Intraspecific heritable variation in life-history traits can alter the outcome of interspecific competition among insect herbivores

Competition is one of the most important biotic factors determining the structure of ecological communities. In this study, we show that there is variation in competitive ability between two clones of the pea aphid, Acyrthosiphon pisum, both of which out-compete a clone of the vetch aphid, Megoura viciae, in the laboratory. We tested whether this variation in competitive ability would alter the outcome of interspecific competition in the field. White one pea aphid clone followed the pattern set in the laboratory, out-competing the Megoura viciae clone, another showed the reverse effect with Megoura viciae dominating. These differences appear to be the result of variation in early population growth rate between the pea aphid clones, rather than predation, although predation did lead to the eventual extinction of colonies. We also questioned whether intra- and interspecific differences in predator escape behaviour could affect the outcome of competition in the field. All three clones responded similarly to the presence of foraging hoverfly larvae (Episyrphus balteatus), but the Megoura viciae clone dropped from the plant significantly less often in response to the presence of a foraging two-spot ladybird (Adalia bipunctata). This work provides evidence that intraspecific variation in competitive ability can alter the outcome of interspecific competitive interactions in nature and suggests that species-specific behavioural. traits may have the potential to modify the outcome of these interactions. (c) 2005 Gesellschaft fur Okologie. Published by Elsevier GmbH. All rights reserved.

Fertilisers and insect herbivores: a meta-analysis

Despite the importance of a thorough understanding of the effect of synthetic fertiliser on insect population dynamics, existing literature is conflicting and an area of intense debate. Here, a categorical random-effects meta-analysis and a vote count meta-analysis are employed to examine the effects of nitrogen(N), phosphorus (P), potassium (K) and NPK fertiliser on insect population dynamics. In agreement with the general consensus, insects were found to respond positively, overall, to fertilisers. Sucking insects showed a much stronger response to fertilisers than chewing insects. The environment in which a study is conducted can have a marked effect on insect responses to fertiliser, with natural environments showing the potential for buffering effects of nitrogen fertilisers in particular. As well as highlighting the potential shortfall in the amount of research investigating particularly the effects of potassium and phosphorus, this study provides an invaluable flag post in the ongoing research investigating fertiliser effects on ecosystems.

An extreme case of plant-insect co-diversification: figs and fig-pollinating wasps

It is thought that speciation in phytophagous insects is often due to colonization of novel host plants, because radiations of plant and insect lineages are typically asynchronous. Recent phylogenetic comparisons have supported this model of diversification for both insect herbivores and specialized pollinators. An exceptional case where contemporaneous plant insect diversification might be expected is the obligate mutualism between fig trees (Ficus species, Moraceae) and their pollinating wasps (Agaonidae, Hymenoptera). The ubiquity and ecological significance of this mutualism in tropical and subtropical ecosystems has long intrigued biologists, but the systematic challenge posed by >750 interacting species pairs has hindered progress toward understanding its evolutionary history. In particular, taxon sampling and analytical tools have been insufficient for large-scale co-phylogenetic analyses. Here, we sampled nearly 200 interacting pairs of fig and wasp species from across the globe. Two supermatrices were assembled: on average, wasps had sequences from 77% of six genes (5.6kb), figs had sequences from 60% of five genes (5.5 kb), and overall 850 new DNA sequences were generated for this study. We also developed a new analytical tool, Jane 2, for event-based phylogenetic reconciliation analysis of very large data sets. Separate Bayesian phylogenetic analyses for figs and fig wasps under relaxed molecular clock assumptions indicate Cretaceous diversification of crown groups and contemporaneous divergence for nearly half of all fig and pollinator lineages. Event-based co-phylogenetic analyses further support the co-diversification hypothesis. Biogeographic analyses indicate that the presentday distribution of fig and pollinator lineages is consistent with an Eurasian origin and subsequent dispersal, rather than with Gondwanan vicariance. Overall, our findings indicate that the fig-pollinator mutualism represents an extreme case among plant-insect interactions of coordinated dispersal and long-term co-diversification.

