RESUMO
Background: Managed populations of the alfalfa leafcutting bee (ALCB), Megachile rotundata (F.), are often not sustainable. In addition to numerous mortality factors that contribute to this, the dense bee populations used to maximize alfalfa pollination quickly deplete floral resources available to bees later in the summer. Providing alternative floral resources as alfalfa declines may help to improve ALCB reproduction. Methods: We examined the relationship between floral resource availability and ALCB reproduction and offspring condition via (1) a field study using alfalfa plots with and without late-blooming wildflower strips to supply food beyond alfalfa bloom, and (2) a field-cage study in which we provided bees with alfalfa, wildflowers, or both as food resources. Results: In the field study, bee cell production closely followed alfalfa floral density with an initial peak followed by large declines prior to wildflower bloom. Few bees visited wildflower strips, whose presence or absence was not associated with any measure of bee reproduction. However, we found that female offspring from cells provisioned earlier in the season, when alfalfa predominated as a source of provisions, eclosed with greater body sizes and proportion body lipids relative to total body mass. For bees restricted to cages, the proportion of offspring that survived to adults was highest on pure alfalfa diets. Adding wildflowers to cages with alfalfa did not affect adult offspring production or female offspring body size and lipid content. Furthermore, although similar numbers of adults were produced on wildflowers alone as with alfalfa alone, females eclosed with smaller body sizes and lower proportion body lipids on wildflowers despite the higher protein content we estimated for wildflower pollen. We found no evidence that adding the late-season wildflower species that we chose to plant enhanced ALCB offspring numbers. Our results highlight the importance of considering multiple measures of reproductive success, including offspring body size and lipid stores, when designing and evaluating floral resource management strategies for agroecosystems.
Assuntos
Flores , Medicago sativa , Polinização , Reprodução , Estações do Ano , Animais , Abelhas/fisiologia , Reprodução/fisiologia , FemininoRESUMO
We examined the relationship of post-diapause rearing temperature to developmental rate, survival, and adult body mass of the solitary wasp Isodontia elegans using prepupae from trap-nests. Isodontia elegans is a member of a genus often found in trap-nests in North America and Europe. Trap-nests are commonly used tools for studying cavity-nesting solitary wasps and bees. In temperate zones, progeny in nests usually overwinter as prepupae before pupating and emerging as adults. An important aspect of properly using trap-nests is determining temperatures that affect survival and health of developing offspring. After overwintering >600 cocoons containing prepupae after the summers of 2015 and 2016, we placed cocoons on a laboratory thermal gradient where offspring experienced one of 19 constant temperatures from 6 to 43 °C; emergence of adults was monitored for 100 days. Our conservative estimate for the critical thermal minimum for development is 14 °C, whereas that for the critical maximum is â¼33 °C. Prepupae transitioned to adults most rapidly at 29-33 °C, but developmental rate was lower for some progeny exposed to temperatures ≥30 °C. Offspring successfully reached the adult stage in <100 days at of temperatures of â¼19-33 °C. Adults from cocoons reared at lower temperatures weighed on average 6-10% more than expected based on their head widths, whereas those reared at higher temperatures weighed 4-10% less than expected. The difference may be due to greater rates of water loss and lipid metabolism during development at higher temperatures. Pre-overwintering cocoon mass was a significant predictor of relative adult body mass, indicating that adult health is partly related to their condition before overwintering. The trends we observed were similar to those for the bee Megachile rotundata, which we previously studied on the same gradient apparatus. However, data is needed on many other species of wasps and bees from a diversity of environments.
