RESUMEN
A generalist predator's ability to contribute to biological control is influenced by the decisions it makes during foraging. Predators often use flexible foraging tactics, which allows them to pursue specific types of prey at the cost of reducing the likelihood of capturing other types of prey. When a pest insect has low nutritional quality or palatability for a predator, the predator is likely to reject that prey in favour of pursuing alternative, non-pest prey. This is often thought to limit the effectiveness of generalist predators in consuming aphids, which are of low nutritional quality for many generalist predators. Here, we report behavioural assays that test the hypothesis that the generalist predator, Grammonota inornata (Araneae: Linyphiidae), preferentially forages for a non-pest prey with high nutritional quality (springtails), and rejects a pest prey with low nutritional quality (aphids). In no-choice assays, molecular gut-content analysis revealed that spiders continued to feed on the low-quality aphids at high rates, even when high-quality springtails were readily available. When provided a choice between aphids and springtails in two-way choice tests, spiders did not show the expected preference for springtails. Decision-making by spiders during foraging therefore appears to be sub-optimal, possibly because of attraction to the less frequently encountered of two preys as part of a dietary diversification strategy. These results indicate that behavioural preferences alone do not necessarily compromise the pest-suppression capacity of natural enemies: even nutritionally sub-optimal pest prey can potentially be subject to predation and suppression by natural enemies.
Asunto(s)
Áfidos/fisiología , Cadena Alimentaria , Conducta Predatoria , Arañas/fisiología , Animales , Femenino , Control Biológico de VectoresRESUMEN
In many arthropods, maternally inherited endosymbiotic bacteria can increase infection frequency by manipulating host reproduction. Multiple infections of different bacteria in a single host population are common, yet few studies have documented concurrent endosymbiont phenotypes or explored their potential interactions. We hypothesized that spiders might be a particularly useful taxon for investigating endosymbiont interactions, because they are host to a plethora of endosymbiotic bacteria and frequently exhibit multiple infections. We established two matrilines from the same population of the linyphiid spider Mermessus fradeorum and then used antibiotic curing and controlled mating assays to demonstrate that each matriline was subject to a distinct endosymbiotic reproductive manipulation. One matriline was co-infected with Rickettsia and Wolbachia and produced offspring with a radical female bias. Antibiotic treatment eliminated both endosymbionts and restored an even sex ratio to subsequent generations. Chromosomal and fecundity observations suggest a feminization mechanism. In the other matriline, a separate factorial mating assay of cured and infected spiders demonstrated strong cytoplasmic incompatibility (CI) induced by a different strain of Wolbachia. However, males with this Wolbachia induced only mild CI when mated with the Rickettsia-Wolbachia females. In a subsequent survey of a field population of M. fradeorum, we detected these same three endosymbionts infecting 55% of the spiders in almost all possible combinations, with nearly half of the infected spiders exhibiting multiple infection. Our results suggest that a dynamic network of endosymbionts may interact both within multiply infected hosts and within a population subject to multiple strong reproductive manipulations.
Asunto(s)
Rickettsia , Razón de Masculinidad , Arañas/genética , Arañas/microbiología , Simbiosis , Wolbachia , Animales , Femenino , Fertilidad , Masculino , FenotipoRESUMEN
The area planted to genetically engineered crops has increased dramatically in the last ten years. This has generated many studies examining non-target effects of bioengineered plants expressing Bacillus thuringiensis endotoxins. To date, most have focused on population-level effects in the field or laboratory evaluation of specific plant-herbivore or plant-herbivore-predator trophic pathways. Using a post-mortem enzyme-linked immunosorbent assay, we examined the uptake of Cry1Ab-endotoxins by predatory coccinellids and the importance of anthesis to this trophic pathway. Adult Coleomegilla maculata, Harmonia axyridis, Cycloneda munda and Coccinella septempunctata contained low, but detectable, quantities of Bt-endotoxin when screened by ELISA. This was most evident in C. maculata, with 12.8% of 775 individuals testing positive for Cry1Ab-endotoxins. Interestingly, the presence of endotoxins in gut samples was not confined to periods around anthesis, but coccinellid adults tested positive two weeks before and up to ten weeks after pollen was shed, suggesting tri-trophic linkages in their food chain facilitates the transfer of endotoxins into higher-order predators. This contrasts with adult Coleomegilla maculata entering overwintering sites where Bt-endotoxins were not detected in gut samples, indicating low levels of persistence of Cry1Ab-endotoxins within coccinellid predators. This study enhances our understanding of complex interactions between transgenic crops and non-target food webs, but further research is required to quantify the significance of specific trophic linkages in the field.
