Grasshoppers efficiently process C 4 grass leaf tissues: implications for patterns of host-plant utilization

Leaf-chewing insects are commonly believed to be unable to crush the nutrient-rich bundle sheath cells (BSC) of C 4 grasses. This physical constraint on digestion is thought to reduce the nutritional quality of these grasses substantially. However, recent evidence suggests that BSC are digested by grasshoppers. To directly assess the ability of grasshoppers to digest C 4 grass BSC, leaf particles of Bouteloua curtipendula (Poaceae) were examined from the digestive tracts of two grasshopper species: Camnula pellucida (Scudder) (primarily a grass feeder) and Melanoplus sanguinipes (Fabricius) (a forb and grass generalist) (Orthoptera: Acrididae). Transmission electron microscopy was used to make the first observations of BSC crushing by herbivorous insects. Camnula pellucida and M. sanguinipes crushed over 58% and 24%, respectively, of the BSC in ingested leaf tissues. In addition, chloroplast and cell membranes were commonly disrupted in uncrushed BSC, permitting soluble nutrients to be extracted, even when BSC walls remain intact. The greater efficiency with which C. pellucida crushes BSC is consistent with the idea that grass-feeding species are better adapted for handling grass leaf tissues than are generalist species. By demonstrating the effectiveness with which the BSC of B. curtipendula can be crushed and extracted by both species of grasshoppers, this study suggests one reason why C 4 grasses are not generally avoided by grasshoppers: at least some C 4 grasses can be more easily digested than has been hypothesized.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/73290/1/j.1570-7458.2005.00324.x.pd

Erratum

The bottom panel of figure number 1 in the article, “Roles of Peritrophic Membranes in Protecting Herbivorous Insects From Ingested Plant Allelochemicals” by Raymond V. Barbehenn, Volume 47, Number 2, June 2001 on pages 86–99 was submitted incorrectly. The corrected figure and legend from page 88 are herein reprinted. The bottom panel is now on the right hand side.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/34926/1/10041_ftp.pd

Non-absorption of ingested lipophilic and amphiphilic allelochemicals by generalist grasshoppers: The role of extractive ultrafiltration by the peritrophic envelope

The role of the peritrophic envelope in the non-absorption of three allelochemicals ingested by generalist grasshoppers was examined. This study tested the hypothesis that the association of lipophilic and amphiphilic allelochemicals with lipid aggregates (mixed micelles) reduces their permeability through the peritrophic envelope, a process similar to extractive ultrafiltration. Each of three allelochemicals (digitoxin, ouabain, and xanthotoxin) were solubilized in a lysolecithin suspension and injected separately into the midgut lumens of adult Melanoplus sanguinipes (Orthoptera: Acrididae). The low permeability of digitoxin through the peritrophic envelope was consistent with the extractive ultrafiltration of this compound. By comparison, ouabain and xanthotoxin permeability coefficients were 7- and 12-fold higher, respectively, than those of digitoxin. The results of extractive ultrafiltration assays confirmed that digitoxin is effectively extracted in lysolecithin micelles, but that neither ouabain nor xanthotoxin aggregates efficiently with these micelles. Arch. Insect Biochem. Physiol. 42:130–137, 1999. © 1999 Wiley-Liss, Inc.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/34925/1/3_ftp.pd

Digestion of uncrushed leaf tissues by leaf-snipping larval Lepidoptera

Cynodon dactylon (Poaceae) leaf pieces recovered from the frass of final-instar Paratrytone melane larvae (Lepidoptera: Hesperiidae) were composed of 14–22 percent crushed cells and 78–86 percent uncrushed cells, yet approximate digestibilities of soluble carbohydrates and protein averaged 78 and 88 percent, respectively. Therefore, nutrients from uncrushed cells were extracted by P. melane . The ability of P. melane and another leaf-snipping lepidopteran, Pseudaletia unipuncta (Noctuidae), to digest the contents of uncrushed bundle sheath and mesophyll cells in C. dactylon was examined with transmission electron microscopy. Organelles and plasma membranes were digested in the foreguts and midguts of both species. These findings suggest that nutrients in uncrushed leaf cells may be extracted through plasmodesmata and cell wall pores after membranes are digested. The generality of leaf-snipping, vis-a-vis leaf crushing, among larval Lepidoptera was assessed by surveying the mandible morphologies of 202 species. In 82 percent of the species surveyed only incisor regions were present. I conclude that leaf-snipping is a common mode of feeding among phytophagous Lepidoptera and that the digestion of cell contents is efficient despite the fact that few of the cells of ingested plant tissues are crushed.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/47796/1/442_2004_Article_BF00317222.pd

Effects of leaf maturity and wind stress on the nutrition of the generalist caterpillar Lymantria dispar feeding on poplar

