Ceratomia Catalpae Research Articles

Flexural rigidity of hawkmoth antennae depends on the bending direction

To probe its environment, the flying insect controllably flexes, twists, and maneuvers its antennae by coupling mechanical deformations with the sensory output. We question how the materials properties of insect antennae could influence their performance. A comparative study was conducted on four hawkmoth species: Manduca sexta, Ceratomia catalpae, Manduca quinquemaculata, and Xylophanes tersa. The morphology of the antennae of three hawkmoths that hover while feeding and one putatively non-nectar-feeding hawkmoth (Ceratomia catalpa) do not fundamentally differ, and all the antennae are comb-like (i.e., pectinate), markedly in males but weakly in females. Applying different weights to the free end of extracted cantilevered antennae, we discovered anisotropy in flexural rigidity when the antenna is forced to bend dorsally versus ventrally. The flexural rigidity of male antennae was less than that of females. Compared with the hawkmoths that hover while feeding, Ceratomia catalpae has almost two orders of magnitude lower flexural rigidity. Tensile tests showed that the stiffness of male and female antennae is almost the same. Therefore, the differences in flexural rigidity are explained by the distinct shapes of the antennal pectination. Like bristles in a comb, the pectinations provide extra rigidity to the antenna. We discuss the biological implications of these discoveries in relation to the flight habits of hawkmoths. Flexural anisotropy of antennae is expected in other groups of insects, but the targeted outcome may differ. Our work offers promising new applications of shaped fibers as mechanical sensors. Statement of significanceInsect antennae are blood-filled, segmented fibers with muscles in the two basal segments. The long terminal segment is muscle-free but can be flexed. Our comparative analysis of mechanical properties of hawkmoth antennae revealed a new feature: antenna resistance to bending depends on the bending direction. Our discovery replaces the conventional textbook scenario considering hawkmoth antennae as rigid rods. We showed that the pectinate antennae of hawkmoths behave as a comb in which the bristles resist bending when they come together. This anisotropy of flexural resistance offers a new mode of environmental sensing that has never been explored. The principles we found apply to other insects with non-axisymmetric antennae. Our work offers new applications for shaped fibers that could be designed to sense the flows.

Relationships among catalpol sequestration, metabolism and nutritional efficiencies of the catalpa sphinx, Ceratomia catalpae (Lepidoptera: Sphingidae)

AbstractSequestration of defensive compounds acquired from the environment can be costly to herbivorous insects. The catalpa sphinx, Ceratomia catalpae Boisduval (Lepidoptera: Sphingidae) sequesters the iridoid glycoside catalpol, which it acquires from Catalpa spp. (Lamiales: Bignoniaceae) host plants, at concentrations above those in host plant leaves. Previous research has shown that C. catalpae larvae are avoided by predatory arthropods; however, catalpol sequestration is negatively associated with the larval immune response, suggesting a cost to sequestration. By measuring the mass of C. catalpae larvae, their frass, and their diet, as well as respiration rate and catalpol sequestration, this study aimed to determine whether sequestration is also associated with reduced growth and nutritional efficiency. I found that respiration rate was negatively correlated with the amount of catalpol sequestered and positively correlated with the concentration, or proportion dry mass of catalpol sequestered, and that the amount of catalpol sequestered was positively correlated with three of four measures of nutritional efficiency. Larger larvae that were closer to pupation sequestered very low proportions dry mass of catalpol and had a reduced respiratory rate per unit mass. These results suggest that sequestration has some costs for expenditure of energy, but is positively correlated with several growth and nutrition‐related processes. Instead, the immunological cost of sequestration measured in previous studies could be due to direct effects on immune system components. Further research on the potential metabolic costs of chemical defense in other specialist species is recommended.

