A lever action hypothesis for pendulous hummingbird flowers: experimental evidence from a columbine.

BACKGROUND AND AIMS: Pendulous flowers (due to a flexible pedicel) are a common, convergent trait of hummingbird-pollinated flowers. However, the role of flexible pedicels remains uncertain despite several functional hypotheses. Here we present and test the 'lever action hypothesis': flexible pedicels allow pendulous flowers to move upwards from all sides, pushing the stigma and anthers against the underside of the feeding hummingbird regardless of which nectary is being visited. METHODS: To test whether this lever action increased pollination success, we wired emasculated flowers of serpentine columbine, Aquilegia eximia, to prevent levering and compared pollination success of immobilized flowers with emasculated unwired and wire controls. KEY RESULTS: Seed set was significantly lower in wire-immobilized flowers than unwired control and wire control flowers. Video analysis of visits to wire-immobilized and unwired flowers demonstrated that birds contacted the stigmas and anthers of immobilized flowers less often than those of flowers with flexible pedicels. CONCLUSIONS: We conclude that flexible pedicels permit the levering of reproductive structures onto a hovering bird. Hummingbirds, as uniquely large, hovering pollinators, differ from flies or bees which are too small to cause levering of flowers while hovering. Thus, flexible pedicels may be an adaptation to hummingbird pollination, in particular due to hummingbird size. We further speculate that this mechanism is effective only in radially symmetric flowers; in contrast, zygomorphic hummingbird-pollinated flowers are usually more or less horizontally oriented rather than having pendulous flowers and flexible pedicels.

Mucilage-bound sand reduces seed predation by ants but not by reducing apparency: a field test of 53 plant species.

Seed mucilage, a coating on seeds or fruit that becomes slimy and sticky when wet, has evolved convergently many times across plants. One common consequence of having seed mucilage is that sand and dirt particles stick to wet seeds and remain tightly bound to the seed surface after the mucilage dries. Here, we test the hypothesis that a mucilage-bound sand coating protects the seed from seed predators; either as a physical barrier or by reducing apparency of the seed (i.e., camouflage). We experimentally manipulated the sand coating on seeds of 53 plant species of 13 families and assayed the defensive benefit of the sand coating in feeding "depots" near harvester ant nests in California's Central Valley. Consistent with a defensive function, sand coating reduced ant predation on seeds in 48 of the 53 species examined. To test whether this striking benefit was due to reduced apparency, we conducted an addition experiment using flax seeds in which we factorially manipulated the color of both the background substrate and the sand coating, creating visually apparent and unapparent seeds. Our results did not support the reduced apparency hypothesis; seeds coated in background-matched sand were removed at the same rate as seeds coated in unmatched sand. The defensive benefit of a sand coating was not well-predicted by seed mass, entrapped sand mass, or sand mass scaled by seed mass. Together, our results demonstrate that seed mucilage is a phylogenetically widespread and effective seed defensive trait and point to the physical barrier, not reduced apparency, as a mechanism.

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 August 2009-30 September 2009.

This article documents the addition of 238 microsatellite marker loci and 72 pairs of Single Nucleotide Polymorphism (SNP) sequencing primers to the Molecular Ecology Resources Database. Loci were developed for the following species: Adelges tsugae, Artemisia tridentata, Astroides calycularis, Azorella selago, Botryllus schlosseri, Botrylloides violaceus, Cardiocrinum cordatum var. glehnii, Campylopterus curvipennis, Colocasia esculenta, Cynomys ludovicianus, Cynomys leucurus, Cynomys gunnisoni, Epinephelus coioides, Eunicella singularis, Gammarus pulex, Homoeosoma nebulella, Hyla squirella, Lateolabrax japonicus, Mastomys erythroleucus, Pararge aegeria, Pardosa sierra, Phoenicopterus ruber ruber and Silene latifolia. These loci were cross-tested on the following species: Adelges abietis, Adelges cooleyi, Adelges piceae, Pineus pini, Pineus strobi, Tubastrea micrantha, three other Tubastrea species, Botrylloides fuscus, Botrylloides simodensis, Campylopterus hemileucurus, Campylopterus rufus, Campylopterus largipennis, Campylopterus villaviscensio, Phaethornis longuemareus, Florisuga mellivora, Lampornis amethystinus, Amazilia cyanocephala, Archilochus colubris, Epinephelus lanceolatus, Epinephelus fuscoguttatus, Symbiodinium temperate-A clade, Gammarus fossarum, Gammarus roeselii, Dikerogammarus villosus and Limnomysis benedeni. This article also documents the addition of 72 sequencing primer pairs and 52 allele specific primers for Neophocaena phocaenoides.

