of the two fertilization treatment. We found that fertilization increased p:c ratio in a concentration-dependent fashion. We counted the number of locusts alive over the course of 2 weeks and showed that fewer females survived on fertilized plants than on control plants. Females that ate plants from the high fertilization treatment laid lighter eggs. Finally, we showed that female locusts prefer unfertilized plants to plants with a high p:c. We hypothesize that this pattern will apply broadly to species that have extensive carbohydrate needs, such as long-distance migrators. Because many ecological studies focus primarily on nitrogen or protein, and fail to consider carbohydrates, this study has important implications for how ecologists consider nutrient limitation of primary consumers in ecosystems globally.

Soil-targeted interventions could alleviate locust and grasshopper pest pressure in West Africa.

Agricultural land use has intended and unintended consequences for human livelihoods through feedbacks within coupled human and natural systems. In Senegal, West Africa, soils are a vital resource for livelihoods and food security in smallholder farming communities. In this study, we explored the connections among land use, soil conditions, plant nutrient content, and the abundance of several locust and grasshopper species. We worked in two rural farming villages in the Kaffrine region of Senegal. Oedaleus senegalensis was least abundant in groundnut areas where plant N was highest and abundance was negatively correlated with plant N across land use types. Overall, grasshoppers were most numerous in grazing and fallow areas. There was little variation in soil properties across land use types and soil organic matter (SOM) and inorganic soil N content were low throughout. SOM was positively correlated with soil inorganic N concentration, which in turn was positively correlated with plant N content. Of the management practices we surveyed, fallowing fields was important for soil N and SOM replenishment. These results corroborate other research indicating that land use, management practices, soil and plant nutrients, and insect herbivore abundance are mechanistically coupled. Although further research is needed, improving soil fertility could be used as an alternative to pesticides to keep locusts at bay and improve crop yields.

Anoxia tolerance of the adult Australian Plague Locust (Chortoicetes terminifera).

Optimal breeding conditions for locust swarms often include heavy rainfall and flooding, exposing individuals to the risk of immersion and anoxia. We investigated anoxia tolerance in solitarious and gregarious adults of the Australian Plague Locust, Chortoicetes terminifera, by measuring the time to enter an anoxic coma after submersion in water, the time for recovery of ventilation and the ability to stand on return to air. We found a longer time to succumb in immature adults that we attribute to a larger tracheal volume. Time to succumb was also longer after autotomizing the hindlegs to reduce the energetic cost of muscular activity. Time to recover was longer in gregarious males and this developed during maturation, suggesting an increase in the cost of neural processing associated with social interactions under crowded conditions. Short-term changes in rearing conditions had effects that we interpret as stress responses, potentially mediated by octopamine.

The impact of nitrogen enrichment on grassland ecosystem stability depends on nitrogen addition level.

Increasing atmospheric nitrogen (N) deposition may affect plant biodiversity, subsequently altering ecosystem stability. While a few studies have explored how simulated N deposition affects community stability and its underlying mechanisms, the experimental levels of N addition used are usually higher than current and future N deposition rates. Thus, their results could produce highly uncertain predictions of ecosystem function, especially if the responses to N deposition are nonlinear. We conducted a manipulative experiment that simulated elevated atmospheric N deposition with several N addition levels to evaluate the effect of N deposition on ecosystem stability and its underlying mechanisms in a semiarid grassland in northern China. Here we show that N addition altered community diversity, reducing species richness, evenness, diversity and dominance. In addition, we found that N addition at current N deposition levels had no significant impact on community stability. In contrast, N addition at levels from 4.6 to 13.8gNm-2yr-1 significantly decreased community stability, although community stability for the 13.8gNm-2yr-1 treatment was higher than that for the 4.6gNm-2yr-1 treatment. These results indicate that the response of community stability to N enrichment is nonlinear. This nonlinear change in community stability was positively correlated with species asynchrony, species richness, and species diversity as well as the stability of dominant species and the stability of the grass functional group. Our data suggest a need to re-evaluate the mechanisms responsible for the effects of N deposition on natural ecosystem stability across multiple levels of N enrichment and that additional experimentation with gradients of N loads more similar to future atmospheric N deposition rates is needed.

Nutritional imbalance suppresses migratory phenotypes of the Mongolian locust (Oedaleus asiaticus).

For many species, migration evolves to allow organisms to access better resources. However, the proximate factors that trigger these developmental changes, and how and why these vary across species, remain poorly understood. One prominent hypothesis is that poor-quality food promotes development of migratory phenotypes and this has been clearly shown for some polyphenic insects. In other animals, particularly long-distance bird migrants, it is clear that high-quality food is required to prepare animals for a successful migration. We tested the effect of diet quality on the flight behaviour and morphology of the Mongolian locust, Oedaleus asiaticus. Locusts reared at high population density and fed low-N grass (performance-enhancing for this species) had enhanced migratory morphology relative to locusts fed high-N grass. Furthermore, locusts fed synthetic diets with an optimal 1 : 2 protein : carbohydrate ratio flew for longer times than locusts fed diets with lower or higher protein : carbohydrate ratios. In contrast to the hypothesis that performance-degrading food should enhance migration, our results support the more nuanced hypothesis that high-quality diets promote development of migratory characteristics when migration is physiologically challenging.