The growth rates of insect herbivores commonly decrease when they feed on mature leaves due to the combined effects of several nutritional and physiological mechanisms. Environmental stresses during leaf development may also decrease herbivore performance. The present study tests two main hypotheses to help clarify the importance of these factors for the nutrition and growth of an insect herbivore: (i) decreases in nutrient levels, consumption rates and nutrient assimilation efficiencies impact negatively on herbivores feeding on mature leaves and (ii) wind stress has a negative impact on herbivores feeding on mature leaves. The results show that mature poplar (Populus alba × Populus tremula) leaves have decreased levels of protein and increased levels of fibre, and that growth rates of gypsy moth (Lymantria dispar L.) are decreased on mature leaves in association with decreased consumption rates. However, in contrast to the first hypothesis, protein and carbohydrate are assimilated efficiently (74–82% and 84–87%, respectively) from immature and mature poplar leaves. The larvae are able to chew mature leaves as efficiently as immature leaves, potentially maximizing nutrient extraction. By contrast to the second hypothesis, wind‐stressed leaves have no significant detrimental effects on nutrient assimilation efficiencies, and the lower growth rates of L. dispar larvae feeding on mature wind‐stressed leaves can be explained by lower consumption rates. Therefore, the availability of nutrients to herbivores feeding on mature tree leaves is not necessarily impacted by lower assimilation efficiencies, even when leaves develop under wind stress. These results help explain some of the large variation between the nutritional qualities of trees for forest Lepidoptera.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/112262/1/phen12105_am.pdfhttp://deepblue.lib.umich.edu/bitstream/2027.42/112262/2/phen12105.pd

Chitinolytic enzymes from Streptomyces albidoflavus expressed in tomato plants: effects on Trichoplusia ni

Tomato ( Lycopersicon esculentum ) cultivars were transformed with genes that encode bacterial chitinolytic enzymes (i.e., endochitinase and chitobiosidase) from Streptomyces albidoflavus . Transgenic tomato plants producing these enzymes were found to have enhanced resistance to cabbage looper, Trichoplusia ni (HÜbner) (Lepidoptera: Noctuidae), consistently reducing the growth rates of larvae. Mortality was significantly increased in two of three feeding trials. Ingestion of endochitinase and chitobiosidase not only affected development of larval T. ni from neonate to ultimate instar, but they also caused mortality and decreased insect weight when exposure began during the third instar. The results of this study provide some insight into the mode of action of the chitinolytic enzymes, by supporting the hypothesis that ingested chitinolytic enzymes damage the chitin component of the peritrophic envelope, leading to increased permeability. The size of marker molecules (FITC-dextrans) that permeated the peritrophic envelopes of T. ni feeding on transgenic plants were 50% larger than those permeating the peritrophic envelopes of T. ni feeding on the control plants. Further research is needed to more clearly identify the sites and modes of action of these chitinolytic enzymes, and the potential for synergy between these enzymes and pathogens, allelochemicals, and other environmental factors.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/72193/1/j.1570-7458.2001.00817.x.pd

The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera)

Tannic acid had no detrimental effect on the growth rates or digestion efficiencies of Orgyia leucostigma larvae. We examined three potential mechanisms which might allow these larvae to tolerate ingested tannic acid. (1) Little chemical modification of ingested tannic acid was found. Less than 10% of the tannic acid ingested by O. leucostigma was hydrolysed to gallic acid when measured with the rhodanine assay, and virtually all tannic acid was recovered in the frass when measured as total phenolics or with HPLC. (2) Peritrophic membranes were freely permeable to gallic acid but were impermeable to the higher molecular weight polyphenolic components of tannic acid. (3) Peritrophic membranes adsorbed less than 1% of the amount of tannic acid present in the guts of O. leucostigma larvae in vivo. Therefore, adsorption is not the means by which tannins are contained within the endoperitrophic space in O. leucostigma. We conclude that the peritrophic membrane acts as an ultrafilter. Further work is needed to determine whether ultrafiltration is dependent on tannin-binding substances in the gut fluid.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/29709/1/0000042.pd

Nutrients are assimilated efficiently by Lymantria dispar caterpillars from the mature leaves of trees in the Salicaceae