Nonpreference ofCeratomia catalpae(Lepidoptera: Sphingidae) to Invertebrate Predators

Aposematic traits such as bright contrasting coloration and gregarious feeding are often signals to predators that a potential prey is unpalatable. Larvae of Ceratomia catalpae (Boisduval) (Lepidoptera: Sphingidae), the catalpa sphinx, show aposematic traits and sequester catalpol, a secondary compound from their host plant Catalpa spp. (Bignoniaceae). Catalpol sequestration by other caterpillar species has been shown to deter both invertebrate and vertebrate predators, but the palatability of C. catalpae has not been explicitly tested. Choice tests were performed with spiders (Hogna carolinensis Walckenaer, Araneae: Lycosidae) and predatory hemipterans (Podisus maculiventris [Say], Hemiptera: Pentatomidae). These tests showed that predators naive to both C. catalpae and the alternate prey Trichoplusia ni (Hubner) (Lepidoptera: Noctuidae) and Manduca sexta (L.) (Lepidoptera: Sphingidae) preferred the alternate species, and that P. maculiventris that were exposed previously to T. ni also preferred T. ni. In nonchoice tests, P. maculiventris grew significantly more slowly upon C. catalpae compared to M. sexta. These results suggest that C. catalpae, like other caterpillars that sequester catalpol, is less palatable to invertebrate predators compared to nonsequestering caterpillar species.

Pre- and Postzygotic Barriers to Reproduction Between Two Host-Foodplant Complex Sources of the Parasitic Wasp,Cotesia congregata(Hymenoptera: Braconidae)

ABSTRACT Parasitic wasps are among the most speciose of all animals yet the drivers and mechanisms underlying their remarkable diversity are not well understood. Cotesia congregata (Say) and host, Manduca sexta (L.), have long-served as a model system for host-parasite and tritrophic interactions at multiple levels, as well as the evolution of symbiotic coevolved bracoviruses that suppress host defenses to parasitism. We investigated potential barriers to reproduction between two genetically differentiated host-foodplant complex sources of C. congregata originating from caterpillar hosts, M. sexta on tobacco (“MsT wasps”) or Ceratomia catalpae (Boisduval) on catalpa (“CcC wasps”). Both MsT and CcC wasps displayed ∼30% lower responses to cuticular washes of females from the alternate complex. Male courtship songs differed with respect to frequency, absolute amplitude, and duration of song elements. Despite differences in courtship behaviors, MsT and CcC wasps mated and produced offspring in the laboratory....

Genetic Differentiation of Two Host–Foodplant Complex Sources ofCotesia congregata(Hymenoptera: Braconidae)

The evolution of tritrophic interactions requires adaptations of natural enemies to both herbivorous hosts and host foodplants that can ultimately lead to the formation of locally adapted populations, host races, or ecological species. To situate our model organism, Cotesia congregata (Say), within this spectrum, we estimated genetic differentiation of wasps originating from two common host–foodplant complexes, Manduca sexta L. on tobacco (“MsT”) and Ceratomia catalpae (Haworth) on catalpa (“CcC”). To test the hypothesis that C. congregata associated with these host–foodplant, complexes were genetically differentiated even where they occur in sympatry, we experimentally introduced tobacco at an established “catalpa site” for two consecutive years and compared wasps collected at this site with wasps collected from allopatric tobacco and catalpa sites in the mid-Atlantic region of North America. Using seven microsatellite loci and the mitochondrial COI locus, we found differences in microsatellite allele frequencies based on host–foodplant complex (ΦPT values 0.47–0.50 among populations from different host–foodplant complexes), but not based on geographic location (mean ΦPT = 0.03). COI haplotypes of MsT and CcC wasps exhibited ∼2% sequence divergence, even where the host–food complexes were colocated within meters at the experimental site. Results indicate that MsT and CcC wasps represent distinct genetic lineages that are most likely incipient or nascent species with limited gene flow.

Incompatibility between plant-derived defensive chemistry and immune response of two sphingid herbivores.

Herbivorous insects use several different defenses against predators and parasites, and tradeoffs among defensive traits may occur if these traits are energetically demanding. Chemical defense and immune response potentially can interact, and both can be influenced by host plant chemistry. Two closely related caterpillars in the lepidopteran family Sphingidae are both attacked by the same specialist endoparasitoid species but have mostly non-overlapping host plant ranges that differ in secondary chemistry. Ceratomia catalpae is a specialist on Catalpa and also will feed on Chilopsis, which both produce iridoid glycosides. Ceratomia undulosa consumes members of the Oleaceae, which produce seco-iridoid glycosides. Immune response of the two species on a typical host plant species (Catalpa bignonioides for C. catalpa; Fraxinus americana for C. undulosa) was compared using a melanization assay, and did not differ. In a second experiment, the iridoid glycoside catalpol was added to the diets of both insects, and growth rate, mass, chemical defense, and immune response were evaluated. Increased dietary catalpol weakened the immune response of C. undulosa and altered the development rate of C. catalpae by prolonging the third instar and accelerating the fourth instar. Catalpol sequestration was negatively correlated with immune response of C. catalpae, while C. undulosa was unable to sequester catalpol. These results show that immune response can be negatively influenced by increasing concentrations of sequestered defensive compounds.