Induced resistance in rice against insects.

Vaccinations are the mainstay of western preventive medicine, and they have been used to protect some crops against disease and insect pests. We consider rice as a model for protection using induced resistance since it is one of the most important staple crops and there have been significant new developments in: cross-resistance among rice insects, chemical pathways involved in induced resistance, sequencing the rice genome and expression of genes conferring resistance against rice insect pests. Insect attack has been found to cause lesions that kill planthopper eggs and early stages of gall midges. Damaged plants released volatiles that made them less likely to be chosen by planthoppers and more attractive to parasitoids. Chemical elicitors have been developed for dicotyledonous plants and these can induce resistance in rice, although rice does not fit models developed to explain signalling in dicots. For example, salicylic acid did not increase in rice after infection by pathogens and did not appear to be the mobile signal for induced resistance against pathogens although it was involved in induced responses to phloem-feeding insects. Jasmonic acid acted as a signal in some induced responses to pathogens as well as chewing insects. Many of the genes associated with induced resistance in rice have recently been mapped, and techniques are being developed to incorporate them into the genome of cultivated varieties. Attempts to control insect pests of rice will affect interactions with pathogens, predators and parasites, and other organisms in this agroecosystem.

Jasmonic acid induced resistance in grapevines to a root and leaf feeder.

We investigated the effects of induced resistance to the folivore Pacific spider mite, Tetranychus pacificus McGregor (Acari: Tetranychidae), as well as the root-feeding grape phylloxera Daktulosphaira vitifoliae (Fitch) (Homoptera: Phylloxeridae) in grapevines using exogenous applications of the natural plant inducer, jasmonic acid. Foliar jasmonic acid application at concentrations that caused no phytotoxicity significantly reduced the performance of both herbivores. There were less than half as many eggs produced by spider mites feeding on the induced leaves compared with control grapevine leaves. Induction reduced the numbers of phylloxera eggs and nymphal instars by approximately threefold and twofold, respectively, on induced compared with control grapevine roots. The negative demographic effects of jasmonic acid application appeared to be caused by changes in fecundity for the Pacific spider mite, and possibly changes in development rate and fecundity for grape phylloxera.

Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush.

The possibility of communication between plants was proposed nearly 20 years ago, although previous demonstrations have suffered from methodological problems and have not been widely accepted. Here we report the first rigorous, experimental evidence demonstrating that undamaged plants respond to cues released by neighbors to induce higher levels of resistance against herbivores in nature. Sagebrush plants that were clipped in the field released a pulse of an epimer of methyl jasmonate that has been shown to be a volatile signal capable of inducing resistance in wild tobacco. Wild tobacco plants with clipped sagebrush neighbors had increased levels of the putative defensive oxidative enzyme, polyphenol oxidase, relative to control tobacco plants with unclipped sagebrush neighbors. Tobacco plants near clipped sagebrush experienced greatly reduced levels of leaf damage by grasshoppers and cutworms during three field seasons compared to unclipped controls. This result was not caused by an altered light regime experienced by tobacco near clipped neighbors. Barriers to soil contact between tobacco and sagebrush did not reduce the difference in leaf damage although barriers that blocked air contact negated the effect.

