Geographical and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinator’s larvae

Interspecific interactions can vary within and among populations and geographical locations, and this variation can influence the nature of the interaction (e.g. mutualistic versus antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies whose larvae feed only on their seeds. Here we document geographical variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33–58%) of seeds are released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10–69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but some pay more than others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plant (positive relationship between numbers of seeds released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.     

Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach

The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is a pest of soybeans in Asia, and in recent years has caused extensive damage to soybeans in North America. Within these agroecosystems, generalist predators form an important component of the assemblage of natural enemies, and can exert significant pressure on prey populations. These food webs are complex and molecular gut-content analyses offer nondisruptive approaches for examining trophic linkages in the field. We describe the development of a molecular detection system to examine the feeding behaviour of Orius insidiosus (Hemiptera: Anthocoridae) upon soybean aphids, an alternative prey item, Neohydatothrips variabilis (Thysanoptera: Thripidae), and an intraguild prey species, Harmonia axyridis (Coleoptera: Coccinellidae). Specific primer pairs were designed to target prey and were used to examine key trophic connections within this soybean food web. In total, 32% of O. insidiosus were found to have preyed upon A. glycines, but disproportionately high consumption occurred early in the season, when aphid densities were low. The intensity of early season predation indicates that O. insidiosus are important biological control agents of A. glycines, although data suggest that N. variabilis constitute a significant proportion of the diet of these generalist predators. No Orius were found to contain DNA of H. axyridis, suggesting intraguild predation upon these important late-season predators during 2005 was low. In their entirety, these results implicate O. insidiosus as a valuable natural enemy of A. glycines in this soybean agroecosystem.     

Consumption of aphids by spiders and the effect of additional prey: evidence from microcosm experiments

Spiders are common generalist predators in agroecosystems and have been suggested to lower herbivore abundance in crops. It is not clear, however, if spiders can effectively suppress pest populations, and if so, by what mechanisms. In a microcosm experiment, we examined the consumption of the bird cherry-oat aphid, Rhopalosiphum padi L. (Homoptera: Aphididae), a pest species in wheat fields, by three spider species that differ in their hunting methods. We then tested the effect of additional prey type on the ability of erigonid spiders to reduce aphids. In a 48-h experiment Mermessus denticulatus (Banks) (Araneae: Linyphiidae; Erigoninae) consumed more aphids than did Enoplognatha gemina Bosmans and Van Keer (Araneae: Theridiidae) and Bathyphantes cf. extricatus (O·P.-Cambridge) (Araneae: Linyphiidae; Linyphiinae). This difference may be due to the ability of erigonids to forage actively on the vegetation in addition to using their webs to catch prey. In a 7-week experiment, we provided springtails (Collembola) in high and low densities as additional prey to mated erigonids, prior to aphid introduction. Spiders in the low-density springtail treatment built more webs on the vegetation, and caused a 50% reduction in aphid populations. There were significantly fewer aphids in the low-density springtail treatment, but not in the high-density treatment, in comparison to the control (high-density springtails without spiders). The results suggest that additional prey density affects predatory interactions between M. denticulatus and R. padi and that erigonids, which occur in high densities in wheat fields in the Negev desert, may be involved in aphid suppression in these agroecosystems.

Identification of trophic interactions between <Emphasis Type="Italic">Macrolophus caliginosus</Emphasis> (Heteroptera: Miridae) and <Emphasis Type="Italic">Myzus persicae</Emphasis> (Homoptera: Aphididae) using real time PCR

Understanding food web interactions in native or agricultural ecosystems is an important step towards establishing sustainable pest management strategies. While the role of generalist predators as biological control agents is increasingly appreciated, the study of trophic interactions between individual predator species and their prey provides practical difficulties. Recently, different approaches have been suggested to determine prey items from predator guts using molecular methods. Macrolophus caliginosus is a generalist predator active in herbaceous agro-ecosystems. We developed a system to identify the DNA of its prey after ingestion, using Myzus persicae as a model. Esterase (MpEST) and cytochrome oxidase I (MpCOI) genes were targeted in the aphid, while M. caliginosus COI gene was used as control for predator DNA. Real time PCR proved to be specific and sensitive enough to detect prey DNA upon ingestion after feeding experiments. The system provided a linear amplification response with only 10 fg of prey genomic DNA as template. The detection system of MpCOI gene was more sensitive than MpEST, while the detection period was similar for both genes. Possibilities for using the system in ecological and biosafety studies with regard to sustainable pest management are discussed.