Chemical Defense Across Three Trophic Levels: Catalpa bignonioides, the Caterpillar Ceratomia catalpae, and its Endoparasitoid Cotesia congregata

Plant secondary chemistry can vary among plant tissues, individuals, and populations, and this variation has population-level consequences for upper trophic levels. In this study, we examined the multi-trophic consequences of variation in iridoid glycosides, which are a component of plant defense against generalist herbivores and also contribute to the unpalatability of sequestering herbivores to both vertebrate and invertebrate predators. Several populations of Catalpa bignonioides were located and examined for the presence of the Catalpa Sphinx, Ceratomia catalpae, a specialist herbivore of Catalpa. We quantified iridoid glycoside content in Catalpa Sphinx caterpillars and in damaged and undamaged C. bignonioides leaves. Overall, leaves of C. bignonioides that were damaged by Catalpa Sphinx caterpillars contained lower concentrations of two major iridoid glycosides, catalpol and catalposide, than leaves of undamaged trees from naturally occurring populations. Catalpa Sphinx caterpillars sequester only catalpol, and increasing catalpol and catalposide concentrations in leaves were associated with increased catalpol sequestration by caterpillars. The parasitoid Cotesia congregata develops successfully inside catalpol-sequestering Catalpa Sphinx caterpillars, and we examined parasitoid larvae for the presence of catalpol. Parasitoid larvae dissected from caterpillars contained catalpol, but at lower concentrations than their host caterpillars. The variation in chemical defense documented here has rarely been documented over multiple trophic levels, but such resolved systems are ideal for examining competing hypotheses about the effects of plant secondary metabolites on higher trophic levels.

Caterpillar Chemical Defense and Parasitoid Success: Cotesia congregata Parasitism of Ceratomia catalpae

Sequestration of plant compounds by herbivorous insects as a defense against predators is well documented; however, few studies have examined the effectiveness of sequestration as a defense against parasitoids. One assumption of the "nasty host" hypothesis is that sequestration of plant defense compounds is deleterious to parasitoid development. We tested this hypothesis with larvae of the sequestering sphingid Ceratomia catalpae, which is heavily parasitized by the endoparasitoid Cotesia congregata, despite sequestering high concentrations of the iridoid glycoside catalpol from their catalpa host plants. We collected C. catalpae and catalpa leaves from six populations in the Eastern US, and allowed any C. congregata to emerge in the lab. Leaf iridoid glycosides and caterpillar iridoid glycosides were quantified, and we examined associations between sequestered caterpillar iridoid glycosides and C. congregata performance. Caterpillar iridoid glycosides were not associated with C. congregata field parasitism or number of offspring produced. Although wasp survival was over 90% in all populations, there was a slight negative relationship between caterpillar iridoid glycosides and wasp survival. Iridoid glycosides were present in caterpillars at levels that are deterrent to a variety of vertebrate and invertebrate predators. Thus, our results support the alternative hypothesis that unpalatable, chemically defended hosts are "safe havens" for endoparasitoids. Future trials examining the importance of catalpol sequestration to potential natural enemies of C. congregata and C. catalpae are necessary to strengthen this conclusion.