Future use of plant signals in agricultural and industrial crops.

Entomologists have begun to develop techniques involving vaccinations and applications of chemical elicitors to protect crops, applying what they know about the signals that mediate induced resistance. Apple and strawberry growers who tolerate some mites have realized reduced subsequent pest problems. Winegrape growers who have had chronically devastating populations of Pacific mites vaccinate their vines with less damaging Willamette mites and achieve smaller pest populations and improved yield. Vaccinations using live herbivores provide all the signals that plants use to induce resistance but are logistically difficult. Many chemicals have been identified as elicitors of induced resistance including one (benzothiadiazole) that is now marketed commercially for use against plant diseases. Exogenous application of jasmonic acid (JA) induces accumulation of many putatively defensive compounds and reduces herbivory in field situations. Ongoing experiments are evaluating the potential of exogenous JA applications in several crops. Recent evidence suggests that the pathways that plants use to protect against pathogens and against herbivores may be antagonistic, such that stimulating one depresses the other. The extent to which this trade-off may limit the ability of natural plants to defend themselves or agriculturists to limit plant parasites remains to be determined.

Induced plant responses and information content about risk of herbivory.

Plant defenses are plastic when a single genotype can produce different phenotypes depending upon the environment. Plastic responses might be favored by selection only if plants can respond appropriately to reliable information in their environments. Recent findings indicate that when information is accurate, plants can benefit by changing their defenses appropriately but, when information is inaccurate they produce inappropriate defenses and have lower fitness. Plants can potentially use a variety of cues to adjust their defensive phenotypes appropriately. The relationship between the information about risk of herbivory and plant defense can be evaluated by determining if the information available to plants is reliable enough to support the evolution of plastic-induced defenses.

Evolution of prolonged development: a life table analysis for periodical cicadas.

According to conventional wisdom, natural selection should favor early reproduction. Prolonged development of 13 and 17 yr has been difficult to explain for periodical cicadas. Earlier, I hypothesized that development may be long for periodical cicadas because fecundity increases as a function of longer development with little increased risk of mortality. In this article, I tested whether the fecundity was greater for 17-yr cicadas than for 13-yr cicadas and estimated the shape of the survivorship curve. A cohort of 17-yr cicadas was followed from 1979 through 1996. Most mortality occurred during the first 2 yr; thereafter mortality was uncommon. Across 17 yr, adult densities increased at five out of seven sites, and in no case did the change exceed three times. Seventeen-year adults had heavier ovaries than did 13-yr adults; this effect was greater for Magicicada cassini (1.80 times) than for Magicicada decim (1.16 times). For M. cassini, the extra fecundity associated with 17-yr development swamped the potential advantages of more frequent reproduction of 13-yr forms under most conditions. For M. decim, realistically low rates of mortality roughly matched the small effect of development on fecundity. Prolonged development in periodical cicadas may be explained adequately by the demographic hypothesis, although it may also reduce predation risk to adults or result from strong selection for large body size.

Exogenous jasmonates simulate insect wounding in tomato plants (Lycopersicon esculentum) in the laboratory and field.

Wounding increases the levels and activities of several defense-related proteins in the foliage of the tomato plant,Lycopersicon esculentum Mill. Evidence indicates that two of these responses, the systemic increases in polyphenol oxidase and proteinase inhibitors, are regulated by an octadecanoid-based signalling pathway which includes the wound hormone, jasmonic acid. It is not known whether other responses to wounding are also regulated by this same signalling pathway. In this paper, we show that application of jasmonates (jasmonic acid or its volatile derivative, methyl jasmonate) in low concentrations to foliage of young tomato plants induced, in a dose-dependent manner, the same protein responses-polyphenol oxidase, proteinase inhibitors, lipoxygenase, and peroxidase-as doesHelicoverpa zea Boddie feeding. Application of jasmonic acid to a single leaflet of four-leaf tomato plants induced these four proteins in a spatial pattern nearly identical to that produced by localized feeding ofH. zea. Exogenous jasmonic acid also decreased suitability of foliage for the beet armyworm,Spodoptera exigua Hubner in the laboratory. Based on these results, we conducted an experiment to measure the effects of jasmonic acid spray under field conditions. We provide the first evidence that jasmonic acid spray on field plants induces production of chemical defenses above the levels found in unsprayed controls. Exogenous jasmonic acid sprayed on plants in agricultural plots increased levels of polyphenol oxidase and proteinase inhibitors. Because application of jasmonic acid induces these defensive compounds at low concentrations in a manner similar to natural wounding, it may prove to be a useful tool for stimulating plant resistance to insects in the field.