All "chick-a-dee" calls are not created equally. Part II. Mechanisms for discrimination by sympatric and allopatric chickadees

The 'chick-a-dee' call, common to all members of the genus Poecile, is used by both sexes throughout the year to putatively co-ordinate flock movements and register alarm. In some regions, two or more chickadee species occupy overlapping territories, and therefore it is essential that these sympatric species learn to discriminate between the acoustically similar calls of the species. Previous work from our laboratory has shown that black-capped (P. atricapillus) and mountain chickadees (P. gambeli) discriminate between the species' calls and treat each species' calls as belonging to separate open-ended categories. In the current set of experiments we use an operant conditioning paradigm to gain an understanding of (1) how the birds perform this discrimination and (2) whether birds with different levels of experience with heterospecific calls perform this task differently. We use natural recordings of chick-a-dee calls and perform several manipulations to test the importance of the introductory 'chick-a' portion and the terminal 'dee' portion for discriminating among the calls of the two species. Evidence suggests that birds mainly use the terminal 'dee' portion, as all groups of birds responded similarly to these probe stimuli and control chick-a-dee calls. We propose that the terminal 'dee' portion, consisting of lower frequency notes, is more likely to be resistant to degradation, and therefore a more reliable species-specific marker.     

Identifying the predator complex of <Emphasis Type="Italic">Homalodisca vitripennis</Emphasis> (Hemiptera: Cicadellidae): a comparative study of the efficacy of an ELISA and PCR gut content assay

A growing number of ecologists are using molecular gut content assays to qualitatively measure predation. The two most popular gut content assays are immunoassays employing pest-specific monoclonal antibodies (mAb) and polymerase chain reaction (PCR) assays employing pest-specific DNA. Here, we present results from the first study to simultaneously use both methods to identify predators of the glassy winged sharpshooter (GWSS), Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae). A total of 1,229 arthropod predators, representing 30 taxa, were collected from urban landscapes in central California and assayed first by means of enzyme-linked immunosorbent assay (ELISA) using a GWSS egg-specific mAb and then by PCR using a GWSS-specific DNA marker that amplifies a 197-base pair fragment of its cytochrome oxidase gene (subunit I). The gut content analyses revealed that GWSS remains were present in 15.5% of the predators examined, with 18% of the spiders and 11% of the insect predators testing positive. Common spider predators included members of the Salticidae, Clubionidae, Anyphaenidae, Miturgidae, and Corinnidae families. Common insect predators included lacewings (Neuroptera: Chrysopidae), praying mantis (Mantodea: Mantidae), ants (Hymenoptera: Formicidae), assassin bugs (Hemiptera: Reduviidae), and damsel bugs (Hemiptera: Nabidae). Comparison of the two assays indicated that they were not equally effective at detecting GWSS remains in predator guts. The advantages of combining the attributes of both types of assays to more precisely assess field predation and the pros and cons of each assay for mass-screening predators are discussed.     

Low light reflectance may explain the attraction of birds to defoliated trees

Plants use volatile organic compounds to attract invertebratepredators and parasitoids of their herbivore pests. Recently,it has been suggested that plants, either through visual orolfactory cues, may also "cry for help" from vertebrate predatorssuch as birds. We show that in a laboratory choice test, passerinebirds (Parus major and Cyanistes caeruleus) were attracted tothe intact branches of trees (Betula pendula) suffering fromfoliar damage caused by herbivore larvae (Epirrita autumnata)in nontest branches. Species, age, or sex of the experimentalbird or lighting (ultraviolet [UV] or non-UV) did not affectthe preference. However, the birds made a clear choice betweenthe treatments when the trees came from a forest patch receivingmore sunlight, whereas no obvious choice was observed when thetrees came from a shadier forest patch. Results of the choicetest were supported by the spectral reflectance of tree leaves.In the sunnier forest patch, control trees reflected more visiblelight than the herbivore trees, whereas no such difference wasfound in the shadier forest patch trees. We suggest that avianpredators use their vision within visible wavelengths to findinsect-rich plants even when they do not see the prey itemsor damaged leaves.     

