Enemy-free Space Research Articles

Trait-mediated trophic cascade creates enemy-free space for nesting hummingbirds.

The indirect effects of predators on nonadjacent trophic levels, mediated through traits of intervening species, are collectively known as trait-mediated trophic cascades. Although birds are important predators in terrestrial ecosystems, clear examples of trait-mediated indirect effects involving bird predators have almost never been documented. Such indirect effects are important for structuring ecological communities and are likely to be negatively impacted by habitat fragmentation, climate change, and other factors that reduce abundance of top predators. We demonstrate that hummingbirds in Arizona realize increased breeding success when nesting in association with hawks. An enemy-free nesting space is created when jays, an important source of mortality for hummingbird nests, alter their foraging behavior in the presence of their hawk predators.

The influence of aphids (Myzus persicae) and pink lady beetle larvae (Coleomegilla maculata) on host plant preference of imported cabbageworm (Pieris rapae)

Oviposition decisions by herbivorous insects hinge on multiple factors, with some of the most important being enemy-free space and competition for resources. It is important to understand whether and how herbivores and predators can influence the maternal egg-laying preference when they are alone and in combination with host plants. Here, we evaluate whether the presence of aphids (a competitor) or a lady beetle larvae (a predator) influence host plant selection by an ovipositing butterfly. Canola (Brassica napus L.) was the highest quality of three putative Brassicaceae host plants for aphids Myzus persicae (Sulzer) (Hemiptera: Aphididae), while the butterfly Pieris rapae (L.) (Lepidoptera: Pieridae) showed similar survival on all. Canola was used to determine that the presence of a competitor herbivore (aphids) had no effect on butterfly oviposition behavior. However, predators significantly influenced the number of eggs laid on the plants, especially on those plants that had both aphids and a lady beetle larva present in combination. We expect that adult female P. rapae did not lay their eggs on the treatment that involved both herbivorous competition and predation risk, due to the combined risk factors along with the volatile chemicals and aphid alarm pheromones emitted on those plants that contained both the aphids and lady beetle larva.

Plant secretions prevent wasp parasitism in nests of wool-carder bees, with implications for the diversification of nesting materials in Megachilidae

Bees make use of plant substrates in more ways than any other group of insects, which is probably linked to their diversification and ecological success. The highly diverse Megachilidae use a wide range of plant-derived brood cell-building materials, including plant leaves, mortar made from plant tissue, resin, plant hairs (‘plant wool’), and plant trichome secretions. While certain plant-derived materials are believed to protect nests against microbial decay, this has not been tested, and the factors driving diversification of nesting materials are poorly understood. Here, we investigated the protective effects of plant-derived extrafloral trichome secretions which female European wool-carder bees, Anthidium manicatum, smear on their brood cells. By breeding bees in cages with differential resource supply we generated brood cells with or without trichome secretions. Brood cells with trichome secretions were less attractive to parasitic wasps (Monodontomerus obscurus) in Y-maze olfactometer tests. Also, when exposed at sites where A. manicatum occurs in natural populations, brood cells smeared with trichome secretions were less affected by wasp (Melittobia acasta) parasitism than those without trichome secretions. On the other hand, trichome secretions did not prevent the growth of mold on brood cells, and larval mortality due to microbial decay was almost non-existent even when brood cells were exposed to rainfall. We conclude that the use of plant trichome secretion for brood cell construction has more likely evolved to create enemy-free space in response to chalcidoid wasp parasitism. Parasitoids are likely an underestimated cause of the diversification of cell construction materials and adaptive radiation in megachilid bees.

A positive association between ants and spiders and potential mechanisms driving the pattern

Biotic interactions play a central role in determining species distribution and abundance. Some ants act as keystone species affecting the distribution and abundance of other species, including spiders. In coffee plantationsPocobletussp. spiders are significantly more abundant in coffee plants patrolled by the aggressive arboreal antsAzteca sericeasur. However, it is unknown if other ant species influence this ant–spider association, how these associates are spatially distributed, and which are the potential drivers of this association. Here we examine the influence of ants,Azteca sericeasurandPheidole synanthropica, and coffee branch density onPocobletusabundance in a coffee farm in southern Mexico. We also analyze the spatial distribution and abundance ofPocobletussp., in relation to the spatial distribution ofA. sericeasurandP. synanthropica. Finally, we examine prey availability and enemy‐free space as potential mechanisms underlying this ant–spider association. Results show thatPocobletusabundance is positively correlated with coffee branch density andA. sericeasurandP. synanthropicapresence. Furthermore, the spatial distribution analysis shows that in 20 × 20 m plotsPocobletusis strongly associated toA. sericeasur,but not toP. synanthropica. Results show that insect abundance in bothPocobletus's webs and sticky traps was significantly higher in the presence ofA. sericeasurwhereas the abundance of the predators ofPocobletusdecreased inA. sericeasur'spresence; suggesting positive direct and indirect effects ofA. sericeasuronPocobletus. Overall, this study highlights the strong influence of ants and plant characteristics on the abundance and spatial distribution of spiders as well their indirect effects on other taxa.