Microbial impacts on plant-herbivore interactions: the indirect effects of a birch pathogen on a birch aphid

The role of indirect interactions in structuring communities is becoming increasingly recognised. Plant fungi can bring about changes in plant chemistry which may affect insect herbivores that share the same plant, and hence the two may interact indirectly. This study investigated the indirect effects of a fungal pathogen (Marssonina betulae) of silver birch (Betula pendula) on an aphid (Euceraphis betulae), and the processes underpinning the interaction. There was a strong positive association between natural populations of the aphid and leaves bearing high fungal infection. In choice tests, significantly more aphids settled on leaves inoculated with the fungus than on asymptomatic leaves. Individual aphids reared on inoculated leaves were heavier, possessed longer hind tibiae and displayed enhanced embryo development compared with aphids reared on asymptomatic leaves; population growth rate was also positively correlated with fungal infection when groups of aphids were reared on inoculated branches. Changes in leaf chemistry were associated with fungal infection with inoculated leaves containing higher concentrations of free-amino acids. This may reflect a plant-initiated response to fungal attack in which free amino acids from the degradation of mesophyll cells are translocated out of infected leaves via the phloem. These changes in plant chemistry are similar to those occurring during leaf senescence, and are proposed as the mechanistic basis for the positive interaction between the fungus and aphid.

Arthropod community structure in pastures of an island archipelago (Azores): looking for local-regional species richness patterns at fine-scales

The arthropod species richness of pastures in three Azorean islands was used to examine the relationship between local and regional species richness over two years. Two groups of arthropods, spiders and sucking insects, representing two functionally different but common groups of pasture invertebrates were investigated. The local-regional species richness relationship was assessed over relatively fine scales: quadrats (= local scale) and within pastures (= regional scale). Mean plot species richness was used as a measure of local species richness (= alpha diversity) and regional species richness was estimated at the pasture level (= gamma diversity) with the 'first-order-Jackknife' estimator. Three related issues were addressed: (i) the role of estimated regional species richness and variables operating at the local scale (vegetation structure and diversity) in determining local species richness; (ii) quantification of the relative contributions of alpha and beta diversity to regional diversity using additive partitioning; and (iii) the occurrence of consistent patterns in different years by analysing independently between-year data. Species assemblages of spiders were saturated at the local scale (similar local species richness and increasing beta-diversity in richer regions) and were more dependent on vegetational structure than regional species richness. Sucking insect herbivores, by contrast, exhibited a linear relationship between local and regional species richness, consistent with the proportional sampling model. The patterns were consistent between years. These results imply that for spiders local processes are important, with assemblages in a particular patch being constrained by habitat structure. In contrast, for sucking insects, local processes may be insignificant in structuring communities.

Potential contribution of natural enemies to patterns of local adaptation in plants

Genetic differentiation among plant populations and adaptation to local environmental conditions are well documented. However, few studies have examined the potential contribution of plant antagonists, such as insect herbivores and pathogens, to the pattern of local adaptation. Here, a reciprocal transplant experiment was set up at three sites across Europe using two common plant species, Holcus lanatus and Plantago lanceolata. The amount of damage by the main above-ground plant antagonists was measured: a rust fungus infecting Holcus and a specialist beetle feeding on Plantago, both in low-density monoculture plots and in competition with interspecific neighbours. Strong genetic differentiation among provenances in the amount of damage by antagonists in both species was found. Local provenances of Holcus had significantly higher amounts of rust infection than foreign provenances, whereas local provenances of Plantago were significantly less damaged by the specialist beetle than the foreign provenances. The presence of surrounding vegetation affected the amount of damage but had little influence on the ranking of plant provenances. The opposite pattern of population differentiation in resistance to local antagonists in the two species suggests that it will be difficult to predict the consequences of plant translocations for interactions with organisms of higher trophic levels.

