First record on epizootics of Entomophthora grylli on grasshopper in Indian subcontinent: pathogen city and bio control potential on Oxya velox

A naturally-occurring fungus called Entomophthora grylli was for the first time isolated from two species of grasshopper Oxya velox and Oxya vicinia in Jammu and Kashmir, India. The epizootic was confined along Indo–Pak border between 74 degrees 24′ and 75 degrees 18′, East longitude and 32 degrees 50′ and 33 degrees 30′ North latitude. The fungus proved to be highly pathogenic and the natural mortality was significantly influenced by the population density which increased from 26.00 to 73.60 over the period of epizootics. On the basis of the available literature this appears to be the first record from the Indian sub-continent. While many infected grasshoppers apparently produced neither conidia nor resting spores, the cadavers were found to be full of hyphal bodies and resting spores towards the end of epizootics. These resting spores or their germ tubes were not invasive as such but if provided a saturated environment for a week, they start germinating, resulting in germ conidia which were able to induce dermal pathogencity. Further, it was observed that the disease could not be transmitted to healthy individuals by ingestion. However, the intra-haemocoel infectivity of fresh resting spores, germinated resting spores, and germ conidia proved to be highly pathogenic as they resulted in 81.4% grasshopper mortality. Although E. grylli is fastidious, it is possible to multiply it on a large scale as protoplasts which are infective upon injection in their hosts. However, the lack of a cell wall renders them very fragile, and they are neither infective upon application to the insect's cuticle nor upon ingestion. In the present study, a method on delivery of pathogen through “sticky molasses pan trap” was developed for inducing infection in grasshoppers in a paddy nursery which would facilitate its use as a bioinsecticide, analogous to other entomopathogenic fungi.     

Natural levels of fungal infections in grasshoppers in Northern Benin

The infection of grasshoppers by naturally occurring, entomopathogenic fungi was monitored at two sites in Malanville, northern Benin, Africa. Grasshoppers were collected and recorded from the sites between June and December 1992 and all of them, barring the first instars, were incubated in ventilated cages. At the first site, 1343 individuals of 35 grasshopper species were incubated, and at the second site, 857 individuals of 36 grasshopper species were incubated. Three hyphomycete fungi (Deuteromycotina: Hyphomycetes), Metarhizium flavoviride Gams and Rozsypal, Beauveria bassiana (Bals.) Vuillemin and Sorosporella sp. were found infecting grasshoppers. The average incidence of M. flavoviride infection was 2.9% and 1.8% at the two sites for all host species. M. flavoviride sporulated on most grasshopper cadavers within 10 days of collection. B. bassiana and Sorosporella sp. were only collected from one and five grasshopper individuals respectively. A significant difference was noted in the time to death of small grasshopper species infected with M. flavoviride compared to larger species. At one site, M. flavoviride infection was positively correlated with rainfall during the 10‐day period in which samples were taken.     

Isolation and growth of the grasshopper pathogen, Entomophthora grylli

Entomophthora grylli was isolated and grown in pure culture in protoplast form. Cultures were obtained by germinating conidia collected from naturally infected adult Carolina grasshoppers, Dissosteira carolina, in Grace's tissue culture medium supplemented with 5% fetal bovine serum and an aqueous extract of grasshopper tissue. Grasshopper extract was not necessary for subsequent growth and subculture of the protoplasts. Healthy adult grasshoppers could be reinfected with the fungus by injection of a protoplast suspension.     

Operational-scale application of entomopathogenic fungi for control of Sahelian grasshoppers

Locusts and grasshoppers regularly threaten agricultural production across large parts of the developed and developing worlds. Recent concerns over the health and environmental impacts of standard chemical control measures have led to a demand for alternative, more environmentally benign control technologies. Here we present the results of a field study to investigate the potential of inundative biological control for control of grasshoppers in the Sahelian region of Africa. The biocontrol agent was an oil-based biopesticide formulation of a naturally occurring entomopathogenic fungus, Metarhizium flavoviride. This was applied at a rate of 2l ha^-1 to a total area of 150 ha using standard equipment normally used for the application of chemical pesticides. Twenty-one days after application, an 80 per cent reduction in grasshopper populations was recorded in treated plots, relative to control populations in equivalent unsprayed areas. We think that this is the first operational-scale application of a biopesticide to demonstrate significant population reductions of key Sahelian grasshopper pests. This represents a substantial development in locust and grasshopper control, and should open the way for a new era of integrated control strategies where reliance on conventional chemicals is reduced.     