Enemy-free space for parasitoids.

Natural enemies often cause significant levels of mortality for their prey and thus can be important agents of natural selection. It follows, then, that selection should favor traits that enable organisms to escape from their natural enemies into "enemy-free space" (EFS). Natural selection for EFS was originally proposed as a general force in structuring ecological communities, but more recently has become conceptually narrow and is typically only invoked when studying the evolutionary ecology of host plant use by specialized insect herbivores. By confining the application of EFS to specialist herbivores, its potential value to community and evolutionary ecology has been marginalized. As a first step toward exploring the potential explanatory power of EFS in structuring ecological niches of higher trophic-level organisms, we consider host use by parasitoids. Here, we present three distinct mechanisms from our studies of caterpillar host-parasitoid interactions suggesting that parasitoids may be under selection to exploit traits of their hosts and the plants on which those hosts feed to garner EFS for their developing offspring. The neglect of EFS as a top-down selective force on host use by parasitoids may be a serious limitation to basic and applied ecology, given the great diversity of parasitoids and their significance in controlling herbivore populations in both natural and managed ecosystems. Parasitoids and other mesopredators represent excellent candidates for further developments of EFS theory and testing of its broader importance.

Preference for isolated host plants facilitates invasion ofDanaus chrysippus(Linnaeus, 1758) (Lepidoptera: Nymphalidae) by a bacterial male-killerSpiroplasma

Matrilinearly inherited endosymbiotic bacteria are estimated to occur in a third of all terrestrial arthropods. They include male killers, which are typically associated with organisms that lay their eggs in batches. Batch laying favours male-killing bacteria because infected female larvae can cannibalise dead brothers and do not have to compete with them for larval resources. This paper tackles the paradox of high male-killer infection rates in Danaus chrysippus (Linnaeus, 1758), a butterfly that lays its eggs singly rather than in batches, making the selective advantage of male killing for the bacterium hard to understand. The study was conducted in the Nairobi region of Kenya where two substantially allopatric but seasonally migratory semispecies of Danaus chrysippus overlap and hybridise. Within this hybrid zone, but apparently not outside it, D. chrysippus hosts the endosymbiotic male killer, Spiroplasma ixodetis. In Nairobi, this bacterium can infect up to 95% of females. Semispecies D. chrysippus chrysippus and its hybrid with D. chrysippus dorippus (form transiens) are heavily infected, unlike the parental pure D. chrysippus dorippus semispecies, which may be protected by a suppressor gene. We find that: (1) adult females oviposit preferentially on isolated host plants; (2) female larvae on isolated plants survive better than on plants growing in clumps; (3) female larvae survive in greater numbers on plants removed to the laboratory compared to plants left outside; (4) high Spiroplasma infection favours female survival; and (5) high egg/larval density adversely affects adult body size. We conclude that: (1) the butterflies' preference for isolated host plants creates high egg densities and hence enables invasion by Spiroplasma; (2) male killing favours female survival through cannibalism of male eggs and the extra food-plant resources so released; and (3) the butterfly's preference for isolated host plants may provide an enemy-free space that protects eggs and larvae from predators and parasitoids.

A specialist herbivore uses chemical camouflage to overcome the defenses of an ant-plant mutualism.