Dietary phosphate affects food selection, post-ingestive phosphorus fate, and performance of a polyphagous herbivore.

Comparisons of the carbon, nitrogen and phosphorus (P) content of plants and insect herbivores suggests that P limitation and herbivore foraging to balance P intake could be common. However, the lack of synthetic diets for testing the effects of lower ranges of dietary P has been a major impediment to experimental assessment of the ecological importance of, and physiological responses to, P limitation for terrestrial herbivores. We manipulated dietary P content (%P) over its observed range in terrestrial foliage using artificial diets containing near-optimal content of other nutrients for the grasshopper Schistocerca americana. Over much of the ecologically relevant range, when consuming single diets over a lifetime, higher P stimulated growth rates and increased survival, with an optimal dietary %P of 0.25-0.50% when measured throughout development. Excessive dietary P (1%) reduced growth and survival. However, with only short-term (3 day) confinement to single diets, dietary P had no effect on food consumption or growth rates. During these short exposures, fifth (but not third) instar hoppers increased the proportion of P excreted relative to P assimilated as dietary P increased. Target experiments demonstrated that, when given a choice, grasshoppers select among foods to attain a P intake target of 0.6%. These data suggest that P limitation could be common for terrestrial insect herbivores and that they can exhibit ingestive and post-ingestive mechanisms to attain sufficient but not excessive P.

Grasshoppers regulate N:p stoichiometric homeostasis by changing phosphorus contents in their frass.

Nitrogen (N) and phosphorus (P) are important limiting nutrients for plant production and consumer performance in a variety of ecosystems. As a result, the N:P stoichiometry of herbivores has received increased attention in ecology. However, the mechanisms by which herbivores maintain N:P stoichiometric homeostasis are poorly understood. Here, using a field manipulation experiment we show that the grasshopper Oedaleus asiaticus maintains strong N:P stoichiometric homeostasis regardless of whether grasshoppers were reared at low or high density. Grasshoppers maintained homeostasis by increasing P excretion when eating plants with higher P contents. However, while grasshoppers also maintained constant body N contents, we found no changes in N excretion in response to changing plant N content over the range measured. These results suggest that O. asiaticus maintains P homeostasis primarily by changing P absorption and excretion rates, but that other mechanisms may be more important for regulating N homeostasis. Our findings improve our understanding of consumer-driven P recycling and may help in understanding the factors affecting plant-herbivore interactions and ecosystem processes in grasslands.

Responses to capture stress and exogenous corticosterone vary with body condition in female red-sided garter snakes (Thamnophis sirtalis parietalis).

This study examined whether hormonal and behavioral responses to capture stress and exogenous corticosterone (CORT) vary with body condition in female red-sided garter snakes (Thamnophis sirtalis parietalis). Female snakes were collected during the spring mating season and treated with 4 h of capture stress. We measured plasma CORT and estradiol before, during and after capture stress treatment followed by latency to copulate, a measure of female receptivity. Body condition was determined as the residual from a regression of body mass on snout-vent-length. Baseline CORT did not differ between females in positive and negative body condition, but females in negative body condition showed a significantly larger increase in plasma CORT in response to capture stress. Estradiol, which is generally low during the mating season in this population, did not change in response to capture stress. Body condition, but not capture stress, influenced latency to copulate, suggesting that females are resistant to the behavioral effects of capture stress during the spring mating season. In a second experiment, only females in negative body condition increased latency to copulate in response to injection of a physiological (15 µg) dose of exogenous CORT, while all females responded to a pharmacological (60 µg) dose. These results indicate that behavioral responses to exogenous CORT vary with female body condition during the short mating season. Taken together, our data suggest that variation in body condition may be associated with differences in HPA axis sensitivity and/or glucocorticoid receptor density in the brain.

Efficient utilization of aerobic metabolism helps Tibetan locusts conquer hypoxia.

BACKGROUND: Responses to hypoxia have been investigated in many species; however, comparative studies between conspecific geographical populations at different altitudes are rare, especially for invertebrates. The migratory locust, Locusta migratoria, is widely distributed around the world, including on the high-altitude Tibetan Plateau (TP) and the low-altitude North China Plain (NP). TP locusts have inhabited Tibetan Plateau for over 34,000 years and thus probably have evolved superior capacity to cope with hypoxia. RESULTS: Here we compared the hypoxic responses of TP and NP locusts from morphological, behavioral, and physiological perspectives. We found that TP locusts were more tolerant of extreme hypoxia than NP locusts. To evaluate why TP locusts respond to extreme hypoxia differently from NP locusts, we subjected them to extreme hypoxia and compared their transcriptional responses. We found that the aerobic metabolism was less affected in TP locusts than in NP locusts. RNAi disruption of PDHE1ß, an entry gene from glycolysis to TCA cycle, increased the ratio of stupor in TP locusts and decreased the ATP content of TP locusts in hypoxia, confirming that aerobic metabolism is critical for TP locusts to maintain activity in hypoxia. CONCLUSIONS: Our results indicate that TP and NP locusts have undergone divergence in hypoxia tolerance. These findings also indicate that insects can adapt to hypoxic pressure by modulating basic metabolic processes.