The efficient aquisition of nutrients from leaves by insect herbivores increases their nutrient assimilation rates and overall fitness. Caterpillars of the gypsy moth (Lymantria dispar L.) have high protein assimilation efficiencies (PAE) from the immature leaves of trees such as red oak (Quercus rubra) and sugar maple (Acer saccharum) (71–81%) but significantly lower PAE from their mature leaves (45–52%). By contrast to this pattern, both PAE and carbohydrate assimilation efficiencies (CAE) remain high for L. dispar larvae on the mature leaves of poplar (Populus alba × Populus tremula) grown in greenhouse conditions. The present study tests two alternative hypotheses: (i) outdoor environmental stresses cause decreased nutrient assimilation efficiencies from mature poplar leaves and (ii) nutrients in the mature leaves of trees in the poplar family (Salicaceae) remain readily available for L. dispar larvae. When poplar trees are grown in ambient outdoor conditions, PAE and CAE remain high (approximately 75% and 78%, respectively) in L. dispar larvae, in contrast to the first hypothesis. When larvae feed on the mature leaves of species in the Salicaceae [aspen (Populus tremuloides), cottonwood (Populus deltoides), willow (Salix nigra) and poplar], PAE and CAE also remain high (68–76% and 72–92%, respectively), consistent with the second hypothesis. Larval growth rates are strongly associated with protein assimilation rates, and more strongly associated with protein assimilation rates than with carbohydrate assimilation rates. It is concluded that tree species in the Salicaceae are relatively high‐quality host plants for L. dispar larvae, in part, because nutrients in their mature leaves remain readily available.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/110710/1/phen12087.pd

Plant‐derived differences in the composition of aphid honeydew and their effects on colonies of aphid‐tending ants

In plant–ant–hemipteran interactions, ants visit plants to consume the honeydew produced by phloem‐feeding hemipterans. If genetically based differences in plant phloem chemistry change the chemical composition of hemipteran honeydew, then the plant's genetic constitution could have indirect effects on ants via the hemipterans. If such effects change ant behavior, they could feed back to affect the plant itself. We compared the chemical composition of honeydews produced by Aphis nerii aphid clones on two milkweed congeners, Asclepias curassavica and Asclepias incarnata , and we measured the responses of experimental Linepithema humile ant colonies to these honeydews. The compositions of secondary metabolites, sugars, and amino acids differed significantly in the honeydews from the two plant species. Ant colonies feeding on honeydew derived from A. incarnata recruited in higher numbers to artificial diet, maintained higher queen and worker dry weight, and sustained marginally more workers than ants feeding on honeydew derived from A. curassavica . Ants feeding on honeydew from A. incarnata were also more exploratory in behavioral assays than ants feeding from A. curassavica . Despite performing better when feeding on the A. incarnata honeydew, ant workers marginally preferred honeydew from A. curassavica to honeydew from A. incarnata when given a choice. Our results demonstrate that plant congeners can exert strong indirect effects on ant colonies by means of plant‐species‐specific differences in aphid honeydew chemistry. Moreover, these effects changed ant behavior and thus could feed back to affect plant performance in the field. The role of indirect effects in trait evolution remains poorly understood. We show that plant chemical traits indirectly affect ant colony fitness and behavior via direct interactions with aphids. These plant‐derived effects on ant behavior could feed back to affect plant fitness in the field.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/109587/1/ece31277.pd

Effects of elevated atmospheric CO 2 on the nutritional ecology of C 3 and C 4 grass-feeding caterpillars

It is plausible that the nutritional quality of C 3 plants will decline more under elevated atmospheric CO 2 than will the nutritional quality of C 4 plants, causing herbivorous insects to increase their feeding on C 3 plants relative to C 4 plants. We tested this hypothesis with a C 3 and C 4 grass and two caterpillar species with different diet breadths. Lolium multiflorum (C 3 ) and Bouteloua curtipendula (C 4 ) were grown in outdoor open top chambers at ambient (370 ppm) or elevated (740 ppm) CO 2 . Bioassays compared the performance and digestive efficiencies of Pseudaletia unipuncta (a grass-specialist noctuid) and Spodoptera frugiperda (a generalist noctuid). As expected, the nutritional quality of L. multiflorum changed to a greater extent than did that of B. curtipendula when grown in elevated CO 2 ; levels of protein (considered growth limiting) declined in the C 3 grass, while levels of carbohydrates (sugar, starch and fructan) increased. However, neither insect species increased its feeding rate on the C 3 grass to compensate for its lower nutritional quality when grown in an elevated CO 2 atmosphere. Consumption rates of P. unipuncta and S. frugiperda were higher on the C 3 grass than the C 4 grass, the opposite of the result expected for a compensatory response to the lower nutritional quality of the C 4 grass. Although our results do not support the hypothesis that grass-specialist insects compensate for lower nutritional quality by increasing their consumption rates more than do generalist insects, the performance of the specialist was greater than that of the generalist on each grass species and at both CO 2 levels. Mechanisms other than compensatory feeding, such as increased nutrient assimilation efficiency, appear to determine the relative performance of these herbivores. Our results also provide further evidence against the hypothesis that C 4 grasses would be avoided by insect herbivores because a large fraction of their nutrients is unavailable to herbivores. Instead, our results are consistent with the hypothesis that C 4 grasses are poorer host plants primarily because of their lower nutrient levels, higher fiber levels, and greater toughness.Peer Reviewedhttp://deepblue.lib.umich.edu/bitstream/2027.42/47706/1/442_2004_Article_1572.pd