Susceptibility of Catalpa, Chilopsis, and Hybrids to Powdery Mildew and Catalpa Sphinx Larvae

A diverse collection of germplasm representing 24 taxa from Catalpa sect. Catalpa Paclt and sect. Macrocatalpa Grisebach, Chilopsis D. Don, and ×Chitalpa Elias & Wisura were screened for susceptibility to powdery mildew (PM) incited by Erysiphe elevata (Burr.) U. Braun & S. Takam and feeding by catalpa sphinx larvae (CSL), Ceratomia catalpae (Boisduval). PM screening was conducted on plants grown in a lathhouse (50% shade) in 2004 and a gravel pad (100% sun) in 2005. The PM causal organism was identified as E. elevata both years. Disease incidence and severity were recorded at 2-week intervals for 6 weeks and used to calculate area under the disease progress curves (AUDPC) for each year. North American Catalpa in sect. Catalpa, Chilopsis, and ×Chitalpa taxa were all moderately to highly susceptible to PM. Chinese Catalpa in sect. Catalpa and West Indian species in sect. Macrocatalpa were resistant to PM. Hybrids between North American and Chinese Catalpa in sect. Catalpa varied in susceptibility, indicating transmission of partial resistance to PM. No differences in survival or growth were found in a no-choice feeding study with CSL reared on taxa from Chilopsis, ×Chitalpa, or either section of Catalpa. Future breeding of ×Chitalpa can use sources of PM resistance identified in this study, but a source of resistance to CSL was not found.

(241) Susceptibility of Catalpa, Chilopsis, and Hybrids to Powdery Mildew and Catalpa Sphinx Larvae

A diverse collection of germplasm representing 24 taxa from Catalpa sect. Catalpa Paclt and sect. Macrocatalpa Grisebach, Chilopsis D. Don, and ×Chitalpa Elias & Wisura were screened for susceptibility to powdery mildew (PM), Erysiphe elevata (Burr.) U. Braun & S. Takam, and Catalpa sphinx larvae (CSL), Ceratomia catalpae (Boisduval), feeding. The PM screening was conducted in 2004–05, with plants grown in a lathhouse (50% shade) in 2004, and a gravel pad (100% full sun) in 2005. The PM causal organism was identified as Erysiphe elevata both years. Disease incidence and severity were recorded at 2-week intervals for 6 weeks and used to calculate area under the disease progress curves (AUDPC) for each taxon for each year. North American Catalpa in sect. Catalpa, Chilopsis, and ×Chitalpa taxa were all moderate to highly susceptible to PM. Chinese Catalpa in sect. Catalpa and West Indian species in sect. Macrocatalpa were resistant to PM. Hybrids between North American and Chinese Catalpa in sect. Catalpa varied in susceptibility, indicating inheritance of partial resistance to PM. A no-choice feeding study conducted with CSL in 2005 found no differences in survival or growth of larvae reared on taxa from Chilopsis, ×Chitalpa, or either section of Catalpa. Future breeding of ×Chitalpa can utilize two different sources of PM resistance, but a source for resistance to CSL was not identified.

Hostplant suitability and defensive chemistry of the Catalpa sphinx, Ceratomia catalpae.

The growth and survival of the Catalpa sphinx, Ceratomia catalpae (Sphingidae), were measured on five different species of Catalpa: C. bignonioides, C. bungeii, C. fargeseii, C. ovata, and C. speciosa. Larval growth varied significantly among these host plant species; however, survival did not differ. Quantification of the iridoid glycoside content of larvae, pupae, adults, larval frass, and leaves of the larval host plant, C. bignonioides, by gas chromatography showed that leaves contained both catalpol and catalposide; larvae, pupae, and frass contained only catalpol; and the adults contained no detectable iridoid glycosides. Amounts were highest in the larvae and declined in the pupal stage. Very small amounts of catalpol were detected in adults of the parasitoid, Cotesia congregata, and in the silken cocoons. The hemolymph in which the parasitoid larvae grew contained over 50% dry weight catalpol. Larvae of C. catalpae often regurgitate when disturbed. This may serve as a defense against predators. A comparison of the growth of larvae pinched with forceps to induce regurgitation with those that were not so treated showed that larvae that were pinched, and usually regurgitated, grew significantly more slowly than those that were not.

The behaviour of grey jays, Perisoreus canadensis, towards palatable and unpalatable Lepidoptera

Grey jays were fed a set of six species of lepidopterans, predicted to be palatable or unpalatable based on their coloration and the fate of ingested host plant allelochemicals. Each of four birds received the entire series of insects. Junonia coenia (Nymphalidae) and Ceratomia catalpae (Sphingidae) were highly palatable as predicted based on their relatively cryptic coloration and lack of chemical defence. Three Euphydryas (Nymphalidae) species were predicted to be unpalatable: larvae and adults are warningly coloured and they sequester iridoid glycosides. However, Euphydryas gillettii was quite palatable, E. anicia was intermediate and E. phaeton was unpalatable. These differences may be due to differences in the iridoid glycoside content of these butterflies. Eumaeus atala (Lycaenidae) sequesters cycasin from its hostplant in the Cycadaceae and larvae and adults are warningly coloured. Adult E. atala were unpalatable.