Many plants and ants engage in mutualisms where plants provide food and shelter to the ants in exchange for protection against herbivores and competitors. Although several species of herbivores thwart ant defenses and extract resources from the plants, the mechanisms that allow these herbivores to avoid attack are poorly understood. The specialist insect herbivore, Piezogaster reclusus (Hemiptera: Coreidae), feeds on Neotropical bull-horn acacias (Vachellia collinsii) despite the presence of Pseudomyrmex spinicola ants that nest in and aggressively defend the trees. We tested three hypotheses for how P. reclusus feeds on V. collinsii while avoiding ant attack: (1) chemical camouflage via cuticular surface compounds, (2) chemical deterrence via metathoracic defense glands, and (3) behavioral traits that reduce ant detection or attack. Our results showed that compounds from both P. reclusus cuticles and metathoracic glands reduce the number of ant attacks, but only cuticular compounds appear to be essential in allowing P. reclusus to feed on bull-horn acacia trees undisturbed. In addition, we found that ant attack rates to P. reclusus increased significantly when individuals were transferred between P. spinicola ant colonies. These results are consistent with the hypothesis that chemical mimicry of colony-specific ant or host plant odors plays a key role in allowing P. reclusus to circumvent ant defenses and gain access to important resources, including food and possibly enemy-free space. This interaction between ants, acacias, and their herbivores provides an excellent example of the ability of herbivores to adapt to ant defenses of plants and suggests that herbivores may play an important role in the evolution and maintenance of mutualisms.

Importance of Secondary Metabolites for Leaf Beetles (Coleoptera: Chrysomelidae)

Leaf beetles (Chrysomelidae) are one of the most diverse families of herbivorous insects. Many of them are important agricultural pests and cause remarkable loss of crop and money as well. Plant leaves and roots are primary food source of both larva and adults of leaf beetles. Plants produce many secondary metabolites in reaction to herbivore insects. It is a well-known phenomenon that quantity and variety of secondary metabolites in plant leaves may change in response to insect attacks. Herbivore insects have to deal with such defensive secondary chemicals and overcome either by detoxifying or storing them. Accordingly, many specialist herbivores coevolved with their host plant. Certain phenolic glycosides may reduce leaf beetle feeding. Condensed tannins are anti-herbivore defenses against leaf chewing beetles, including leaf beetles. Flavonoid compounds are feeding deterrents for many flea leaf beetles. Cinnamic acid derivatives are other known feeding deterrents for leaf beetles. Secondary metabolites quantity and nutritional quality of host plants are not only important for feeding but also for providing enemy-free space and suitable oviposition sites.

Reframing the Governance of Addictions

The ALICE RAP (Addictions and Lifestyles in Contemporary Europe – Reframing Addictions Project; www. alicerap.eu) is a five year E 10 million endeavour, cofinanced by the European Commission, studying the place of addictions in contemporary Europe. Based on ALICE RAP s new research and its synthesis of existing research, in this editorial, I highlight three themes that can drive a reframing of the governance of addictions. The first theme is that an ecological analysis of addictive substances suggests that humans are active and functional in relation to the drugs thatwe take, rather thanbeing passive and vulnerable (Sullivan & Hagen, 2014). For example, in the story of life over the last 400 million years, one of the developments has been the battle between plants, and the animals that eat them. Of many defence mechanisms, plants produce secondarymetabolites, including nicotine, morphine, and cocaine, potent neurotoxins that evolved because they punished and deterred consumption by plant-eating animals. Counterbalancing this, animals have evolved to counter-exploit the products of these hundreds of millions of years of research by plants to inhibit and kill their own parasites by subsisting on a mixed diet of palatable and toxic plants, trading off diet quality (and thus growth) for what is termed enemy-reduced or enemy-free space. This also applies to humans. Amongst Congo basin hunter gatherers, the quantity of cigarettes smoked is titrated against intestinal worm burden – the higher the worm burden, the greater the number of cigarettes smoked. Further, when treated with the anthelmintic drug, abendazole, the number of cigarettes smoked is reduced (Roulette et al., 2014). In another example, the presence of ethanol within ripe fruit suggests low-level but chronic dietary exposure for all fruit-eating animals, with volatilized alcohols from fruit potentially serving in olfactory localization of nutritional resources (Dudley, 2014). The same seems to apply to humans, since, whereas primate ancestors living 16–21 million years ago could not effectively metabolize consumed ethanol, by 6–12 million years ago, human s last common ancestor with gorillas and chimpanzees had evolved a digestion fully capable ofmetabolizing consumed ethanol, at levels found in fermenting fruits (Brenner, 2013). That humans are active and functional in relation to the drugs that we take, including alcohol and nicotine, has at least three implications. First, prohibition and “war(s) on drugs” are likely to fail, because substance use is not “caused” by biological frailty in people in general; second, understanding the ecological contexts and dynamics of drug use may point to new preventive and clinical approaches – the above example of anti-worm treatment reducing cigarette use; third, active and functional speak to potency as being a primary driver of drug use and related harm. This brings us to the second theme, toxicological analysis. For example, margin of Exposure (MoE) analysis compares the ratio of a toxic dose of a drug with the dose consumed (Lachenmeier & Rehm, 2014). A MoE of 1 implies consuming the toxic dose; a MoE of 100 implies consuming 1/100 toxic dose. The European Food Safety Authority (EFSA) sets a MoE of 1,000 for carcinogens whose toxic dose is assessed in humans and whose consumption is voluntary (unlike drinking water). Such aMoE does not imply that consumption is safe, only low risk. The MoE for the consumption of alcohol by European adults is assessed at 1.3 when based on animal studies in which the equivalent does increases death rates by 10 %, and 1.0 when based on human studies with a 1.5 % increased risk of death from liver cirrhosis. This means that European adults consume alcohol at the toxic dose, or 1,000 times the dose were the EFSA guidelines applied to alcohol (EFSA does not assess alcohol). This, together with the fact that the risk of premature death under the age of 70 years for an alcohol-related cause increases linearly with the dose of alcohol consumption (Rehm, Lachenmeier &Room, 2014) implies that the potency of the alcohol we consume is far too high. The strength of alcoholic products could be reduced without consumer preferences being compromised (Lachenmeier, Kanteres & Rehm, 2014). In another example, almost all of the nicotine humans consume (West, Brown&Beard, 2014) is in the form of the SUCHT, 60 (6), 2014, 309 – 311