Asunto(s)
Proteínas Bacterianas/análisis , Toxinas Bacterianas/análisis , Escarabajos/química , Endotoxinas/análisis , Cadena Alimentaria , Proteínas Hemolisinas/análisis , Animales , Toxinas de Bacillus thuringiensis , Proteínas Bacterianas/metabolismo , Toxinas Bacterianas/metabolismo , Endotoxinas/metabolismo , Tracto Gastrointestinal/química , Proteínas Hemolisinas/metabolismo , Polen/metabolismo , Factores de Tiempo , Zea mays/metabolismo , Zea mays/fisiologíaRESUMEN
The utility of temperature gradient gel electrophoresis (TGGE) as a means of analysing the gut contents of predators was evaluated. Generalist predators consume multiple prey species and a species-specific primer approach may not always be a practical means of analysing predator responses to prey diversity in complex and biodiverse ecosystems. General invertebrate primers were used to amplify the gut contents of predators, generating banding patterns that identified component prey remains. There was no evidence of dominance of the polymerase chain reaction (PCR) by predator DNA. When applied to field samples of the carabid predator Pterostichus melanarius (Illiger) nine banding patterns were detected, including one for aphids. To further distinguish between species, group-specific primers were designed to separate species of earthworm and aphid. TGGE of the earthworm PCR products generated banding patterns that varied with haplotype in some species. Aphid and earthworm DNA could be detected in the guts of carabids for up to 24 h using TGGE. In P. melanarius, with low numbers of prey per insect gut (mean<3), interpretation of banding patterns proved to be tractable. Potential problems of interpretation of TGGE gels caused by multiple prey bands, cryptic bands, haplotype variation, taxonomic uncertainties (especially with regard to earthworms), secondary predation, scavenging and presence of parasites and parasitoids in the prey or the predators, are discussed. The results suggest that PCR, using combinations of general invertebrate and group-specific primers followed by TGGE, provides a potentially useful approach to the analysis of multiple uncharacterized prey in predators.
Asunto(s)
Escarabajos/metabolismo , Electroforesis en Gel de Poliacrilamida/veterinaria , Invertebrados/clasificación , Invertebrados/metabolismo , Animales , Áfidos/genética , Escarabajos/genética , Cartilla de ADN/química , Digestión/fisiología , Complejo IV de Transporte de Electrones/genética , Electroforesis en Gel de Poliacrilamida/métodos , Femenino , Mucosa Intestinal/metabolismo , Invertebrados/genética , Masculino , Datos de Secuencia Molecular , Oligoquetos/genética , Reacción en Cadena de la Polimerasa/veterinaria , ARN Ribosómico/genética , Factores de TiempoRESUMEN
Environment-friendly farming techniques seek to increase invertebrate biodiversity in part with the intention of encouraging greater numbers of predators that will help to control crop pests. However, in theory, this effect may be negated if the availability of a greater abundance and diversity of alternative prey diverts predators away from feeding on pests. The hypothesis that access to alternative prey can lead to reduced pest suppression under semi-field conditions was tested. Alternative prey type and diversity were manipulated in 70 mesocosms over 7+ weeks in the presence of the carabid Pterostichus melanarius (Illiger), a known predator of slugs, and reproducing populations of the slug Deroceras reticulatum (Müller). Significantly fewer slugs survived where no alternative prey were provided. Maximum slug numbers and biomass were found in treatments containing either carabids plus a high diversity of alternative prey (many species of earthworm and three of Diptera larvae) or a single additional prey (blowfly larvae, Calliphora vomitoria Linnaeus). In these treatments slug numbers and biomass were as high as in plots lacking predators. The effects of alternative prey were taxon-specific. Alternative prey strongly affected carabid fitness in terms of biomass and egg load. The fittest predators (those with access to high alternative prey diversity or C. vomitoria larvae) reduced slug numbers the least. The mean individual slug weights were greater in treatments with alternative prey than where no alternative prey were provided to the carabids. These results suggest that pests may survive and reproduce more rapidly in patches where predators have access to alternative prey.
