When given a choice, most animals will self-select an optimal blend of nutrients that maximizes growth and reproduction (termed “intake target” or IT). For example, several grasshopper and locust species select a carbohydrate-biased IT, consuming up to double the amount of carbohydrate relative to protein, thereby increasing growth, survival, and migratory capacity. ITs are not static, and there is some evidence they can change through ontogeny, with activity, and in response to environmental factors. However, little research has investigated how these factors influence the relative need for different nutrients and how subsequent shifts in ITs affect the capacity of animals to acquire an optimal diet in nature. In this study, we determined the ITs of 5^th instar (final juvenile stage) Melanoplus sanguinipes (Fabricius, 1798), a prevalent crop and rangeland grasshopper pest in the United States, using two wild populations and one lab colony. We simultaneously collected host plants to determine the nutritional landscapes available to the wild populations and measured the performance of the lab colony on restricted diets. Overall, we found that the diet of the wild populations was more carbohydrate-biased than their lab counterparts, as has been found in other grasshopper species, and that their ITs closely matched their nutritional landscape. However, we also found that M. sanguinipes had the lowest performance metrics when feeding on the highest carbohydrate diets, whereas more balanced diets or protein-rich diets had higher performance metrics. This research may open avenues for studying how management strategies coincide with nutritional physiology to develop low-dose treatments specific to the nutritional landscape for the pest of interest.

geometric framework, macronutrient preference, nutritional ecology, nutritional landscape, plant–insect interactions, rangeland grasshopper

Rangelands in the western United States are important agricultural and environmental resources, serving not only as grazing lands for livestock, but also as habitats for wildlife (Havstad et al. 2007). While the U.S. has not been home to a locust species since the 1870s [the extinct Rocky Mountain locust, Melanoplus spretus (Walsh, 1866) (†), originally described within Caloptenus by Walsh in 1866, see Lockwood 2004], the rangelands are sometimes plagued by large grasshopper outbreaks (Capinera and Sechrist 1982, Joern and Gaines 1990, Schell and Lockwood 1997). Grasshoppers represent a significant problem for ranchers and farmers across the United States, but especially in the western rangelands (Hewitt and Onsager 1983). Grasshopper outbreaks can represent a significant economic hardship to ranchers, with conservative estimates placing the economic damage of grasshoppers at $393 million in rangeland forage lost annually (Hewitt and Onsager 1983). There is support for the use of fungal management for rangeland grasshoppers (Streett 1996–2000, Bidochka and Roberts 2000, Branson et al. 2006), and nutritional ecology can be helpful when applying these management strategies. However, few studies have bridged lab and field research to understand how the nutritional requirements of grasshoppers relate to the host plants available to them in the field.

In rangelands, the migratory grasshopper M. sanguinipes (Fabricius) is the most destructive grasshopper, causing more forage loss than any other grasshopper species in the United States (Pfadt 2002). This grasshopper is not exceptionally large, with a body length of approximately 16–23 mm for 5^th instars, 20–26 mm for adult males, and 20–29 mm for adult females (Pfadt 2002). Management of this species is particularly challenging because populations that emerge in rangelands can then migrate to croplands miles away. Due to their mixed (grasses and forbs) feeding behavior, they will consume vegetables in addition to cereal crops and grasses (Pfadt 2002, Murray 2016). Indeed, as described in COPR (1982), this species is “decidedly ambivorous” and will “devour and thrive on almost any available plant,” including plants from grasslands and crops to hedge mustard and moss. This grasshopper is especially problematic because of its large outbreak potential, with outbreak populations able to reach 80 individuals/yd² (Murray 2016). Due to its economic impact, M. sanguinipes has often been the subject of population management research (Pickford and Mukerji 1974, Hewitt 1977, Hewitt and Onsager 1983, Pfadt 2002), as well as nutritional and life history studies (Behmer and Joern 2008, Fielding and Defoliart 2008). However, there is still much unknown about this major rangeland pest species’ nutrient preferences in field populations and how those compare with long-term lab colonies.

When given a choice, most animals will self-select the blend of nutrients that maximizes growth and reproduction (termed “intake target” or IT), which arises from the Geometric Framework for Nutrition, or GFN (Raubenheimer and Simpson 1997, Raubenheimer et al. 2009, Simpson and Raubenheimer 2012). GFN research spans many taxa and has demonstrated that numerous insect populations, particularly lab colonies, exhibit a consistent IT. For example, Plutella xylostella (Linnaeus, 1758) caterpillars select a macronutrient ratio similar to ancestral colony conditions (3.25 mg protein: 3.00 mg carbohydrates), and that ratio corresponds with a narrow and high peak in performance (Warbrick-Smith et al. 2009). Several migratory grasshopper and locust species select a carbohydrate-biased IT, consuming up to double the amount of carbohydrate relative to protein, which increases growth, survival, and migratory capacity (Behmer and Joern 2008, Cease et al. 2012, 2017, Le Gall et al. 2019, Le Gall et al. 2020a, b, Talal et al. 2020).