Assuntos
Diapausa , Animais , Feminino , Masculino , Caracteres Sexuais , Taxa de Sobrevida , Temperatura , Fatores de Tempo , Vespas/crescimento & desenvolvimento , EnvelhecimentoRESUMO
Background: Orchid bees are abundant and widespread in the Neotropics, where males are important pollinators of orchids they visit to collect fragrant chemicals later used to court females. Assemblages of orchid bees have been intensively surveyed in parts of Central America, but less so in Belize, where we studied them during the late-wet and early-dry seasons of 2015-2020. Methods: Using bottle-traps baited with chemicals known to attract a variety of orchid bee species, we conducted surveys at sites varying in latitude, historical annual precipitation, elevation, and the presence of nearby agricultural activities. Each sample during each survey period consisted of the same number of traps and the same set of chemical baits, their positions randomized along transects. Results: In 86 samples, we collected 24 species in four genera: Euglossa (16 species), Eulaema (3), Eufriesea (3), and Exaerete (2). During our most extensive sampling (December 2016-February 2017), species diversity was not correlated with latitude, precipitation, or elevation; species richness was correlated only with precipitation (positively). However, a canonical correspondence analysis indicated that species composition of assemblages varied across all three environmental gradients, with species like Eufriesea concava, Euglossa imperialis, and Euglossa viridissima most common in the drier north, and Euglossa ignita, Euglossa purpurea, and Eulaema meriana more so in the wetter southeast. Other species, such as Euglossa tridentata and Eulaema cingulata, were common throughout the area sampled. Mean species diversity was higher at sites with agricultural activities than at sites separated from agricultural areas. A Chao1 analysis suggests that other species should yet be found at our sites, a conclusion supported by records from adjacent countries, as well as the fact that we often added new species with repeated surveys of the same sites up through early 2020, and with the use of alternative baits. Additional species may be especially likely if sampling occurs outside of the months/seasons that we have sampled so far.
Assuntos
Himenópteros , Feminino , Masculino , Abelhas , Animais , Belize , Estações do Ano , América CentralRESUMO
Megachile rotundata (F.) is an important pollinator of alfalfa in the United States. Enhancing landscapes with wildflowers is a primary strategy for conserving pollinators and may improve the sustainability of M. rotundata. Changing cold storage temperatures from a traditionally static thermal regime (STR) to a fluctuating thermal regime (FTR) improves overwintering success and extends M. rotundata's shelf life and pollination window. Whether floral resources enhance overwintering survival and/or interact with a thermal regime are unknown. We tested the combined effects of enhancing alfalfa fields with wildflowers and thermal regime on survival and macronutrient stores under extended cold storage (i.e., beyond one season). Megachile rotundata adults were released in alfalfa plots with and without wildflower strips. Completed nests were harvested in September and stored in STR. After a year, cells were randomly assigned to remain in STR for 6 months or in FTR for a year of extended cold storage; emergence rates were observed monthly. Macronutrient levels of emerged females were assessed. FTR improved M. rotundata survival but there was no measurable effect of wildflower strips on overwintering success or nutrient stores. Timing of nest establishment emerged as a key factor: offspring produced late in the season had lower winter survival and dry body mass. Sugars and glycogen stores increased under FTR but not STR. Trehalose levels were similar across treatments. Total lipid stores depleted faster under FTR. While wildflowers did not improve M. rotundata survival, our findings provide mechanistic insight into benefits and potential costs of FTR for this important pollinator.
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Himenópteros , Feminino , Abelhas , Animais , Temperatura , Medicago sativa , Trealose , Nutrientes , Glicogênio , LipídeosRESUMO
The alfalfa leafcutting bee, Megachile rotundata (F.), contributes to the pollination of more than two-thirds of alfalfa used in seed production in North America. However, losses in managed populations of more than 50% are common in the United States. Thus, understanding the causes of mortality of M. rotundata is critical to find ways to maintain and increase bee populations. Over 2 yr, we identified and quantified six mortality classes of M. rotundata, as well as estimated mortality risk using the demographic life-table model, M-DEC. Research was conducted on an alfalfa field in Toston, Montana and offspring mortality was assessed in the fall of each year. Nest shelters were manipulated for a main temperature treatment (low vs high), and nest boxes inside the shelters were manipulated for a parasitism sub-treatment (parasitism-resistant vs parasitism-enabled). Total mortality was approximately 15% for both years, but the proportion for each mortality class differed substantially. Mortality increased with increasing internal nest-tunnel temperature, and nest boxes with parasitism-enabled entry had nearly double the mortality than those with parasitism-resistant entry. Based on demographic multiple decrement life table analyses, mortality from each class was highly irreplaceable. Identifying and quantifying irreplaceable mortality classes and strategies to mitigate those causes may help producers decrease total population loss of M. rotundata before the adult stage.