Endophyte-grass-herbivore interactions: the case of Neotyphodium endophytes in Arizona fescue populations

Neotyphodium endophytes in introduced agronomic grasses are well known to increase resistance to herbivores, but little is known of interactions between Neotyphodium endophytes and herbivores in native grass populations. We investigated whether endophytes mediate plant-herbivore interactions in a native grass species, Festuca arizonica in the southwestern United States, in two ways. First, to test the prediction that the presence and frequency of endophyte-infected (E+) plants should increase with increasing herbivory, we determined endophyte frequencies over a 4-year period in six natural Arizona fescue populations. We compared Neotyphodium frequency among plants growing inside and outside long-term vertebrate grazing exclosures. Second, we experimentally tested the effects of Neotyphodium infection, plant clone, and soil nutrients on plant resistance to the native grasshopper Xanthippus corallipes. Contrary to predictions based upon the hypothesis that endophytes increase herbivore resistance, levels of infection did not increase in plants subjected to grazing outside of exclosures relative to ungrazed plants within exclosures. Instead, endophyte frequencies tended to be greater inside the exclosures, where long-term vertebrate grazing was reduced. The grasshopper bioassay experiment corroborated these long-term patterns. Survival of grasshoppers did not differ between infected (E+) and uninfected (E–) plants. Instead, mean relative growth rate of grasshoppers was higher on E+ grasses than on E– ones. Growth performance of newly hatched grasshopper nymphs varied among host plant clones, although two of six clones accounted for most of this variation. Our results suggest that Neotyphodium-grass-herbivore interactions may be much more variable in natural communities than predicted by studies of agronomically important Neotyphodium-grass associations, and herbivory is not always the driving selective force in endophyte-grass ecology and evolution. Thus, alternative hypotheses are necessary to explain the wide distribution and variable frequencies of endophytes in natural plant populations. Received: 15 February 1999 / Accepted: 19 July 1999     

Natural Incidence of Metarhizium flavoviride Infection in Two Grasshopper Communities in Northern Benin

The infection of grasshoppers by naturally occurring entomopathogenic fungi was monitored at two sites in Malanville, northern Benin, Africa. Grasshoppers were collected during the monsoon seasons of 1993, 1994 and 1995. At the first site, 982 individuals of 38 grasshopper species were incubated. At the second site, 899 individuals of 33 grasshopper species were incubated. Two hyphomycete fungi (Deuteromycotina: Hyphomycetes), Metarhizium flavoviride Gams and Rozsypal and Sorosporella sp., were found infecting grasshoppers. The mean incidence of M. flavoviride infection was 0.3-1.7% at the first site and 1.2-3.2% at the second site for all grasshopper species. Sorosporella sp. was only collected from two grasshopper individuals in 1993. The majority of infected species had adult quiescence or continuously reproducing life cycles, and were either arboricolous or terricolous. Comparisons are made with a previous study of the two sites performed during 1992.     

Dynamics of two Montana grasshopper populations: relationships among weather,food abundance and intraspecific competition

The population dynamics of two grasshoppers (Melanoplus femurrubrum and M. sanguinipes) were studied using experimental microcosms over 8 years at a Palouse prairie site in Montana. Grasshopper density, survival and reproduction in the experimental populations responded in a density-dependent fashion to natural and experimental changes in food availability for all grasshopper developmental stages, both within and between all years. We observed that field populations of the grasshoppers at the site exhibited density, survival and reproductive responses similar to the experimental populations over the period of the study. Because we could not identify any differences between the field and microcosm environments or the grasshopper individuals in them, we contend that field populations were ultimately limited by food within and between years. Density-dependent food limitation occurred for all age categories over the entire summer, because food abundance declined relative to grasshopper food requirements over the summer. Food limitation occurred between years, because in years with the lowest food abundance, the populations produced more hatchlings for the next year than could be supported by the highest observed food abundance. Finally, the observed annual changes in food abundance were correlated with the annual variation in weather (rainfall and temperature), which indicated that the long established relationship between grasshopper densities and weather conditions does not imply population limitation by density-independent processes.     