Iridoid glycosides in the nectar ofCatalpa speciosa are unpalatable to nectar thieves

The floral nectar ofCatalpa speciosa has a chemical mechanism that limits thievery. A bioassay employing sphingid larvae,Ceratomia catalpae, shows that catalpa iridoid glycosides are present in the floral nectar. When potential nectar thieves are fed nectar, a sucrose solution of identical concentration, or a sucrose solution plus 0.4% catalpol and 0.4% catalposide (catalpa iridoids), the thieves drink significantly more of the pure sucrose solution than either of the other two sugar sources. Those thieves that drink either the nectar or the sucrose solution plus catalpa iridoids develop behavioral abnormalities including regurgitation and loss of locomotion. The response of the potential nectar thieves to nectar or the sucrose solution plus catalpa iridoids cannot be distinguished by the amount consumed or by their behavior. The legitimate diurnal pollinators ofC. speciosa are not affected by the iridoid glycosides.

The Role of the Extrafloral Nectaries of Catalpa Speciosa in Limiting Herbivory and Increasing Fruit Production

The leaves of Catalpa speciosa (Bignoniaceae) have extrafloral nectaries that are active from early June to September. Peak nectar secretion occurs in late June and early July when the eggs and young larvae of the first generation of the principal herbivore, Ceratomia catalpae (Sphingidae), are present. Leaves that have been damaged by this herbivore secrete significantly more nectar than undamaged leaves. The nectaries are visited by various species of ants, ladybird beetles, and a parasitoid. These predaceous insects attack and/or remove the eggs and young larvae of the herbivore. A series of ant exclusion experiments show that branches without ants have significantly fewer larvae removed, have significantly more leaf herbivory, and produce significantly fewer mature fruits than control branches (with ants). These data suggest that secretion of extrafloral nectar by C. speciosa and its subsequent harvesting by insects is mutually beneficial to both the plant and the predaceous insects.

Electrophysiological studies of gustation in lepidopterous larvae

The electrophysiological responses of the maxillary gustatory sensilla of ten species of lepidopterous larvae to sugars, polyhydric alcohols, amino acids, organic acids, glycosides, and sterols were tested. Of the caterpillars examined three were monophagous (Calpodes ethlius, Ceratomia catalpae, Danaus plexippus), three were oligophagous (Pieris rapae, Papilio polyxenes, Malacosoma americana), and four were polyphagous (Helioihis zea, Estigmene acrea, Isia isabella, Porthetria dispar). The sensilla of all species are structurally similar to the extent of having four chemosensory bipolar neurons in each peg.

Electrophysiological studies of gustation in lepidopterous larvae

The electrophysiological responses of the maxillary gustatory sensilla of ten species of lepidopterous larvae to sugars, polyhydric alcohols, amino acids, organic acids, glycosides, and sterols were tested. Of the caterpillars examined three were monophagous (Calpodes ethlius, Ceratomia catalpae, Danaus plexippus), three were oligophagous (Pieris rapae, Papilio polyxenes, Malacosoma americana), and four were polyphagous (Helioihis zea, Estigmene acrea, Isia isabella, Porthetria dispar). The sensilla of all species are structurally similar to the extent of having four chemosensory bipolar neurons in each peg. It is not possible to account for the wide range of responsiveness to diverse compounds in terms of narrowly specific receptors characterized as water, sugar, salt, inositol, or amino acid receptors. Bach receptive cell was found to have only a limited degree of specificity. Not all amino acids stimulated the same cell. Some amino acids stimulated only one; some stimulated two; some inhibited all cells; some inhibited one while stimulating another. Differential sensitivity to amino acids varied from species to species and even between the two sensilla in an individual. The diversity of relationships found with amino acids existed also with respect to acids and glycosides. Ascorbic and hydrochloric acids at equivalent pH values each stimulated a different cell. Glycosides stimulated one or two cells depending on the species and sensillum. Synergism occurred nearly as often as inhibition. Among the instances were synergistic reactions between sucrose and inositol, proline and inositol, sucrose and sinigrin, glycine and sucrose. The occurrence of the phenomenon was specific to certain species and sensilla. Results point to the conclusion that the basis of difference in sensitivity to different compounds from species to species and from receptor to receptor reflects variations in the molecular structure of the receptor substrate. Whatever the mechanisms involved it is clear that caterpillars are able to detect not only compounds that may be of nutritive value but also non-nutritive compounds some of which are secondary plant substances. When the total taste sensitivities of the various species of caterpillars are compared, there is no obvious difference between polyphagous, oligophagous, and monophagous species.