Assuntos
Himenópteros , Animais , Abelhas , Tábuas de Vida , Medicago sativa , Montana , América do Norte , SementesRESUMO
Improving pollinator habitat on farmlands is needed to further wild bee conservation and to sustain crop pollination in light of relationships between global declines in pollinators and reductions in floral resources. One management strategy gaining much attention is the use of wildflower strips planted alongside crops to provide supplemental floral resources for pollinators. However, farmer adoption of pollinator-friendly strategies has been minimal, likely due to uncertainty about costs and benefits of providing non-crop flowering plants for bees. Over 3 yr, on four diversified farms in Montana, United States, we estimated the potential economic profit of harvesting and selling wildflower seeds collected from flower strips implemented for wild bee conservation, as an incentive for farmers to adopt this management practice. We compared the potential profitability of selling small retail seed packets versus bulk wholesale seed. Our economic analyses indicated that potential revenue from retail seed sales exceeded the costs associated with establishing and maintaining wildflower strips after the second growing season. A wholesale approach, in contrast, resulted in considerable net economic losses. We provide proof-of-concept that, under retail scenarios, the sale of native wildflower seeds may provide an alternative economic benefit that, to our knowledge, remains unexplored. The retail seed-sales approach could encourage greater farmer adoption of wildflower strips as a pollinator-conservation strategy in agroecosystems. The approach could also fill a need for regionally produced, native wildflower seed for habitat restoration and landscaping aimed at conserving native plants and pollinators.
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Motivação , Polinização , Animais , Abelhas , Análise Custo-Benefício , Flores , Montana , SementesRESUMO
Terrestrial arthropods are a critical component of rangeland ecosystems that convert primary production into resources for higher trophic levels. During spring and summer, select arthropod taxa are the primary food of breeding prairie birds, of which many are imperiled in North America. Livestock grazing is globally the most widespread rangeland use and can affect arthropod communities directly or indirectly through herbivory. To examine effects of management on arthropod community structure and avian food availability, we studied ground-dwelling arthropods on grazed and ungrazed sagebrush rangelands of central Montana. From 2012 to 2015, samples were taken from lands managed as part of a rest-rotation grazing program and from idle lands where livestock grazing has been absent for over a decade. Bird-food arthropods were twice as prevalent in managed pastures despite the doubling of overall activity-density of arthropods in idle pastures. Activity-density on idled lands was largely driven by a tripling of detritivores and a doubling in predators. Predator community structure was simplified on idled lands, where Lycosid spiders increased by fivefold. In contrast, managed lands supported a more diverse assemblage of ground-dwelling arthropods, which may be particularly beneficial for birds in these landscapes if, for example, diversity promotes temporal stability in this critical food resource. Our results suggest that periodic disturbance may enhance arthropod diversity, and that birds may benefit from livestock grazing with periodic rest or deferment.
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Artrópodes , Animais , Aves , Ecossistema , Pradaria , Gado , Montana , América do NorteRESUMO
Industrialized farming practices result in simplified agricultural landscapes, reduced biodiversity, and degraded species-interaction networks. Thus far, most research assessing the combined effects of farming systems and landscape complexity on beneficial insects has been conducted in relatively diversified and mesic systems and may not represent the large-scale, monoculture-based dryland agriculture that dominates many regions worldwide. Specifically, the effects of farming systems on forbs, bees, and their interactions are poorly understood in highly simplified dryland landscapes such as those in the Northern Great Plains, United States, an area globally important for conventional and organic small grain, pulse, forage, and oilseed production. During a 3-yr (2013-2015) study, we assessed 1) the effects of dryland no-till conventional and tilled organic farming on forbs, bees, and bee-flower networks and 2) the relationship between natural habitat and bee abundance. Flower density and richness were greater in tilled organic fields than in no-till conventional fields, and forb community composition differed between farming systems. We observed high bee diversity (109 taxa) in this highly simplified landscape, and bee abundance, richness, and community composition were similar between systems. Compared with tilled organic fields, bee-flower interactions in no-till conventional fields were poorly connected, suggesting these systems maintain relatively impoverished plant-pollinator networks. Natural habitat (11% of the landscape) did not affect small-bodied bee abundance in either farming system but positively affected large-bodied bees within 2,000 m of crop-field centers. In highly simplified agricultural landscapes, dryland organic farming and no-till conventional farming together support relatively high bee diversity, presumably because dryland organic farming enhances floral resources and bee-flower networks, and no-till management in conventional farming provides undisturbed ground-nesting habitats for wild bees (Hymenoptera: Apoidea).