Morphologically Conservative but Physiologically Diverse: The Mode of Stasis in Anostraca (Crustacea: Branchiopoda).

The essay discusses whether biotic and abiotic environments differ in their ability to speed up or slow down morphological change and the generation of new lineages. Examples from the class Branchiopoda show that morphological conservatism is associated with enemy free space in species-poor habitats dominated by abiotic factors, while Red Queen mechanisms are predominant in larger systems with complex biotic interactions. Splitting of Branchiopod main lineages is associated with increased fish predation during the Devonian. The order Cladocera adapted and remained in larger aquatic systems, and subsequently generated a variety of new families, genera and species. The order Anostraca, on the other hand, maintained its ancestral morphology and survived only as “living fossils” in isolated ponds of harsh habitats. Despite their archaic morphology, however, they possess highly sophisticated adaptations to local physicochemical properties of their extreme environment. Hence, although morphologically conservative and possessing traits typical for “living fossils”, anostracan physiological abilities are closely adapted to the challenging and variable physicochemical conditions of ponds and ephemeral pools.

Bottom-up effects on top-down regulation of a floating aquatic plant by two weevil species: the context-specific nature of biological control

Summary Plant nutrition (bottom-up effects) impacts a plant's ability to withstand herbivory (top-down effects) and influences phytophagous insect fecundity. These factors confound efficacy predictions for biological control purposes. We investigated the importance of these forces with regard to invasibility of Eichhornia crassipes. We also examined whether one could have predicted whether the weevil species Neochetina eichhorniae or Neochetina bruchi would have been the better biocontrol agent. Three experiments compared E. crassipes performance when subjected to herbivory by these weevils across a range of fertilizer levels. A low initial plant density experiment examined growth and flowering while allowing density to increase. A high plant density experiment evaluated reduction in biomass and surface coverage. A third experiment evaluated plant growth unconstrained by space. Herbivory effects varied between treatments; interactions varied between experiments. Herbivory reduced plant density and biomass, except in low fertilizer conditions, and consistently reduced flowering. N. bruchi alone or both weevil species together reduced growth more than N. eichhorniae alone, elucidating N. bruchi as the better agent. However, N. eichhorniae better reduced biomass and plant density under initial conditions of complete plant coverage, suggesting it as the superior choice. Synthesis and applications. Bottom-up and top-down forces acting in concert affect invasibility of plant species. Plasticity to resource availability enables invaders to persist in conditions that are unfavourable to herbivores (enemy-free space). Consequently, biological control efficacy is nuanced and context specific, so predictability requires assessment of multiple parameters across a range of conditions. Overly simplistic evaluations risk rejection of effective agents capable of mediating non-native plant invasions. These results also argue that biological control practitioners should disregard the concept that a single best agent can be identified to control an invasive plant that exploits a broad range of habitats and environmental conditions. Aquaphyte invasions often coincide with watershed nutrification so unless weed control is carried out concurrently with measures that reduce nutrient inputs, removal of infestations will merely reduce competition thereby accelerating regrowth or facilitating replacement by other undesirable species (the ‘invasive treadmill’). The suppressive effects of biological control are valuable and complimentary, even when replacement by other, presumably less problematic, species may occur. These subtler effects should be considered with protocols developed for integrated control strategies.