Asunto(s)
Escarabajos/fisiología , Ecosistema , Gastrópodos , Control Biológico de Vectores/métodos , Conducta Predatoria , Animales , Tamaño CorporalRESUMEN
The drive towards a more sustainable and integrated approach to pest management has engendered a renewed interest in conservation biological control, the role of natural enemy communities and their interactions with prey. Monoclonal antibodies have provided significant advances in enhancing our knowledge of trophic interactions and can be employed to help quantify predation on target species. The tetragnathid spider Pachygnatha degeeri Sundevall was collected from fields of winter wheat in the UK and assayed by ELISA for aphid proteins. It was demonstrated that this spider did not simply consume greater quantities of aphids because it was bigger. In addition, P. degeeri contained significantly greater concentrations of aphid in their guts than other spiders, showing that aphids comprised a greater proportion of their diet. Although P. degeeri constituted only 6% of the spider population numerically, females and males respectively contained 16% and 37% of total aphid proteins within all spiders screened, significantly more than their density would predict. These spiders also preyed upon aphids at a disproportionately high rate in June, during the aphid establishment phase, theoretically the best time for limiting growth in the aphid population. Although less abundant than other generalist predators, the capability of these hunting spiders to consume large numbers of aphids highlights them as a more significant component of the predator complex than had previously been realized. Limitation of aphid numbers early in the year by generalist predators provides more time for the specialist aphid predators and parasitoids to move in.
Asunto(s)
Anticuerpos Monoclonales/inmunología , Conducta Alimentaria/fisiología , Control Biológico de Vectores/métodos , Arañas/fisiología , Análisis de Varianza , Animales , Áfidos/inmunología , Ensayo de Inmunoadsorción Enzimática/métodos , Cadena Alimentaria , Contenido Digestivo , Proteínas de Insectos/análisis , Reino UnidoRESUMEN
Molecular detection systems used to analyse the gut contents of invertebrate predators have enhanced our understanding of trophic interactions, but do not distinguish between the methods of consumption. Many predators regularly scavenge, which could have profound implications for quantitative analyses of the dynamics of predation. We report the first quantified assessment of the potential error caused by scavenging in post-mortem measurements of predation in a slug-carabid system. An anti-slug monoclonal antibody was able to detect antigens from decayed slugs after surprisingly long periods, significantly longer on relatively sterile peat than on natural soil. On soil the half-life of antibody-detectable slug proteins was 8.2 days while on peat it was 11.5 days. When slugs that had decayed on soil for 100 h were fed to the carabid predator Pterostichus melanarius, slug proteins could still be identified after 6 h (but not 12 h) digestion. Fresh and decayed slug was eaten in equal quantities by the beetles suggesting no aversion to the latter. The results suggest that significant errors may be caused by scavenging leading to inaccurate interpretation of predation rates in the field.
Asunto(s)
Escarabajos/fisiología , Moluscos/química , Conducta Predatoria/fisiología , Animales , Anticuerpos Monoclonales , Sistema Digestivo/química , Conducta Alimentaria/fisiología , Proteínas/análisis , Factores de TiempoRESUMEN
DNA-based techniques are providing valuable new approaches to tracking predator-prey interactions. The gut contents of invertebrate predators can be analysed using species-specific primers to amplify prey DNA to confirm trophic links. The problem is that each predator needs to be analysed with primers for the tens of potential prey available at a field site, even though the mean number of species detected in each gut may be as few as one or two. Conducting all these PCRs (polymerase chain reactions) is a lengthy process, and effectively precludes the analysis of the hundreds of predators that might be required for a meaningful ecological study. We report a rapid, more sensitive and practical approach. Multiplex PCRs, incorporating fluorescent markers, were found to be effective at amplifying degraded DNA from predators' guts and could amplify mitochondrial DNA fragments from 10+ species simultaneously without 'drop outs'. The combined PCR products were then separated by size on polyacrylamide gels on an ABI377 sequencer. New primers to detect the remains of aphids, earthworms, weevils and molluscs in the guts of carabid predators were developed and characterized. The multiplex-sequencer approach was then applied to field-caught beetles, some of which contained DNA from as many as four different prey at once. The main prey detected in the beetles proved to be earthworms and molluscs, although aphids and weevils were also consumed. The potential of this system for use in food-web research is discussed.