Summer drought alters plant-mediated competition between foliar- and root-feeding insects

Summer droughts are predicted to increase in severity and frequency in the United Kingdom, due to climate change. Few studies have addressed the impacts of drought on interactions between species, and the majority have focussed on increases in CO2 concentration and changes in temperature. Here, the effect of experimental summer drought on the strength of the plant-mediated interaction between leaf-mining Stephensia brunnichella larvae and root-chewing Agriotes larvae was investigated. Agriotes larvae reduced the abundance and performance of S. brunnichella feeding on a mutual host plant, Clinopodium vulgare, as well as the rate of parasitism of the leaf-miner. The interaction did not, however, occur on plants subjected to a severe drought treatment, which were reduced in size. Changes to summer rainfall, due to climate change, may therefore reduce the occurrence of plant-mediated interactions between insect herbivores.

Are polyphagous geometrid moths with flightless females adapted to budburst phenology of local host species?

The majority of studies demonstrating local adaptation of insect herbivores involve sessile species, particularly those with a parthenogentic phase to their life history or endophagous "parasites" of plants. Current arguments suggest the strength of selection determines whether local adaptation can or cannot take place. Therefore local adaptation should not be limited to species with such traits. We studied the ability of three polyphagous geometrid moths with flightless adult females (Erannisdefoliaria, Operophtera brumata and O. fagata) to synchronise their egg hatching with the budburst of a local host species in north east Scotland. A strong selection for hatching time is expected among generalist moths given the large variation in budburst phenology and an inability to hatch in synchrony with budburst decreases moth fitness substantially. In two successive seasons, we trapped emerging females from patches of five host species and recorded the temperature sum needed for 50% egg hatch of each brood laid by the trapped females. The hatching times of broods were compared against the average budburst time of the maternal host species in the study area. In addition, the trapping dates of each female were recorded. Only O. brumata showed synchrony with egg hatch and budburst which suggests local phenological adaptation to different host species. This could be maintained by selection and partial reproductive isolation between populations dwelling on different host species. No phenological adaptation was found in the other common geometrids of the study area

Intra-specific variation affects the structure of the natural enemy assemblage attacking pea aphid colonies

1. Intra-specific variation in plant defence traits has been shown to profoundly affect herbivore community structure. Here we describe two experiments designed to test whether similar effects occur at higher trophic levels, by studying pea aphid–natural enemy interactions in a disused pasture in southern England. 2. In the first experiment, the numbers and identity of natural enemies attacking different monoclonal pea aphid colonies were recorded in a series of assays throughout the period of pea aphid activity. 3. In the summer assay, there was a significant effect of clone on the numbers of aphidophagous hoverfly larvae and the total number of non-hoverfly natural enemies recruited. Clone also appeared to influence the attack rate suffered by the primary predator in the system, the hoverfly Episyrphus balteatus, by Diplazon laetatorius, an ichneumonid parasitoid. Colonies were generally driven to extinction by hoverfly attack, resulting in the recording of low numbers of parasitoids and entomopathogens, suggesting intense intra-guild predation. 4. To further examine the influence of clonal variation on the recruitment of natural enemies, a second experiment was performed to monitor the temporal dynamics of community development. Colonies were destructively sampled every other day and the numbers of natural enemies attacking aphid colonies were recorded. These data demonstrated that clonal variation influenced the timing, abundance, and identity of natural enemies attacking aphid colonies. 5. Taken together, these data suggest that clonal variation may have a significant influence on the patterns of interactions between aphids and their natural enemies, and that such effects are likely to affect our understanding of the ecology and biological control of these insect herbivores.