An orb‐weaver spider exploits an ant–acacia mutualism for enemy‐free space

Exploiters of protection mutualisms are assumed to represent an important threat for the stability of those mutualisms, but empirical evidence for the commonness or relevance of exploiters is limited. Here, I describe results from a manipulative study showing that an orb-weaver spider, Eustala oblonga, inhabits an ant-acacia for protection from predators. This spider is unique in the orb-weaver family in that it associates closely with both a specific host plant and ants. I tested the protective effect of acacia ants on E. oblonga by comparing spider abundance over time on acacias with ants and on acacias from which entire ant colonies were experimentally removed. Both juvenile and adult spider abundance significantly decreased over time on acacias without ants. Concomitantly, the combined abundance of potential spider predators increased over time on acacias without ants. These results suggest that ant protection of the ant-acacia Acacia melanocerus also protects the spiders, thus supporting the hypothesis that E. oblonga exploits the ant–acacia mutualism for enemy-free space. Although E. oblonga takes advantage of the protection services of ants, it likely exacts little to no cost and should not threaten the stability of the ant–acacia mutualism. Indeed, the potential threat of exploiter species to protection mutualisms in general may be limited to species that exploit the material rewards traded in such mutualisms rather than the protection services.

Distance and sex determine host plant choice by herbivorous beetles.

BackgroundPlants respond to herbivore damage with the release of volatile organic compounds (VOCs). This indirect defense can cause ecological costs when herbivores themselves use VOCs as cues to localize suitable host plants. Can VOCs reliably indicate food plant quality to herbivores?MethodologyWe determined the choice behavior of herbivorous beetles (Chrysomelidae: Gynandrobrotica guerreroensis and Cerotoma ruficornis) when facing lima bean plants (Fabaceae: Phaseolus lunatus) with different cyanogenic potential, which is an important constitutive direct defense. Expression of inducible indirect defenses was experimentally manipulated by jasmonic acid treatment at different concentrations. The long-distance responses of male and female beetles to the resulting induced plant volatiles were investigated in olfactometer and free-flight experiments and compared to the short-distance decisions of the same beetles in feeding trials.ConclusionFemale beetles of both species were repelled by VOCs released from all induced plants independent of the level of induction. In contrast, male beetles were repelled by strongly induced plants, showed no significant differences in choice behavior towards moderately induced plants, but responded positively to VOCs released from little induced plants. Thus, beetle sex and plant VOCs had a significant effect on host searching behavior. By contrast, feeding behavior of both sexes was strongly determined by the cyanogenic potential of leaves, although females again responded more sensitively than males. Apparently, VOCs mainly provide information to these beetles that are not directly related to food quality. Being induced by herbivory and involved in indirect plant defense, such VOCs might indicate the presence of competitors and predators to herbivores. We conclude that plant quality as a food source and finding a potentially enemy-free space is more important for female than for male insect herbivores, whereas the presence of a slightly damaged plant can help males to localize putative mating partners.

Herbivory-associated degradation of tomato trichomes and its impact on biological control of Aculops lycopersici