Susceptibility of Bufonacris claraziana (Orthoptera: Tristiridae) to Beauveria bassiana (Ascomycota: Hypocreales) under controlled conditions

Bufonacris claraziana outbreaks, an endemic grasshopper of Argentinian Patagonia, are a recurrent phenomenon in that region, causing severe damage to forage. The aim of this study was to evaluate the susceptibility of B. claraziana to different strains of the entomopathogenic fungus Beauveria bassiana under laboratory conditions. The strains tested were LPSc 1225, LPSc 1226, and LPSc 1227. Percentage of mortality was 100% for all three strains, a significant difference was registered with the control where mortality was from 26.66?±?2.76%. Results obtained represent a first contribution on the use of an entomopathogenic microorganism as a potential biocontrol agent of this species.     

The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe

Gypsy moth, Lymantria dispar L., is one of the most important pests of deciduous trees in Europe. In regular cycles, it causes large‐scale defoliation mostly of oak, Quercus spp., forests. Government authorities in the most infested countries in Europe conduct large‐scale applications of pesticides against gypsy moth. In 1999, a new natural enemy, the entomopathogenic fungus Entomophaga maimaiga, was successfully introduced into a gypsy moth population in Bulgaria. Recent investigations suggest that now E. maimaiga is quickly spreading in Europe. Herein, past studies are reviewed regarding this fungus with special emphasis on its potential for becoming an important factor regulating gypsy moth populations in Europe, focusing on the host's population dynamics in relation to the fungus, the influence of environmental conditions on fungal activity, the influence of E. maimaiga on the native entomofauna, including other gypsy moth natural enemies, and spread of the fungus. Based on this analysis, the potential of E. maimaiga for providing control in European gypsy moth populations is estimated.     

Epizootics and behavioral alteration in the arctiid caterpillar Chionarctia nivea (Lepidoptera: Arctiidae) caused by an entomopathogenic fungus, Entomophaga aulicae (Zygomycetes: Entomophthorales)

We observed epizootics and behavioral alteration in the arctiid caterpillar Chionarctia nivea after infection by an entomopathogenic fungus, Entomophaga aulicae, in April at a riverbank in Kyoto Prefecture, central Japan. The density of arctiid cadavers infected with E. aulicae was 1.31 individuals/m². The critically ill caterpillars crawled up the dead stems of grasses and herbs such as the common reed Phragmites communis and the Japanese mugwort Artemisia indica var. maximowiczii to die at and near the highest parts of the stems, while the healthy larvae usually wandered on the ground and fed on the leaves of small herbs. This behavioral difference could be caused by infection with E. aulicae to enhance dispersal of conidia by active discharge in Entomophthorales with the aid of wind and rainfall.     

Cellular and humoral immune defenses of Oxya japonica (Orthoptera: Acrididae) to entomopathogenic fungi Metarhizium anisopliae

One Indonesian isolate of the fungus Metarhizium anisopliae, named Majalengka strain, was evaluated not only for its virulence but also for the immune response of rice grasshopper Oxya japonica (Orthoptera: Acrididae) as a target organism. Five aqueous suspensions with different conidia concentrations in logarithmic series were prepared. The fungus showed high virulence as it caused 100% mortality at low conidia concentration (1.5 × 10² conidia/mL). Remarkable changes in the cellular and humoral responses were also observed when adult grasshoppers were infected with the fungus. The number of hemocytes decreased significantly within 12 h after infection. In addition, the total number of granulocytes increased rapidly in the first 12 h then gradually decreased 24 and 48 h after infections, while the number of coagulocytes fluctuated over time. The infection influenced the humoral response by increasing the phenoloxidase activity.     