ITs are dynamic, and there is some evidence they can shift through ontogeny, with activity, and in response to environmental factors (Raubenheimer and Simpson 1997, Simpson and Raubenheimer 2012, Lawton et al. 2020). There is also evidence that meeting an IT not only maximizes growth performance under optimal conditions, but also aids in survival when faced with toxins and pathogens. Helicoverpa armiger (Hübner, 1808) and Helicoverpa punctigera (Wallengren, 1860) caterpillars fed on diets that match their IT have lower susceptibility to several Bt toxins (Tessnow et al. 2018). Chortoicetes terminifera (Walker, 1870), the Australian plague locust, adjusts its IT when faced with a pathogen challenge, and the adjusted IT reduces the grasshopper’s susceptibility to the pathogen (Graham et al. 2014). Given how important external factors are on ITs, little research has investigated how these factors influence the relative need for different nutrients and how subsequent shifts in ITs affect the capacity of animals to acquire an optimal diet in nature.

The GFN has been used to analyze long-term and first-generation lab colonies of M. sanguinipes. For example, one lab study on 5^th instar first-generation lab-reared grasshoppers collected from Arapaho Prairie (Arthur Co., Nebraska) showed that M. sanguinipes had a 1:0.96 preferred dietary ratio of protein to carbohydrate (p:c) (Behmer and Joern 2008). Results from another study on two 2^nd generation lab populations of grasshoppers from Alaska (1p:0.90c) and Idaho (1p:0.95c) suggested that the ITs of both populations remained similar, though the Alaska population regulated more tightly than the Idaho grasshoppers (Fielding and Defoliart 2008). However, no studies have examined macronutrient preferences of M. sanguinipes collected directly from field populations. Understanding how an organism’s nutritional requirements compare to their habitat’s macronutrient composition can aid in developing management strategies based on nutrition (e.g., Cease et al. 2015, Le Gall and Tooker 2017, Word et al. 2019, Le Gall et al. 2020a).

The primary goals of this study were to 1) compare the IT of two field populations of M. sanguinipes to their given nutritional landscape, 2) compare the IT of these two field populations to the IT of a long-term lab colony, and 3) determine if the lab colony IT maximized performance by restricting grasshoppers to one of five diets varying in p:c ratio. Our null prediction was that a given field population of grasshoppers would have an IT that roughly matched the protein and carbohydrate ratios of plants available to them. We predicted that, relative to the long-term lab colony, the field populations would be more carbohydrate-biased, similar to other field populations of migratory acridids (Cease et al. 2012, Le Gall et al. 2020b, Lawton et al. 2021), perhaps due to increased activity or stressors. Finally, we hypothesized that grasshoppers select a diet that provides optimal performance and, thus, predicted that the p:c ratio of the diet on which the lab colony performed the best in restricted diet experiments would be similar to the lab colony IT.

Our long-term lab colony selected a balanced 1p:1c IT, which is similar to previous studies using first (1p:0.96c; Behmer and Joern 2008) and second (1p:0.90c and 1p:0.95c; Fielding and Defoliart 2008) generation lab-reared M. sanguinipes. Our lab colony performance experiments supported our hypothesis that M. sanguinipes selects an IT range that aligns with high performance, similar to Behmer and Joern (2008) and Fielding and Defoliart (2008). In contrast with the lab populations, we found that M. sanguinipes collected directly from field populations had carbohydrate-biased ITs (1p:2.1c and 1p:3.5c). The field populations may have shifted their ITs to better match their nutritional landscape and/or in response to disease, elevated activity, or other environmental factors (Fig. 2). For example, the Boise landscape had a higher representation of forbs than Bliss, ID, which may have contributed to the slightly less carbohydrate-biased IT of that population (Table 1); further studies are needed to disentangle these potential hypotheses. Understanding how these factors impact ITs will be key to predicting the nutritional physiology of these organisms in different environments, which, in turn, may assist in the development of novel management methods.