Predator-mediated apparent competition between two herbivores that feed on grapevines.

We have been releasing economically unimportant herbivorous mites of one species early in the season and protecting grapevines against another, more damaging herbivorous mite throughout the growing season. In this experiment, releases of economically unimportant Willamette mites alone, or of predatory mites alone, failed to reduce populations of the damaging Pacific spider mite. However, where both herbivorous Willamette mites and predatory mites were released together populations of Pacific mites were reduced. This interaction between effects of Willamette mites and predatory mites suggests that predation against Pacific mites was more effective where alternate prey (Willamette mites) were available for the predators. The "apparent competition" between Willamette mites and Pacific mites, mediated through their shared predator, can be an important force in the agroecosystem although its importance varies from year to year and vineyard to vineyard.

Induced resistance and interspecific competition between spider mites and a vascular wilt fungus.

The fungal pathogen Verticillium dabliae was less likely to cause symptoms of verticillium wilt on cotton seedlings that had been previously exposed to spider mites than on unexposed cotton seedlings. Conversely, populations of the spider mite Tetranychus urticae grew less rapidly on seedlings that had been inoculated with V. dabliae than on uninoculated controls. Changes caused by pathogen or herbivore attack reduced the suitability of the host plant to a diversity of organisms. This result suggests that highly unrelated organisms that share a host plant may interact strongly.

Environmental conditions affecting the strength of induced resistance against mites in cotton.

Spider mites (Tetranychus urticae) were raised on cotton plants that had been damaged by a previous bout of mite feeding (T. turkestani) and on control plants that were previously not exposed to mites. The effect of induced plant responses upon mite populations was variable ranging from a 4-fold reduction in population growth to no difference at all. The strength of induced resistance was greatest when the population growth of mites was low for other, unknown, reasons. When mite population growth on control plants was great, the effects of induced resistance were diminished.Mite population growth was inversely related to levels of initial damage caused by previous feeding. There was no evidence of a damage threshold that needed to be exceeded before induced resistance became effective. Increased levels of initial damage were not associated with morphological changes in the plants.

Effects of clonal variation of the host plant, interspecific competition, and climate on the population size of a folivorous thrips.

The effects of clonal variation, interspecific competition, and climate upon the population size of Apterothrips secticornis was assessed by a series of observations and experimental manipulations. Three clones of the host plant, Erigeron glaucus, consistently supported different numbers of thrips during monthly censuses. When rosettes of the three clones were transplanted to a common garden, relative numbers of thrips on the clones remained the same as those observed where the clones grew in situ. The presence or absence of other hervivores had no effect on thrips numbers in the common garden. Plume moth caterpillars and thrips were observed to co-occur less often than expected in the field but this was caused by differences in habitat selection by these two species rather than being the result of interspecific competition. Populations of thrips were affected by climate, but analyses suggest that the host clone was a more important factor.

Induced resistance of cotton seedlings to mites.

Mite populations grew more rapidly on new growth of cotton seedlings that had never been exposed to mites than on new growth of plants whose cotyledons had been previously exposed to them. Experiments in which a second mite introduction on the exposed plants involved a different mite species produced this same result. The substance or substances responsible for the response are transported systemically among leaves of cotton seedlings.