Extreme host plant conservatism during at least 20 million years of host plant pursuit by oak gallwasps

Diversification of insect herbivores is often associated with coevolution between plant toxins and insect countermeasures, resulting in a specificity that restricts host plant shifts. Gall inducers, however, bypass plant toxins and the factors influencing host plant associations in these specialized herbivores remain unclear. We reconstructed the evolution of host plant associations in Western Palaearctic oak gallwasps (Cynipidae: Cynipini), a species-rich lineage of specialist herbivores on oak (Quercus). (1) Bayesian analyses of sequence data for three genes revealed extreme host plant conservatism, with inferred shifts between major oak lineages (sections Cerris and Quercus) closely matching the minimum required to explain observed diversity. It thus appears that the coevolutionary demands of gall induction constrain host plant shifts, both in cases of mutualism (e.g., fig wasps, yucca moths) and parasitism (oak gallwasps). (2) Shifts between oak sections occurred independently in sexual and asexual generations of the gallwasp lifecycle, implying that these can evolve independently. (3) Western Palaearctic gallwasps associated with sections Cerris and Quercus diverged at least 20 million years ago (mya), prior to the arrival of oaks in the Western Palaearctic from Asia 5-7 mya. This implies an Asian origin for Western Palaearctic gallwasps, with independent westwards range expansion by multiple lineages.

Influence of elevated CO2 on interspecific interactions at higher trophic levels

We report the results of a study investigating the influence of elevated CO2 on species interactions across three trophic levels: a plant (Brassica oleracea), two aphid herbivores (the generalist Myzus persicae and the specialist Brevicoryne brassicae), and two natural enemies (the coccinellid Hippodamia convergens (ladybird) and the parasitoid wasp Diaeretiella rapae). Brassica oleracea plants reared under elevated CO2 conditions (650 ppmv vs. 350 ppmv) were larger and had decreased water and nitrogen content. Brevicoryne brassicae reared on plants grown in elevated CO2 were larger and accumulated more fat, while there was no change in M. persicae traits. Fecundity of individual aphids appeared to be increased when reared on plants grown in elevated CO2. However, these differences were generally lost when aphids were reared in colonies, suggesting that such changes in plant quality will have subtile effects on aphid intraspecific interactions. Nevertheless, CO2 treatment did influence aphid distribution on plants, with significantly fewer M. persicae found on the shoots, and B. brassicae was only found on senescing leaves, when colonies were reared on plants grown in elevated CO2. We reared B. brassicae and M. persicae in competition on plants grown at both the CO2 concentration treatments. We found a significantly lower ratio of M. persicae: B. brassicae on plants grown under elevated CO2 conditions, strongly suggesting that increasing CO2 concentrations can alter the outcome of competition among insect herbivores. This was also reflected in the distribution of the aphids on the plants. While the CO2 treatment did not influence where B. brassicae were found, fewer M. persicae were present on senescing leaves under elevated CO2 conditions. Changes in plant quality resulting from the CO2 treatments did not appear to alter aphid quality as prey species, as the number consumed by the ladybird H. convergens, and the number parasitised by the parasitoid wasp D. rapae, did not change. To our knowledge, this study provides the first empirical evidence that changes in host plant quality mediated by increasing levels of CO2 can alter the outcome of interspecific competition among insect herbivores.

Elevated atmospheric carbon dioxide impairs the performance of root-feeding vine weevils by modifying root growth and secondary metabolites