There is some evidence from lab-based experiments that populations either adapt or acclimate to their nutritional environment by matching their IT and performance to their ancestral diet (Raubenheimer et al. 2012). For instance, as mentioned briefly earlier, P. xylostella moths reared on a single homogenous food with a fixed nutrient composition for about 350 generations exhibited a strong selection for the same nutrient balance as their ancestral colony diet and had a sharp decline in performance when they deviated from that macronutrient balance, showing an extreme food specialization (Warbrick-Smith et al. 2009). A prior study reared the same species for multiple generations on either carbohydrate-rich or poor foods. The selected lines developed the capacity to minimize or maximize body fat accumulation to improve fitness when confined to their treatment diet (Warbrick-Smith et al. 2006). The diets did impact host plant preference for egg laying, but the authors did not test whether the selection experiment shifted ITs.

Results from field-based research, on the other hand, suggest that aligning ITs and performance to match the nutritional landscape is uncommon in the absence of long-term specialization and that physiological status is a better predictor of IT than ambient plant nutrient contents. For example, in West Africa, Oedaleus senegalensis (Krauss, 1877), the Senegalese grasshopper, did not shift its IT to match seasonal shifts in plant p:c; instead, ITs correlated poorly with plant nutrients and varied with age and sex (Le Gall et al. 2021). In Australia, a comparison of a non-migratory and two migratory grasshopper species through space and time revealed that populations of the non-migratory grasshopper had different ITs through space, but it was likely to redress nutrient imbalances from the local environment rather than to match them (Lawton et al. 2021). The migratory species largely maintained the same IT, even when there was a mismatch between their IT and their nutritional landscape, similar to Senegalese grasshoppers (also a migratory species).

In Paraguay, field populations of Schistocerca cancellata (Serville, 1838), the South American locust, maintained a carbohydrate-biased IT and only gained mass when fed the most carbohydrate-biased plants, despite being in a quite protein-biased landscape (Talal et al. 2020). This result corroborates earlier research indicating that locusts and migratory grasshoppers require a carbohydrate-biased diet to undergo long-distance migration (Cease et al. 2017) and that low p: high c environments support population growth (Cease et al. 2012, Word et al. 2019, Le Gall et al. 2020a, b). In the face of shifting environments, organisms and populations will acclimate, evolve, move, or perish. Collectively, these studies suggest that migratory species may rely on migration or post-ingestive mechanisms to regulate nutrient balance in the face of environmental change and that physiological constraints in nature limit matching a population’s IT to its nutritional landscape except when under strong selection.

The current study using the migratory grasshopper provides some support for both non-mutually exclusive hypotheses: that population IT is shaped by local nutritional landscape and by physiological status. Under standard rearing conditions, the colony has ad libitum access to foods encompassing a broad macronutrient range: wheat seedlings (1.9p:1c), romaine lettuce (1p:2.6c), and wheat bran (1p:4.1c) (Brosemann et al. unpubl.; FoodData Central 2021a). Therefore, it is unlikely that there was strong selective pressure to develop a narrow IT based on the lab diet, in contrast to the long-term moth colony reared on a single food choice (Warbrick-Smith et al. 2009). The lab colony likely arrived at a 1p:1c IT (Fig. 1) because it maximizes performance in a lab colony. While there was not a narrow performance peak, the IT was within the range where the lab colony maintained a high growth rate and fast development time across the 1:1, 1:2, 2:1, and 5:1 p:c diets (Fig. 3).

The field populations both had carbohydrate-biased ITs that matched their local environments. Although the 1p:2c Boise population IT could have been reached based on the plants available in both field environments, the 1p:3c IT that the Bliss population selected could only have readily been reached in the Bliss location (Fig. 2). Furthermore, neither field environment would have supported populations to select for the 1p:1c IT that the lab population selected. The Boise location had an average of 25% forb ground cover, and the Bliss location had <1% (Table 1), indicating that the few forbs closer to 1p:1c were sparse in the landscape and that the Bliss population was in an extremely carbohydrate-biased landscape. Therefore, it is possible that the grasshopper field populations, particularly for Bliss, were under some selective pressure to have carbohydrate-biased ITs to align with their nutritional landscape. However, all tests of lab colony ITs of M. sanguinipes nymphs performed to date resulted in a narrow range (1p:0.90c to 1p:1c) regardless of being first or second generation, being in a colony since 1970, or being originally collected from Alaska, Idaho, Nebraska, or Arizona (Behmer and Joern 2008, Fielding and Defoliart 2008; Fig. 1). Therefore, it is unlikely that the alignment between IT and local plant nutrients that we measured in this study represents local adaptation, though it could be evidence of an evolved ability to plastically respond to a restricted diet.