Caterpillars selected for large body size and short development time are more susceptible to oxygen-related stress.

Recent studies suggest that higher growth rates may be associated with reduced capacities for stress tolerance and increased accumulated damage due to reactive oxygen species. We tested the response of Manduca sexta (Sphingidae) lines selected for large or small body size and short development time to hypoxia (10 kPa) and hyperoxia (25, 33, and 40 kPa); both hypoxia and hyperoxia reduce reproduction and oxygen levels over 33 kPa have been shown to increase oxidative damage in insects. Under normoxic (21 kPa) conditions, individuals from the large-selected (big-fast) line were larger and had faster growth rates, slightly longer developmental times, and reduced survival rates compared to individuals from a line selected for small size (small-fast) or an unselected control line. Individuals from the big-fast line exhibited greater negative responses to hyperoxia with greater reductions in juvenile and adult mass, growth rate, and survival than the other two lines. Hypoxia generally negatively affected survival and growth/size, but the lines responded similarly. These results are mostly consistent with the hypothesis that simultaneous acquisition of large body sizes and short development times leads to reduced capacities for coping with stressful conditions including oxidative damage. This result is of particular importance in that natural selection tends to decrease development time and increase body size.

How locusts breathe.

Insect tracheal-respiratory systems achieve high fluxes and great dynamic range with low energy requirements and could be important models for bioengineers interested in developing microfluidic systems. Recent advances suggest that insect cardiorespiratory systems have functional valves that permit compartmentalization with segment-specific pressures and flows and that system anatomy allows regional flows. Convection dominates over diffusion as a transport mechanism in the major tracheae, but Reynolds numbers suggest viscous effects remain important.

Heavy livestock grazing promotes locust outbreaks by lowering plant nitrogen content.

Current paradigms generally assume that increased plant nitrogen (N) should enhance herbivore performance by relieving protein limitation, increasing herbivorous insect populations. We show, in contrast to this scenario, that host plant N enrichment and high-protein artificial diets decreased the size and viability of Oedaleus asiaticus, a dominant locust of north Asian grasslands. This locust preferred plants with low N content and artificial diets with low protein and high carbohydrate content. Plant N content was lowest and locust abundance highest in heavily livestock-grazed fields where soils were N-depleted, likely due to enhanced erosion. These results suggest that heavy livestock grazing and consequent steppe degradation in the Eurasian grassland promote outbreaks of this locust by reducing plant protein content.

Are color or high rearing density related to migratory polyphenism in the band-winged grasshopper, Oedaleus asiaticus?

Locusts represent an impressive example of migratory polyphenism, with high densities triggering a switch from a solitarious, shorter dispersal range, and sometimes greenish phenotype to a gregarious and sometimes darker form exhibiting behavioral, morphological and physiological traits associated with long-distance migratory swarms. While such polyphenism has been well documented in Locusta migratoria and Schistocerca gregaria, the extent to which other grasshoppers exhibit this type of migratory polyphenism is unclear. Anecdotally, the Chinese grasshopper, Oedaleus asiaticus, forms migratory swarms comprised mostly of a darker, brown-colored morph, but also exhibits a non-migratory green-colored morph that predominates at low densities. In a population in Inner Mongolia not currently exhibiting migratory swarms, we found that while green and brown O. asiaticus are found concurrently across our sampled range, only brown grasshoppers were found in high densities. Differences between field-collected brown and green forms matched some but not key predictions associated with the hypothesis that the brown form is morphologically and physiologically specialized for gregarious migration. Controlling for body mass, brown forms had more massive thoraxes, abdomens and legs, and higher metabolic rates, but not more flight muscle or lipid stores. Further, the brown and green grasshoppers did not differ in gregarious behavior, and neither would fly in multiple lab and field trials. Lab or field-rearing at high densities for one-to-multiple juvenile instars caused grasshoppers to exhibit some morphological traits predicted to benefit migration (larger wings and a shift in relative mass from abdomen to thorax), but did not change color or induce flight behavior. One hypothesis to explain these data is that a migratory form of O. asiaticus is partially triggered by high field densities, but that existing ecological conditions blocked full expression of such traits (and outbreak swarms). Alternatively, color variation in this species may more tightly linked to other functions in this species such as crypsis or disease resistance, and mechanisms other than late-juvenile rearing density (e.g. genetic variation, maternal effects) may be more critical for promoting variation in color and/or migratory polyphenism.