Assuntos
Agricultura , Agricultura Orgânica , Animais , Abelhas , Biodiversidade , Ecossistema , Flores , PolinizaçãoRESUMO
BACKGROUND: Over three years (2013-2015), we sampled bees using nets and bowl traps on four diversified vegetable farms in Gallatin County, Montana, USA, as part of a study evaluating the use of wildflower strips for supporting wild bees and crop pollination services on farmlands (Delphia et al. In prep). We document 202 species and morphospecies from 32 genera within five families, of which 25 species represent the first published state records for Montana. This study increases our overall understanding of the distribution of wild bee species associated with agroecosystems of the northern US Rockies, which is important for efforts aimed at conserving bee biodiversity and supporting sustainable crop pollination systems on farmlands. NEW INFORMATION: We provide a species list of wild bees associated with diversified farmlands in Montana and increase the number of published bee species records in the state from 374 to at least 399. The list includes new distributional records for 25 wild bee species, including two species that represent considerable expansions of their known ranges, Lasioglossum (Dialictus) clematisellum (Cockerell 1904) with previously published records from New Mexico, Arizona, California and Utah and Melissodes (Eumelissodes) niveus Robertson 1895 which was reported to range from New York to Minnesota and Kansas, south to North Carolina, Alabama and Mississippi.
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Current regulatory requirements for insecticide toxicity to nontarget insects focus on the honey bee, Apis mellifera (L.; Hymenoptera: Apidae), but this species cannot represent all insect pollinator species in terms of response to insecticides. Therefore, we characterized the toxicity of pyrethroid insecticides used for adult mosquito management (permethrin, deltamethrin, and etofenprox) on a nontarget insect, the adult alfalfa leafcutting bee, Megachile rotundata (F.; Hymenoptera: Megachilidae) in two separate studies. In the first study, the doses causing 50 and 90% mortality (LD50 and LD90, respectively) were used as endpoints and 2-d-old adult females were exposed to eight concentrations ranging from 0.0075 to 0.076 µg/bee for permethrin and etofenprox, and 0.0013-0.0075 µg/bee for deltamethrin. For the second study, respiration rates of female M. rotundata were also recorded for 2 h after bees were dosed at the LD50 values to give an indication of stress response. Results indicated a relatively similar LD50 for permethrin and etofenprox, 0.057 and 0.051 µg/bee, respectively, and a more toxic response, 0.0016 µg/bee for deltamethrin. Comparatively, female A. mellifera workers have a LD50 value of 0.024 µg/bee for permethrin and 0.015 µg/bee for etofenprox indicating that female M. rotundata are less susceptible to topical doses of these insecticides, except for deltamethrin, where both A. mellifera and M. rotundata have an identical LD50 of 0.0016 µg/bee. Respiration rates comparing each active ingredient to control groups, as well as rates between each active ingredient, were statistically different (P < 0.0001). The addition of these results to existing information on A. mellifera may provide more insights on how other economically beneficial and nontarget bees respond to pyrethroids.
Assuntos
Abelhas/efeitos dos fármacos , Inseticidas/toxicidade , Nitrilas/toxicidade , Permetrina/toxicidade , Piretrinas/toxicidade , Animais , Feminino , Testes de Toxicidade AgudaRESUMO
The alfalfa leafcutting bee, Megachile rotundata F. (Hymenoptera: Megachilidae), is one of the most intensively managed solitary bees and greatly contributes to alfalfa production in both the United States and Canada. Although production of certain commodities, especially alfalfa seed, has become increasingly dependent on this species' pollination proficiency, little information is known about how M. rotundata is affected by insecticide exposure. To better understand the risk posed to M. rotundata by the increasing use of insecticides to manage mosquitoes, we conducted field experiments that directly exposed M. rotundata nests, adults, and larvae to a pyrethroid insecticide via a ground-based ultra-low-volume (ULV) aerosol generator. We directly targeted nest shelters with Zenivex® E20 (etofenprox) at a half-maximum rate of 0.0032 kg/ha at dusk and then observed larval mortality, adult mortality, and the total number of completed nests for both the treated and control groups. There was no significant difference in the proportion of dead (P = 0.99) and alive (P = 0.23) larvae when the control group was compared with the treated group. We also did not observe a significant difference in the number of emerged adults reared from the treated shelters (P = 0.22 and 0.50 for females and males, respectively), and the number of completed cells after exposure to the insecticides continued to increase throughout the summer, indicating that provisioning adults were not affected by the insecticide treatment. The results from this study suggest that the amount of insecticide reaching nest shelters may not be sufficient to cause significant mortality.