Tomato plants have their leaves, petioles and stems covered with glandular trichomes that protect the plant against two-spotted spider mites and many other herbivorous arthropods, but also hinder searching by phytoseiid mites and other natural enemies of these herbivores. This trichome cover creates competitor-free and enemy-free space for the tomato russet mite (TRM) Aculops lycopersici (Acari: Eriophyidae), being so minute that it can seek refuge and feed inbetween the glandular trichomes on tomato cultivars currently used in practice. Indeed, several species of predatory mites tested for biological control of TRM have been reported to feed and reproduce when offered TRM as prey in laboratory experiments, yet in practice these predator species appeared to be unable to prevent TRM outbreaks. Using the phytoseiid mite, Amblydromalus limonicus, we found exactly the same, but also obtained evidence for successful establishment of a population of this predatory mite on whole plants that had been previously infested with TRM. This successful establishment may be explained by our observation that the defensive barrier of glandular plant trichomes is literally dropped some time after TRM infestation of the tomato plants: the glandular trichome heads first rapidly develop a brownish discoloration after which they dry out and fall over onto the plant surface. Wherever TRM triggered this response, predatory mites were able to successfully establish a population. Nevertheless, biological control was still unsuccessful because trichome deterioration in TRM-infested areas takes a couple of days to take effect and because it is not a systemic response in the plant, thereby enabling TRM to seek temporary refuge from predation in pest-free trichome-dense areas which continue to be formed while the plant grows. We formulate a hypothesis unifying these observations into one framework with an explicit set of assumptions and predictions to be tested in future experiments.Electronic supplementary materialThe online version of this article (doi:10.1007/s10493-012-9638-6) contains supplementary material, which is available to authorized users.

ECOLOGICAL VERSUS PHYLOGENETIC DETERMINANTS OF TROPHIC ASSOCIATIONS IN A PLANT-LEAFMINER-PARASITOID FOOD WEB

Specialized trophic interactions in plant-herbivore-parasitoid food webs can spur "bottom-up" diversification if speciation in plants leads to host-shift driven divergence in insect herbivores, and if the effect then cascades up to the third trophic level. Conversely, parasitoids that search for victims on certain plant taxa may trigger "top-down" diversification by pushing herbivores into "enemy-free space" on novel hosts. We used phylogenetic regression methods to compare the relative importance of ecology versus phylogeny on associations between Heterarthrinae leafmining sawflies and their parasitoids. We found that: (1) the origin of leafmining led to escape from most parasitoids attacking external-feeding sawflies; (2) the current enemies mainly consist of generalists that are shared with other leafmining taxa, and of more specialized lineages that may have diversified by shifting among heterarthrines; and (3) parasitoid-leafminer associations are influenced more by the phylogeny of the miners' host plants than by relationships among miner species. Our results suggest that vertical diversifying forces have a significant-but not ubiquitous-role in speciation: many of the parasitoids have remained polyphagous despite niche diversification in the miners, and heterarthrine host shifts also seem to be strongly affected by host availability.

Boomeranging in structural defense

Plant defensive behaviors that resist arthropod herbivory include trichome-mediated defenses, and variation in plant trichome morphology and abundance provides examples of the mechanistic complexities of insect-plant interactions. Trichomes were removed from Cycas revoluta cataphylls on the island of Guam to reveal Aulacaspis yasumatsui scale infestation, and predation of the newly exposed insects by pre-existing Rhyzobius lophanthae beetles commenced within one day. The quotient of predated/total scale insects was 0.5 by day 4 and stabilized at that found on adjacent glabrous leaves in about one week. The trichome phenotype covering the C. revoluta cataphyll complex offers the invasive A. yasumatsui armored scale effectual enemy-free space in this system. This pest and predator share no known evolutionary history with C. revoluta, therefore, the adaptive significance of this plant behavior in natural habitat is not yet known.

Caterpillar feeding impairs an indirect defence: costs or strategy?