Insect-resistant biotech crops and their impacts on beneficial arthropods

With a projected population of 10 billion by 2050, an immediate priority for agriculture is to achieve increased crop yields in a sustainable and cost-effective way. The concept of using a transgenic approach was realized in the mid-1990s with the commercial introduction of genetically modified (GM) crops. By 2010, the global value of the seed alone was US $11.2 billion, with commercial biotech maize, soya bean grain and cotton valued at approximately US $150 billion. In recent years, it has become evident that insect-resistant crops expressing δ-endotoxin genes from Bacillus thuringiensis have made a significant beneficial impact on global agriculture, not least in terms of pest reduction and improved quality. However, because of the potential for pest populations to evolve resistance, and owing to lack of effective control of homopteran pests, alternative strategies are being developed. Some of these are based on Bacillus spp. or other insect pathogens, while others are based on the use of plant- and animal-derived genes. However, if such approaches are to play a useful role in crop protection, it is desirable that they do not have a negative impact on beneficial organisms at higher trophic levels thus affecting the functioning of the agro-ecosystem. This widely held concern over the ecological impacts of GM crops has led to the extensive examination of the potential effects of a range of transgene proteins on non-target and beneficial insects. The findings to date with respect to both commercial and experimental GM crops expressing anti-insect genes are discussed here, with particular emphasis on insect predators and parasitoids.     

Maximizing collection and minimizing risk: does vacuum suction sampling increase the likelihood for misinterpretation of food web connections?

Molecular tools that characterize the structure of complex food webs and identify trophic connectedness in the field have become widely adopted in recent years. However, characterizing the intensity of predator-prey interactions can be prone to error. Maximizing collection success of small, fast-moving predators with vacuum suction samplers has the potential to increase the likelihood of prey DNA detection either through surface-level contamination with damaged prey or direct consumption within the sampling device. In this study, we used PCR to test the hypothesis that vacuum suction sampling will not cause an erroneous increase in the detection of 'predation', thereby incorrectly assigning trophic linkages when evaluating food web structure. We utilized general (1) Aphidoidea and (2) Collembola primers to measure the predation rates of Glenognatha foxi (Araneae: Tetragnathidae) on these prey collected by hand versus those sampled with a vacuum suction device. With both primer pairs, there was no significant increase in predators screening positive for prey DNA when sampled by vacuum suction versus those predators collected, in parallel, by hand. These results clearly validate the application of vacuum suction sampling during molecular gut-content analysis of predator-prey feeding linkages in the field. Furthermore, we found no evidence that predation was occurring inside the suction sampler because specimens collected were never observed to be feeding nor did they screen positive at greater frequencies than hand-collected individuals. Therefore, it can be concluded that the use of vacuum suction sampling devices (in this case a Modified CDC Backpack Aspirator Model 1412) is suitable for molecular gut-content analysis.     

Does maternal care evolve through egg recognition or directed territoriality?

The mechanism that facilitates the evolution of maternal care is ambiguous in egg‐laying terrestrial vertebrates: does the ability of mothers to recognize their own eggs lead them under some circumstances to begin providing care or can maternal care evolve from simply being in close proximity to the eggs (e.g. through territorial behaviour)? This question is difficult to answer because in most species, parental care is either absent altogether or present; in only a few species we have the opportunity to observe intraspecific variation in the expression of parental care. We studied a population of long‐tailed skinks (Eutropis longicaudata) in which females have recently evolved maternal care from a noncaring state. Females on Orchid Island, Taiwan, remain with their eggs during incubation and when doing so, actively deter egg predation by egg‐eating snakes (Oligodon formosanus); in all other populations, females lack post‐ovipositional maternal care. Nest‐guarding females on Orchid Island (i) showed antipredator behaviours only in the original nest site in which they laid eggs, even after we removed all of the eggs or substituted them with those of a conspecific; (ii) protect any eggs present inside the original nest site (even when the eggs belong to a conspecific); and (iii) develop this behaviour while gravid (i.e. prior to laying eggs). This supports the hypothesis that long‐tailed skinks cannot recognize their own eggs, suggesting that maternal care is a directed form of territoriality only expressed towards egg‐eating snakes and only during reproduction. Nest guarding is among the most primitive forms of parental care, and the recent evolution of this behaviour in a single population provides insight into one of the mechanisms by which parental care can originate in terrestrial vertebrates.