Many environmental factors can influence herbivore physiology and result in shifting the IT, such as activity level and pathogens. For example, Locust migratoria (Linnaeus, 1758), the migratory locust, increased carbohydrate, but not protein, consumption following 120 min of tethered flight (Raubenheimer and Simpson 1999). Nutrient balance affects insect immune function, and thus their ability to survive sickness and infections (Ponton et al. 2011a, b; Graham et al. 2014, Deans et al. 2017). Different immune components may be heightened by diets with different macronutrient contents, as was the case for Spodoptera littoralis (Boisduval, 1833) caterpillars (Cotter et al. 2011). Furthermore, Graham et al. (2014) found that Australian plague locusts that selected more carbohydrate-biased diets were better able to fight infections from the fungal pathogen Metarhizium. ITs that are highly carbohydrate-biased, such as we observed in our study’s Bliss, ID population, could be indicative of grasshoppers selecting this diet to fight sickness or infection. Indeed, we found that the Bliss population suffered significant mortality during the experiment and prior to the start of the experiment. When we completed the setup of the Bliss population experiment, approximately 30% of the grasshoppers we had collected the previous day were dead. The Bliss population also had more cases of grasshoppers losing mass than the Boise population. While not conclusive, these signs indicate that the population may have been suffering from pathogens or parasites. Further studies on field populations are needed to determine if the selected ITs maximize performance in those conditions, as well as the potential mechanisms driving variation in population ITs. However, our data suggest that, at least for these populations, they could achieve their preferred p:c ratio locally.

Understanding the nutritional requirements of rangeland grasshoppers is important not only for understanding what types of vegetation grasshoppers will be most likely to eat but also for developing novel management strategies. For example, the balance of macronutrients is important for immune function in insects and may be important to consider when biopesticides are used for management (Lee et al. 2008, Ponton et al. 2011a, b, Deans et al. 2017, Tessnow et al. 2018). Insects that can meet their ITs in their nutritional landscapes are likely to be less susceptible to biological control strategies—either less susceptible to pathogens or less susceptible to toxins produced by the biological control agent (Graham et al. 2014, Deans et al. 2017, Tessnow et al. 2018). There is evidence that for some insects, nutritional physiology differs between populations. Research on Spodoptera frugiperda (J.E. Smith, 1797), studying its susceptibility to Bt toxins, showed that for one population, meeting the IT actually increased that population’s susceptibility to the toxins. In the other two populations, eating at the IT did not affect individuals’ susceptibility to the toxins (Tessnow et al. 2021). This suggests that not only will there be differences in how IT relates to performance and survival between species, but there could also be differences among populations, so analyzing populations’ nutritional physiology and ecology is critical to any management strategy. Understanding how the nutritional landscape interacts with an organism’s IT and macronutrient requirements is going to be important, especially with more farmers and ranchers turning to biopesticides as means of managing grasshopper outbreaks (Gardner and Thomas 2002). Similar to how there are recommended temperature ranges across which biopesticides are most effective (McNeill and Hurst 2008, Rai et al. 2014, Kim et al. 2019), there should be guidance as to what types of nutritional landscapes will make pests most susceptible to biopesticides.

Another aspect to consider is how biopesticide treatment might affect pest host plant preference, as it could cause the target pests to consume crops and other plants it might not normally otherwise. Biopesticides aside, knowing how pests respond to nutritional landscapes can open pathways for population suppression through agricultural practices. For example, for locusts and migratory grasshoppers that thrive in low nitrogen environments (Cease et al. 2012, Word et al. 2019), the nutritional landscape could be altered through soil amendments, crop rotations, or other practices that increase soil organic matter and nitrogen availability; this would, in turn, increase the plant protein: carbohydrate ratio and suppress pest populations (Cease et al. 2015, Word et al. 2019). To support the development of sustainable management options, future research should study how biopesticide challenges affect the nutritional demands of M. sanguinipes and if this species can alter its diet to decrease its susceptibility. As with the Australian plague locust, such research would add greater understanding to the potential relationship between the nutritional physiology of grasshoppers and biopesticide efficacy, leading to more diverse, sustainable, and efficient management options.

Special acknowledgments to Lori Atkins in Boise, Idaho for the use of her property for running the field experiments; Brad Newbry of the United States Department of Agriculture’s Animal and Plant Health Inspection Service (APHIS) Plant Protection and Quarantine (PPQ) Field Operations in Idaho for grasshopper field survey information; Dustin Grief, who helped with running some experiments; the Cease Lab, Arizona State University; the Global Locust Initiative; and Mark Tubbs of Tubbs Land and Cattle LLC in South Dakota for graciously allowing us to use his ranch for a test run of the field population studies. This material was made possible, in part, by a Cooperative Agreement (AP17PPQS&T00C180) from USDA APHIS. It may not necessarily express APHIS’ views.