The secretion of extrafloral nectar (EFN) represents a widely distributed and efficient inducible anti-herbivore defence. Providing sweet rewards on their vegetative parts enables plants to attract ants and other predators as well as parasitoids, which generally benefits the host plant. As plants are smart, they can also eavesdrop on signals of danger that are emitted by their neighbours. For example, lima bean (Phaseolus lunatus) plants respond with higher EFN secretion rates to the exposure to volatile organic compounds (VOCs) from infested neighbours prior to herbivore attack (Heil & Silva Bueno 2007; Blande, Holopainen & Li 2010), a response that benefits plants in terms of decreased rates of herbivory under natural conditions (Heil & Silva Bueno 2007). In short, EFN secretion is a common inducible defensive response whose responsiveness to herbivore-induced VOCs ensures that plants can prepare themselves successfully for future attack. In this issue, however, Li et al. (2012) question the general applicability of these statements. The authors studied the herbivore-induced VOCs release and EFN secretion by hybrid aspen (Populus tremula 9 tremuloides) after exposure to the headspace of damaged conspecific neighbours. The authors found a direct induction of EFN secretion: hybrid aspen ‘smells’ when a neighbouring plant is damaged and then starts to attract ants as a preparation for future threats. By contrast, the emission of VOCs was not directly induced by an exposure to VOCs, although the exposed plants were primed to release higher amounts of monoterpenes, homoterpenes and sesquiterpenes when consecutively being infested by caterpillars. All these observations make ecological sense, because VOCs represent only information, whereas EFN is a resource (Kessler & Heil 2011). That is, a plant that emits herbivore-induced VOCs without being infested would ‘lie’ and ‘cheat’ its defenders. By contrast, EFN represents a resource per se that can enhance the survival of multiple predators such as lacewings (Limburg & Rosenheim 2001), predatory mites (Van Rijn & Tanigoshi 1999; Gnanvossou et al. 2005), parasitic wasps (Rose, Lewis & Tumlinson 2006) and ants (Lach, Hobbs & Majer 2009; Wilder & Eubanks 2010). Therefore, a direct induction upon to herbivore-induced VOCs makes ecological sense for EFN, but not so for VOCs. However, in contrast to what represents a convenient and generally accepted state of the art in the research on tritrophic interactions and plant–plant signalling, Li et al. (2012) also report that VOCs did not prime EFN secretion for stronger increase upon direct herbivore damage. By contrast, feeding by caterpillars of autumn moth (Epirrita autumnata) impaired, rather than induced, the secretion of EFN on mature leaves. This result was confirmed for three different poplar clones: intact leaves of infested plants secreted less EFN than intact leaves of un-infested plants, and directly damaged leaves exhibited even lower secretion rates. Why does poplar reduce EFN secretion in response to caterpillar feeding? Because we are commonly not as open as we should be to unexpected ideas, the authors present various explanations for their seemingly inconvenient observation. First, feeding caterpillars might directly damage the extrafloral nectaries. Second, the feeding might damage the photosynthetic tissue to a degree that limits the de novo synthesis of sugars for EFN production. Third, caterpillar feeding might induce defensive responses that compete with EFN for limited resources and fourth, the caterpillars might posses a mechanism to actively suppress EFN secretion. Although these arguments are non-exclusive, options two and four are those that will make this article the basis for many future studies. The authors discuss that the caterpillar, as a generalist, is unlikely to possess a mechanism for active manipulation of host defence. Is this necessarily true? In fact, generalist herbivores would gain particularly significant selective benefits from suppressing general plant resistance responses. Whereas specialist herbivores can evolve strategies against the specific resistance traits of their host, generalists are unlikely to evolve specific enzymes that allow for the successful detoxification of the entire arsenal of secondary compounds that they face in their multiple host species. In fact, generalists can possess multiple or highly promiscuous detoxification enzymes (Li, Schuler & Berenbaum 2003; Li et al. 2004; Pauchet et al. 2008), but the synthesis of multiple enzymes comes at high metabolic costs, whereas promiscuous enzymes are usually less efficient than specialized ones in accelerating any of the catalysed reactions. By contrast, suppressing general plant signalling pathways can render plants much more susceptible. For example, many Pseudomonas strains inject *Correspondence author. E-mail: mheil@ira.cinvestav.mx

Spatial distribution patterns of three fig wasps on Ficus semicordata: How non-pollinators affect pollinator’s sex ratio