Assuntos
Abelhas/efeitos dos fármacos , Inseticidas/efeitos adversos , Larva/efeitos dos fármacos , Piretrinas/efeitos adversos , Animais , Abelhas/crescimento & desenvolvimento , Abelhas/fisiologia , Larva/crescimento & desenvolvimento , Montana , Controle de MosquitosRESUMO
During the nesting season, adult females of the solitary bee Megachile rotundata (F.) face considerable physical and energy demands that could include increasing wear and tear on their bodies and decreasing lipid reserves. Consequently, their reproductive performance may be affected not only by extrinsic factors (e.g., weather and floral resource availability), but intrinsic changes in their own bodies. Because of the potential fitness effects of seasonal changes in body condition, our objectives were to determine how wing wear, lipid reserves, and oocyte sizes vary during nesting seasons, beginning when females emerge as adults. As nesting progressed, females in two populations experienced a steady increase in wing wear, which is known to reduce foraging efficiency and increase risk of mortality in other bees. Soon after emergence, females exhibited sharp declines in lipid content which remained low for the remainder of the season. Newly-emerged females ingested pollen, an activity known to be correlated with the initiation of egg maturation in this species. Additionally, the early summer drop in lipid stores was correlated with an increase in the size of the oocytes carried. However, by â¼6 weeks after emergence, oocytes began to decrease in length and volume, perhaps due to nutrient deficiencies related to loss of stored lipids. Our results suggest management of M. rotundata should include rearing bees at temperatures that maximize stored lipid reserves in adults and timing bee release so that significant pollen resources are available for both adults and offspring.
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Females of solitary, nest-provisioning bees have relatively low fecundity, but produce large eggs as part of their overall strategy of investing substantially in each offspring. In intraspecific comparisons of several species of solitary, nest-provisioning bees and wasps, the size of the mature eggs produced increases with female body size. We further examined oocyte size-body size correlations in the solitary bee Megachile rotundata (F.), an important crop pollinator. We hypothesized that larger females carry larger basal oocytes (i.e., those next in line to be oviposited) but that body size-oocyte size correlations would be absent soon after emergence, before their first eggs fully matured. Because egg production is likely affected by the quantity of stored lipids carried over from the bees' immature stages, we also tested the hypothesis that female body size is correlated with the body lipid content at adult emergence, the time during which oocyte growth accelerates. We found significant correlations of body size with oocyte size variables chosen to reflect: (1) the magnitude of the investment in the next egg to be laid (i.e., the length and volume of the basal oocyte) and (2) the longer term potential to produce mature oocytes (i.e., the summed lengths and volumes of the three largest oocytes in each female). Positive correlations existed throughout the nesting season, even during the first week following adult emergence. The ability to produce and carry larger oocytes may be linked to larger females starting the nesting season with greater lipid stores (which we document here) or to greater space within the abdomen of larger females. Compared to other species of solitary bees, M. rotundata appears to have (1) smaller oocytes than solitary nest-provisioning bees in general, (2) comparable oocyte sizes relative to congeners, and (3) larger oocytes than related brood parasitic megachilids.
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Temperature plays an important role in effective management of the alfalfa leafcutting bee [Megachile rotundata (F.); Megachilidae], the major commercial pollinator of seed alfalfa [Medicago sativa (L.); Fabaceae] in North America. To improve our understanding of threshold and optimum rearing temperatures of M. rotundata, we examined the effect of temperature on postwintering development by using a greater number of temperature treatments than applied in previous studies (19 versus eight or fewer) and analytical tools formulated to model nonlinear relationships between temperature and insect development rates. We also tested the hypothesis that rearing temperature influences adult body lipid content at emergence, which could affect adult survival, establishment and performance as a pollinator, and reproductive success. We found that the Lactin-2 and Briere-2 models provided the best fits to data and gave reasonable estimates of lower (16-18°C) and upper (36-39°C) developmental thresholds and optimum (33-34°C) rearing temperatures for maximizing development rate. Bees successfully emerged over a broad range of temperatures (22-35°C), but variation in development rate among individuals reared at the same temperature was lowest at 31-33°C. The optimum rearing temperature to maximize the proportion of body lipids in adults was 27-29°C. Our results are discussed in relation to previous findings and speak to the difficulties in designing practical rearing guidelines that simultaneously maximize development rate, survival, and adult condition, while synchronizing adult emergence with alfalfa bloom.