Thermal ecology of Zonocerus variegatus and its effects on biocontrol using pathogens

1 Thermal behaviour of the variegated grasshopper, Zonocerus variegatus, was investigated in the humid tropical zone of southern Benin, west Africa, in the dry seasons of 1996 and 1998. In 1998, investigations included studies of a population of grasshoppers sprayed with an oil‐based formulation of the entomopathogenic fungus Metarhizium anisopliae var acridum. 2 Body temperature measurements and observations of thermal behaviour both in the field and on thermal gradients in the laboratory, suggest that Z. variegatus was not an active behavioural thermoregulator. Although it did show shade‐seeking behaviour at high temperatures, no overt behavioural postures or microhabitat selection associated with heat gain and elevation of body temperatures was observed. Moreover, no alterations to thermal behaviour were found in response to infection by Metarhizium. 3 Body temperatures exhibited by Z. variegatus in the field will lengthen disease incubation of M. anisopliae var acridum compared with laboratory maintained, constant temperature conditions and may have a significant impact on pathogens with a lower thermal tolerance. 4 Habitat structure appeared to be an important factor determining the extent of body temperature elevation. The effect of habitat differences on infection and growth of M. anisopliae var acridum and other entomopathogenic fungi is discussed.     

黑河上游天然草地蝗虫空间异质性与分布格局

蝗虫空间分布格局是物种长期适应自然的结果,是蝗虫与环境、蝗虫之间关系的反映,有助于理解蝗虫发生学的环境背景。采用地统计学方法,在黑河上游山区天然草地研究了微生境影响下的蝗虫空间格局与异质性。结果表明:该区域5种优势种蝗虫的半变异函数模型均为非线性模型,表现为聚集分布;不同种类蝗虫样点之间空间依赖的范围为2.29—24.59 m;在蝗虫种群总异质性中随机部分引起的空间异质性占15.77%—88.64%。受食性和栖息地选择的影响,蝗虫种群形成了片状和斑块状的分布格局;尺度依赖性使蝗虫分布格局趋于多元化和繁杂化的特点,不同蝗虫种群之间相互交错嵌插,同种蝗虫高低值呈非均匀扩散,整体上形成了均衡性与互补性的斑块镶嵌结构,这种分布格局反映了蝗虫对生境和气候变化的多元适应性结构。     

Body size influences differently the detectabilities of colour morphs of cryptic prey

Body size and coloration may contribute to variation in performance and fitness among individuals; for example, by influencing vulnerability to predators. Yet, the combined effect of size and colour pattern on susceptibility to visual predators has received little attention, particularly in camouflaged prey. In the colour polymorphic pygmy grasshopper Tetrix subulata (Linnaeus, 1758), females are larger than males, although there is a size overlap between sexes. In the present study, we investigated how body size and colour morph influenced detection of these grasshoppers, and whether differences in protective value among morphs change with size. We conducted a computer‐based experiment and compared how human ‘predators’ detected images of large, intermediate or small grasshoppers belonging to black, grey or striped colour morphs when embedded in photographs of natural grasshopper habitats. We found that time to detection increased with decreasing size, that differences in time to detection of the black, grey and striped morphs depended differently on body size, and that no single morph provided superior or inferior protection in all three size classes. By comparing morph frequencies in samples of male and female grasshoppers from natural populations, we also examined whether the joint effects of size and colour morph on detection could explain evolutionary dynamics in the wild. Morph frequency differences between sexes were largely in accordance with expectations from the results of the detection experiment. The results of the present study demonstrate that body size and colour morph can interactively influence detection of camouflaged prey. This may contribute to the morph frequency differences between male and female pygmy grasshoppers in the wild. Such interactive effects may also influence the dynamics of colour polymorphisms, and contribute to the evolution of ontogenetic colour change and sexual dichromatism. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 112–122.     

Insect herbivory and vertebrate grazing impact food limitation and grasshopper populations during a severe outbreak

1. Competition between herbivores often plays an important role in population ecology and appears strongest when densities are high or plant production is low. Phytophagous insects are often highly abundant, but relatively few experiments have examined competition between vertebrates and phytophagous insects. 2. In grassland systems worldwide, grasshoppers are often the dominant phytophagous insect, and livestock grazing is a dominant land use. For this study, a novel experiment was conducted examining competition between vertebrates and invertebrates, where both grasshopper densities and sheep grazing were manipulated inside 10‐m² caged mesocosms during a grasshopper outbreak. We examined how grasshopper densities and the timing of vertebrate herbivory affected grasshopper densities, if the effects of vertebrates on survival and reproduction changed with grasshopper density, and how a naturally occurring grasshopper outbreak affected grasshopper populations in the following year. 3. Densities of grasshoppers at the site peaked at 130 m^–2. Food‐limited competition was stronger in treatments with higher grasshopper densities and repeated or late livestock herbivory, leading to reduced survival, femur length, and functional ovarioles, a measure of future reproduction. Strong food‐limited density‐dependent reproduction and survival led to reduced hatching densities in 2001. 4. As competition was typically stronger with high grasshopper densities than with livestock grazing, competition from vertebrates could be relatively less important for phytophagous insect population dynamics during outbreaks. The experiment provides insights into how competition between insect and vertebrate herbivores influences insect population dynamics, and indicates that severe outbreaks can rapidly subside with strong competition from vertebrate and insect herbivores.     