Sex ratio theory is one of the most productive fields in research on evolutionary biology. Pollinating fig wasps, due to their particular natural life history, are considered to be a valuable model for the study of sex ratio evolution. A great deal of research concerning the factors that affect pollinator fig wasp (Agaonidae) progeny sex ratio has been done, and at present three main factors (haplodiploidy, local mate competition and inbreeding) are found to be important at the population level. However, there still exists variation between empirical data and model predictions. Another factor to which little thought has been given before is the effect of non-pollinating fig wasps (NPFWs) which parasitize in the larvae gall of pollinator thus kill pollinators and exploit the fig/fig pollinator mutualistic systems. In this study, we focus on why and how non-pollinating fig wasps distort pollinator fig wasp’s original sex ratio. Through controlling the number of ovipositing foundresses inside a fig, combined with the observation of ovipositing behavior and sequence, we studied three species of wasp in the figs of a dioecious fig Ficus semicordata including the pollinator Ceratosolen gravely and NPFWs Platyneura cunia, Sycoscapter trifemmensis in tropical area of Xishuangbanna from September to December 2009. First, we observed the timing of oviposition of all fig wasps utilizing F. semicordata and found differences when compared to previous studies. Such as P. cunia is the fourth rather then the secondary fig wasps to oviposit on the syconia approximately 10days after the pollinator. S. trifemmensis oviposits much earlier than previously thought, 14–32days after the pollinators. We examined the spatial location of male and female progeny of the pollinator. We found foundresses of pollinator prefer to use innermost ovules first. Only at high offspring numbers were the outer ovules used. More male pollinator offspring were developed near the fig cavity, while female pollinator offspring were more evenly distributed among ovule layers. As pollinator offspring numbers increased, this phenomenon became more pronounced. This pattern of segregation of male larvae gall in inner ovules and female larvae gall in outer ovules suggests that female offspring might be more vulnerable to attack by parasitic wasps that oviposit from outside the syconium. Experiments later demonstrated that NPFWs are restricted by their ovipositor length and they prefer to or can only lay their eggs into ovules near the fig wall. Then we examined the spatial location of NPFWs and compared this with the spatial location of male/female progeny of pollinator. NPFWs had a high probability of parasitizing female pollinator larvae. Thus, NPFWs have a substantial effect on the sex ratio of the pollinator, as parasitism risk decreases towards the center of the syconium, where inner ovules provide enemy-free space for most of male pollinator offspring. Partial correlation analyse shows that sex ratio of pollinator progeny has a positive relationship with the number of NPFWs. We suggest that the resulting gradient in offspring viability between male and female contributes to selection on pollinators’ for a less female-biased sex ratio. When the affect of NPFWs was excluded, the pollinator sex ratio was not in good agreement with local mate competition theory, although it was still female-biased. In addition, the average number of offspring per foundress decreased with increasing foundress number, but pollinator sex ratio was positively related to brood size. Thus, pollinator females do not appear to adjust their sex ratio to foundress density directly, but use brood size and foundress density simultaneously as cues to assess potential LMC.

Spatial Stratification of Internally and Externally Non-Pollinating Fig Wasps and Their Effects on Pollinator and Seed Abundance in Ficus burkei

Fig trees (Ficus spp.) are pollinated by tiny wasps that enter their enclosed inflorescences (syconia). The wasp larvae also consume some fig ovules, which negatively affects seed production. Within syconia, pollinator larvae mature mostly in the inner ovules whereas seeds develop mostly in outer ovules—a stratification pattern that enables mutualism persistence. Pollinators may prefer inner ovules because they provide enemy-free space from externally ovipositing parasitic wasps. In some Australasian Ficus, this results in spatial segregation of pollinator and parasite offspring within syconia, with parasites occurring in shorter ovules than pollinators. Australian figs lack non-pollinating fig wasps (NPFW) that enter syconia to oviposit, but these occur in Africa and Asia, and may affect mutualist reproduction via parasitism or seed predation. We studied the African fig, F. burkei, and found a similar general spatial pattern of pollinators and NPFWs within syconia as in Australasian figs. However, larvae of the NPFW Philocaenus barbarus, which enters syconia, occurred in inner ovules. Philocaenus barbarus reduced pollinator abundance but not seed production, because its larvae replaced pollinators in their favoured inner ovules. Our data support a widespread role for NPFWs in contributing to factors preventing host overexploitation in fig-pollinator mutualisms.

Herbivory limits the yellow water lily in an overgrown lake and in flowing water

Aquatic macrophytes with floating leaves are often key ecological species that affect entire aquatic ecosystems. Here we describe an investigation of the importance of insect herbivory for population growth and leaf senescence in the yellow water lily (Nuphar lutea). In order to gain a general picture of the importance of herbivory under different conditions, we experimentally manipulated herbivory in a large lily population in natural still water and observed the natural development of 32 smaller populations in flowing water. Herbivory drastically increased leaf senescence, reducing leaf density. In the still water, over one summer, leaf density increased by a factor of 1.23 in the presence of water lily leaf beetles and 1.61 when herbivory was eliminated. In flowing water, population growth was restricted mainly by leaf crowdedness, which limited large dense populations. Herbivory by water lily leaf beetles also had a limiting effect on yellow water lily, again mainly in large dense populations. Small populations supported a lower density of beetles. Previous studies have not addressed population-level responses of vascular plants with floating leaves. Our results suggest that herbivory can result in greater light penetration into the water and reduce “enemy-free space” for aquatic species that find such space in water lily stands. We suggest that the water lily leaf beetle should be considered an “ecological engineer.”