Asunto(s)
Cadena Alimentaria , Contenido Digestivo/química , Pruebas Genéticas/métodos , Invertebrados/genética , Reacción en Cadena de la Polimerasa/métodos , Animales , Cartilla de ADN , ADN Mitocondrial/genética , Colorantes Fluorescentes , Invertebrados/fisiología , Técnicas de Amplificación de Ácido Nucleico , Análisis de Regresión , Análisis de Secuencia de ADN , Especificidad de la EspecieRESUMEN
Collembola comprise a major source of alternative prey to linyphiid spiders in arable fields, helping to sustain and retain these predators as aphid control agents within the crop. Polymerase chain reaction primers were developed for the amplification, from spider gut samples, of DNA from three of the most abundant species of Collembola in wheat crops in Europe, namely Isotoma anglicana, Lepidocyrtus cyaneus and Entomobrya multifasciata. The primers amplified fragments of the mitochondrial cytochrome oxidase subunit I (COI) gene and were designed following alignment of comparable sequences for a range of predator and prey species. Each of the primer pairs proved to be species-specific to a Collembola species, amplifying DNA fragments from 211 to 276 base pairs in length. Following consumption of a single collembolan, prey DNA was detectable in 100% of spiders after 24 h of digestion. We report the first use of DNA-based techniques to detect predation by arthropods on natural populations of prey in the field. All three species of Collembola were consumed by the spiders. By comparing the ratios of the Collembola species in the field with the numbers of spiders that gave positive results for each of those species, it was possible to demonstrate that the spiders were exercising prey choice. Overall, a single target species of Collembola was eaten by 48% of spiders while a further 16% of spiders contained DNA from two different species of Collembola. Preference was particularly evident for I. anglicana, the species most frequently found in spider guts yet the least numerous of the three target species in the field.
Asunto(s)
Conducta Alimentaria/fisiología , Cadena Alimentaria , Insectos/genética , Arañas/fisiología , Animales , Secuencia de Bases , Cartilla de ADN , Complejo IV de Transporte de Electrones/genética , Electroforesis en Gel de Agar , Contenido Digestivo , Datos de Secuencia Molecular , Análisis de Secuencia de ADN , Especificidad de la Especie , Reino UnidoRESUMEN
"Secondary predation" occurs when one predator feeds on a second predator, which has in turn eaten a target prey. Detection of prey remains within predators using monoclonal antibodies cannot distinguish between primary and secondary predation, potentially leading to quantitative and qualitative food chain errors. We report the first fully replicated experiments to measure secondary predation effects, using an aphid-spider-carabid system. Aphids, Sitobion avenae, were fed to spiders, Lepthyphantes tenuis, which were allowed to digest their prey for a range of time intervals. The spiders were then fed to carabids, Poecilus (=Pterostichus) cupreus, which were again allowed to digest their prey for set periods. The anti-aphid monoclonal antibody used to identify S. avenae remains in P. cupreus was one that detected an epitope that increased in availability over the first few hours of digestion, amplifying the signal, extending detection periods and thus increasing the chances of detecting secondary predation. Despite this, and the fact that spiders are known to digest their prey more slowly than many other predators, detection of secondary predation was only possible if the carabids were killed immediately after consuming at least two spiders which were, in turn, eaten immediately after consuming aphids. As this scenario is unlikely to occur frequently in the field it was concluded that secondary predation is unlikely to be a serious source of error during field studies.