Discovery of a North American genetic variant of the entomopathogenic fungus <Emphasis Type="Italic">Metarhizium anisopliae</Emphasis> var. <Emphasis Type="Italic">anisopliae</Emphasis> pathogenic to grasshoppers

A genetic variant of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae, isolated from a soil in Alberta, Canada, from a location with a history of severe grasshopper infestations, was evaluated for pathogenicity in bioassays of living grasshoppers. Mortality in treated individuals drawn from a laboratory colony was 99% (LT₅₀ = 6.7 days, LT₉₀ = 9.6 days) at 12 days post-inoculation compared to 100% (LT₅₀ = 4.1 days, LT₉₀ = 5.8 days) mortality at 8 days in insects exposed to a commercial isolate of M. anisopliae var. acridum (IMI 330189). Experimental infection of field-collected grasshoppers under laboratory conditions with the native isolate of M. anisopliae var. anisopliae resulted in 100% (LT₅₀ = 4.4 days, LT₉₀ = 5.4 days) mortality attained within 7 days compared to 100% (LT₅₀ = 4.7 days, LT₉₀ = 6.3 days) mortality in 9 days in insects treated with M. anisopliae var. acridum. Amplification of fungal genomic DNA from the indigenous isolate with primers for the specific detection of M. anisopliae var. anisopliae produced a product almost 300 bp larger than expected based on previously known isolates. This is the first demonstration of a highly virulent, indigenous non-chemical control agent of grasshoppers in North America. GenBank Accession Nos. DQ342236, DQ342237.     

Field observations of the effects of fenitrothion and Metarhizium anisopliae var. acridum on non-target ground dwelling arthropods in the Sahel

The effect of the chemical insecticide, fenitrothion, and a mycoinsecticide based on Metarhizium anisopliae var. acridum on the activity of non-target epigeal arthropod scavengers was investigated in areas of open savannah in southeast Niger Republic, West Africa. Both insecticides were applied as full cover sprays to unreplicated 800 ha plots to assess their season-long control of Sahelian grasshoppers. Compared with control plots, fenitrothion caused an immediate but temporary reduction in grasshopper numbers, whereas M. anisopliae var. acridum provided delayed but prolonged control. Scavenging rates of pyrethroid-killed grasshoppers placed along transects in unsprayed plots and those treated with fenitrothion and M. anisopliae var. acridum at various intervals after spraying were assessed. In the fenitrothion plot, an immediate reduction in scavenging activity occurred that was still apparent after 40 days at the plot center, although recovery at the plot edges was more rapid. By contrast scavenging rates remained high over equivalent areas in the M. anisopliae var. acridum and two untreated plots. Concurrent to the scavenging study, counts of grasshopper cadavers resulting from the spray treatments were conducted. These counts revealed that the density of grasshopper cadavers remained low throughout the M. anisopliae var. acridum plot and explained <1% of the reduction in live grasshoppers resulting from treatment, compared with >20% in the fenitrothion plot. This shortfall in grasshopper cadavers resulting from the spray treatment in the M. anisopliae var. acridum plot was unexpected because in a monitoring study, fungus-killed (unlike pyrethroid-killed) grasshoppers were unattractive to scavengers and readily persisted in this plot, and thus should have become apparent. Given we did not observe significant grasshopper dispersal, the scarcity of cadavers generated in the M. anisopliae var. acridum plot, together with unquantified visual observations, suggests that predation of infected but living grasshoppers was high. Our data provide circumstantial evidence that the different effects of chemical and biological grasshopper control on grasshopper natural enemies may influence the efficacy of large-scale treatments.     