Assuntos
Abelhas/crescimento & desenvolvimento , Metabolismo dos Lipídeos , Temperatura , Animais , Abelhas/metabolismo , Tamanho Corporal , Feminino , Masculino , Análise de Regressão , Razão de MasculinidadeRESUMO
Livestock grazing can affect habitat quality for grasshoppers through effects on food and oviposition site availability, microclimate, and other factors. Because of this, some authors have suggested that grazing programs can be used to help manage pest grasshopper populations. In a 6-yr study, we controlled access of cattle to replicated experimental plots on an Agropyron spicatum/Poa sandbergii pasture to create consistent year-to-year differences in postgrazing plant cover, with resultant affects on microclimate. After sampling grasshoppers multiple times after grazing treatments each summer, we found evidence of between-treatment differences in grasshopper abundance for the entire assemblage during 4 of the 6 yr. Some species, including Melanoplus sanguinipes (perhaps the worse rangeland grasshopper pest in the western United States), tended to be more abundant on ungrazed plots, whereas Melanoplus gladstoni often had greater densities on heavily-grazed plots. The effect of grazing on grasshopper densities in this study was lower in magnitude and less consistent among years than in a study we conducted simultaneously at a nearby site where the vegetation was dominated by the exotic species crested wheatgrass (Agropyron cristatum). Our results generally support proposals that grazing could be used to reduce pest grasshopper densities, although the effectiveness of a particular grazing scheme may vary among sites, years, and grasshopper and vegetation assemblages.
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Bovinos , Gafanhotos , Criação de Animais Domésticos , Animais , Microclima , Montana , Plantas , Densidade DemográficaRESUMO
Miridae of the genera Labops and Irbisia, collectively referred to as "black grass bugs," can cause significant damage to wheatgrasses (Poaceae) of several genera on western North American rangeland. Another mirid in the same area, Capsus cinctus (Kolenati), causes damage to bluegrass (Poa spp.). Previous studies suggest that grazing management may reduce mirid populations on rangeland by eliminating preferred oviposition sites and reducing accumulations of litter that provide diurnal refuges for nymphs. We tested the hypothesis that grazing reduces mirid populations, along with those of Reduviidae, during a controlled grazing experiment. Densities of mirids and reduviids declined with increasing intensity of grazing, even though grazing occurred after the peak of mirid abundance each year. This suggests that declines in hemipteran densities resulted from grazing that occurred during previous years, perhaps because the most heavily grazed plots had the least plant litter. The results further confirm that grazing has the potential to control black grass bug populations, although the benefits could be potentially offset by negative impacts on beneficial insects such as reduviids.
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Bovinos , Hemípteros/fisiologia , Poaceae/parasitologia , Animais , Ecossistema , Comportamento Alimentar , Controle Biológico de Vetores , Fatores de TempoRESUMO
The short-term behavioral responses of adult grasshoppers, Melanoplus sanguinipes (F.) (Orthoptera: Acrididae), were examined after they experienced changes in microclimate when beingforced to change positions in their habitat. It was also determined if and when behavioral tactics allowed adults to achieve body temperatures within their preferred range. The preferred or set-point range, here taken as the interquartile range of temperatures selected on a laboratory thermal gradient, was estimated to be 37.4-40.5 degrees C. In the field, adults progressed through a relatively consistent daily sequence of behaviors, basking on the soil early in the day, but moving onto vegetation as temperatures increased. Although basking allowed grasshoppers to maximize body temperature within the available range, as much as 7 degrees C in excess of air temperature, they could not attain preferred body temperatures until soil surface temperatures reach about 35 degrees C. Basking was more effective in grazed than ungrazed pastures due to a lower degree of shading of the soil surface. As soil surface temperatures exceeded 35 degrees C, grasshoppers could achieve body temperatures within the preferred range by moving to the appropriate height on vegetation. These results illustrate the advantage of assessing behavior in the field in relation to preferred body temperatures determined in the laboratory.