Resistance to Cold in Ceratomia catalpae

SALT1 has reported resistance to frost and to being frozen in several species of arthropods. He has also reported on the synthesis and accumulation of a low molecular weight solute (glycerol) in insects and has suggested that this may explain resistance to cold2. Lozina-Lozinsky3 stated that in the caterpillar, Pyrausta nubilalis, which can tolerate extremely low temperatures, the proteins and nucleoproteins can resist an increase in concentrations of the electrolytes. Asahina and Tanno4 found that the overwintering pre-pupal larvae of a sawfly, Trichiocampus populi, were able to survive freezing at −30° C for a full day, and withstand liquid nitrogen temperature (−195.8° C) provided they had been previously frozen at temperatures lower than −20° C.

The Chemical Basis of the Host Selection in the Catalpa Sphinx, Ceratomia catalpae (Lepidoptera, Sphingitlae)1

The monophagy of the larvae of the catalpa sphinx on leaves of several species of the catalpa tree has been confirmed. A mixture of catalposides has been isolated from leaves of Catalpa bignonioides , and their chemical properties found identical with those described in the literature. These catalposides elicited a strong feeding response when tested in an agar diet. The activity was lost after acid hydrolysis. It is suggested that the presence of catalposides in the catalpa tree is responsible for the monophagous habit of this insect.

The Hornworm Parasite, Apanteles Congregatus Say and the Hyperparasite, Hypopteromalus Tabacum (Fitch)1

Apanteles congregatus (Say) is a common and widely distributed parasite of Sphingidae. In North Carolina it is the most important enemy of the catalpa sphinx, Ceratomia catalpae (Bdv.) and the tomato worm, Protoparce sexta (Johan.), which in this region is usually called the tobacco horn worm. The hornworms increase in numbers rapidly in the late summer in fields where the tobacco stalks are left standing after harvest, and if the foliage is not completely destroyed they will usually remain in the fields until the first killing frost. Hornworm eggs can often be found in the field as late as October 1. The percentage of hornworms parasitized by Apanteles also increases steadily but there is considerable variation between different fields.

Additions to Our Knowledge of the Toxicity of Stomach Poisons to Insects

The so-called sandwich method was used to study the effect of calcium hydroxide, calcium caseinate, precipitated sulfur, dry Bordeaux mixture, and hydrated ferric oxide on the toxicity of acid lead arsenate for the fourth instar silkworm. No remarkable effect was produced by any of these substances. It is fairly certain, however, that calcium hydroxide and calcium caseinate increase the toxicity of acid lead arsenate when mixed with it in approximately equal proportions by weight: The indications are that precipitated sulfur may increase the toxicity of acid lead arsenate, and that dry Bordeaux mixture and hydrated ferric oxide may decrease it. Experiments were made by the sandwich method on the relative susceptibility to acid lead arsenate of the following caterpillars in the last instar: Eastern tent caterpillar (Malacosoma Americana Fab.), fall webworm (Hyphantria cunea Drury), walnut caterpillar (Datana integerrima G. & R.). and the catalpa sphinx (Ceratomia catalpae Boisd.) With the median lethal dose of acid lead arsenate for the fourth-instar silkworm as the standard of comparison, it was found that the first two insects were less susceptible and the last two more susceptible to acid lead arsenate than the fourth instar silkworm. It was also shown that, although the median lethal doses of acid lead arsenate and cuprous cyanide are different for the catalpa sphinx and silkworm, their relative toxicity is about the same for each of these insects. Certain improvements in the sandwich method are described.