Seasonal prevalence of the insect pathogenic fungus Colletotrichum nymphaeae in Brazilian citrus groves under different chemical pesticide regimes

We report an endemic entomopathogenic fungus, known in Brazil as the 'salmão' fungus and identified here as Colletotrichum nymphaeae (Sordariomycetes: Glomerellales), infecting populations of citrus orthezia scale, Praelongorthezia praelonga. The seasonal prevalence of this pathogen in P. praelonga populations was investigated in three commercial citrus groves maintained under different pesticide regimes. Two citrus groves included inundative releases of another insect pathogenic fungus, Lecanicillium longisporum. Natural epizootics were consistently observed, with up to 84% infection rates being recorded during the warm rainy season. Temporal progression of C. nymphaeae-induced disease varied among the three pesticide regimes. Low infection levels from C. nymphaeae were associated with intensive application of broad spectrum pesticides. However, the prevalence of C. nymphaeae followed a density-dependent pattern with insect host abundance, irrespective of the pesticide regime. High proportions of Lecanicillium-infected insects were observed following infection peaks of C. nymphaeae and both fungi together contributed to 95% overall mortality of citrus orthezia during the wet season. Hence, the combined effect of both fungi considerably improves the biological control of citrus orthezia. We also surmise that the host abundance, environmental conditions, and application frequency of chemical pesticides in citrus groves exert a great influence in the seasonal prevalence of C. nymphaeae-induced disease. Altogether, these results suggest that C. nymphaeae is an important pathogen of P. praelonga and indicate that frequent use of synthetic pesticides may delay or reduce fungal epizootics.     

Status of the alien pathogen Paranosema locustae (Microsporidia) in grasshoppers (Orthoptera: Acridoidea) of the Argentine Pampas

After experimental introductions from North America in 1978–1982, the biocontrol agent Paranosema locustae became established in grasshopper communities of the western Pampas region of Argentina. The use and establishment of P. locustae in Argentina constitute both a case of neoclassical or new association biological control (use of an alien species against native pests) and a case of pathogen pollution (anthropogenic introduction–establishment of an infectious disease in populations of native species). Since P. locustae is a multihost pathogen among grasshoppers, its presence in the western Pampas represents an additional factor disrupting grasshopper communities according to the differential susceptibility of each species and possibly threatening some species. Microscopic examination of 504 grasshopper samples (the mean number of individuals per sample = 185) belonging to 43 species from 93 localities throughout the Pampas revealed an establishment area of approximate 90,000 km² from about 35° North to 38° South and from 61° East to 65° West. Field infections by P. locustae have now been detected in 21 grasshopper species in the western Pampas. Susceptible species with geographic distributions mostly restricted to the establishment area and with numerically small populations, like the melanopline Scotussa daguerrei, are predicted to be the ones facing higher risks of negative impacts.     

Herbivore phenology can predict response to changes in plant quality by livestock grazing

Livestock grazing can have a strong impact on herbivore abundance, distribution and community. However, not all species of herbivores respond the same way to livestock grazing, and we still have a poor understanding of the underlying mechanisms driving these differential responses. Here, we investigate the effect of light intensity cattle grazing on the abundance of two grasshoppers (Euchorthippus cheui and E. unicolor) that co-occur in the same grasslands and feed on the same food plant (the dominant grass Leymus chinensis). The two grasshopper species differ in phenology so that their peak abundances are separated into early- and late-growing seasons. We used an exclosure experiment to monitor grasshopper abundance and food quality in the field under grazed and ungrazed conditions, and performed feeding trials to examine grasshopper preference for grazed or ungrazed food plants in the laboratory. We found that the nitrogen content of L. chinensis leaves continuously declined in the ungrazed areas, but was significantly enhanced by cattle grazing over the growing season. Cattle grazing facilitated the early-season grasshopper E. cheui, whereas it suppressed the late-season grasshopper E. unicolor. Moreover, feeding trials showed that E. cheui preferred L. chinensis from grazed plots, while E. unicolor preferred the leaves from ungrazed plots. We conclude that livestock grazing has opposite effects on the two grasshopper species, and that these effects may be driven by grazing-induced changes in plant nutrient content and the unique nutritional niches of the grasshoppers. These results suggest that insects that belong to the same guild can have opposite nutrient requirements, related to their distinct phenologies, and that this can ultimately affect their response to cattle grazing. Our results show that phenology may link insect physiological needs to local resource availabilities, and should be given more attention in future work on interactions between large herbivores and insects.