Predicting how insect crop pests will respond to global climate change is an important part of increasing crop production for future food security, and will increasingly rely on empirically based evidence. The effects of atmospheric composition, especially elevated carbon dioxide (eCO(2)), on insect herbivores have been well studied, but this research has focussed almost exclusively on aboveground insects. However, responses of root-feeding insects to eCO(2) are unlikely to mirror these trends because of fundamental differences between aboveground and belowground habitats. Moreover, changes in secondary metabolites and defensive responses to insect attack under eCO(2) conditions are largely unexplored for root herbivore interactions. This study investigated how eCO(2) (700 mu mol mol-1) affected a root-feeding herbivore via changes to plant growth and concentrations of carbon (C), nitrogen (N) and phenolics. This study used the root-feeding vine weevil, Otiorhynchus sulcatus and the perennial crop, Ribes nigrum. Weevil populations decreased by 33% and body mass decreased by 23% (from 7.2 to 5.4 mg) in eCO(2). Root biomass decreased by 16% in eCO(2), which was strongly correlated with weevil performance. While root N concentrations fell by 8%, there were no significant effects of eCO(2) on root C and N concentrations. Weevils caused a sink in plants, resulting in 8-12% decreases in leaf C concentration following herbivory. There was an interactive effect of CO(2) and root herbivory on root phenolic concentrations, whereby weevils induced an increase at ambient CO(2), suggestive of defensive response, but caused a decrease under eCO(2). Contrary to predictions, there was a positive relationship between root phenolics and weevil performance. We conclude that impaired root-growth underpinned the negative effects of eCO(2) on vine weevils and speculate that the plant's failure to mount a defensive response at eCO(2) may have intensified these negative effects.

Effects of organic and conventional fertiliser treatments on host selection by the aphid parasitoid Diaeretiella rapae

The type and quantity of fertilizer supplied to a crop will differ between organic and conventional farming practices. Altering the type of fertilizer a plant is provided with can influence a plant’s foliar nitrogen levels, as well as the composition and concentration of defence compounds, such as glucosinolates. Many natural enemies of insect herbivores can respond to headspace volatiles emitted by the herbivores’ host plant in response to herbivory. We propose that manipulating fertilizer type may also influence the headspace volatile profiles of plants, and as a result, the tritrophic interactions that occur between plants, their insect pests and those pests’ natural enemies. Here, we investigate a tritrophic system consisting of cabbage plants, Brassica oleracea, a parasitoid, Diaeretiella rapae, and one of its hosts, the specialist cabbage aphid Brevicoryne brassicae. Brassica oleracea plants were provided with either no additional fertilization or one of three types of fertilizer: Nitram (ammonium nitrate), John Innes base or organic chicken manure. We investigated whether these changes would alter the rate of parasitism of aphids on those plants and whether any differences in parasitism could be explained by differences in attractivity of the plants to D. rapae or attack rate of aphids by D. rapae. In free-choice experiments, there were significant differences in the percentage of B. brassicae parasitized by D. rapae between B. oleracea plants grown in different fertilizer treatments. In a series of dual-choice Y-tube olfactometry experiments, D. rapae females discriminated between B. brassicae-infested and undamaged plants, but parasitoids did not discriminate between similarly infested plants grown in different fertilizer treatments. Correspondingly, in attack rate experiments, there were no differences in the rate that D. rapae attacked B. brassicae on B. oleracea plants grown in different fertilizer treatments. These findings are of direct relevance to sustainable and conventional farming practices.

Thorn-dwelling ants provide antiherbivore defence for camelthorn trees, Vachellia erioloba, in Namibia

Ants are widely employed by plants as an antiherbivore defence. A single host plant can associate with multiple, symbiotic ant species, although usually only a single ant species at a time. Different plant-ant species may vary in the degree to which they defend their host plant. In Kenya, ant–acacia interactions are well studied, but less is known about systems elsewhere in Africa. A southern African species, Vachellia erioloba, is occupied by thorn-dwelling ants from three different genera. Unusually, multiple colonies of all these ants simultaneously and stably inhabit trees. We investigated if the ants on V. erioloba (i) deter insect herbivores; (ii) differ in their effectiveness depending on the identity of the herbivore; and (iii) protect the tree against an important herbivore, the larvae of the lepidopteran Gonometa postica. We show that experimental exclusion of ants leads to greater levels of herbivory on trees. The ants inhabiting V. erioloba are an effective deterrent against hemipteran and coleopteran, but not lepidopteran herbivores. Defensive services do not vary among ant species, but only Crematogaster ants exhibit aggression towards G. postica. This highlights the potential of the V. erioloba–ant mutualism for studying ant–plant interactions that involve multiple, simultaneously resident thorn-dwelling ant species.