Tritrophic interactions between a fungal pathogen,a spider predator,and the blacklegged tick

The blacklegged tick Ixodes scapularis is the primary vector for the bacterium causing Lyme disease in eastern North America and for other medically important pathogens. This species is vulnerable to attack by fungal pathogens and arthropod predators, but the impacts of interactions between biocontrol agents have not been examined. The biocontrol agent Met52^®, containing the entomopathogenic fungus Metarhizium brunneum (=M. anisopliae), controls blacklegged ticks with efficacy comparable to chemical acaricides. The brush‐legged wolf spider Schizocosa ocreata is a predator of I. scapularis that reduces their survival under field conditions. We conducted a field microcosm experiment to assess the compatibility of Met52 and S. ocreata as tick biocontrol agents. We compared the fits of alternative models in predicting survival of unfed (flat) and blood‐fed (engorged) nymphs. We found the strongest support for a model that included negative effects of Met52 and S. ocreata on flat nymph survival. We found evidence for interference between biocontrol agents, with Met52 reducing spider survival, but we did not find a significant interaction effect between the two agents on nymph survival. For engorged nymphs, low recovery rates resulted in low statistical power to detect possible effects of biocontrol agents. We found that nymph questing activity was lower when the spider was active above the leaf litter than when the spider was unobserved. This provides the first evidence that predation cues might affect behavior important for tick fitness and pathogen transmission. This study presents field microcosm evidence that the biopesticide Met52 and spider Schizocosa ocreata each reduced survival of blacklegged ticks Ixodes scapularis. Met52 reduced spider survival. Potential interference between Met52 and the spider should be examined at larger scales, where overlap patterns may differ. Ticks were more likely to quest when the spider was inactive, suggesting the ticks changed their behavior to reduce danger.     

Lethal and sublethal effects of Embelia ribes and two commercial pesticides on a generalist predator

Even as new substances show promise as biopesticides for controlling pests due to their natural properties and high effectiveness in inhibiting pests, their side effects on non‐target organisms must nevertheless be evaluated before they can be included into integrated pest management systems. In this study, a crude extract from dried leaves of Embelia ribes was evaluated together with two commercial pesticides: azadirachtin (a natural product) and amitraz (a synthetic acaricide). We examined both lethal and sublethal effects on the predatory potential of the lynx spider Oxyopes lineatipes, which is among the most dominant predator in tropical agricultural agroecosystems. We found that the spider's mortality increased with rising concentration of both commercial products, azadirachtin and amitraz, but not with rising concentration of the extracts from E. ribes. The greatest mortality occurred when amitraz was used. That material caused almost 100% spider mortality in the doses recommended for field spraying. Azadirachtin significantly reduced the rate at which O. lineatipes captured prey, while there was no significant difference in capture rates among spiders exposed to a control treatment and the E. ribes treatment. Considering its absence of unfavourable impacts on O. lineatipes in terms of mortality and predatory activity, the plant extract from E. ribes shows promise as a new biopesticide material. In contrast, azadirachtin, which has been considered as safe for non‐target organisms, exhibited slight lethal effect only in higher concentrations and strong sublethal effect by reducing spiders’ predation rate.     

Selection of aphid prey by a generalist predator: do prey chemical defences matter?

1. For predators, prey selection should maximise nutrition and minimise fitness costs. In the present study, it was investigated whether a generalist predator [Chrysoperla carnea (Stephens) lacewing larvae] rejected harmful, chemically‐defended prey [Brevicoryne brassicae (Linnaeus) aphids] when non‐defended prey [Myzus persicae (Sulzer) aphids] were available. 2. It was tested: (i) whether consuming different prey species affects predator mortality; (ii) whether naïve predators reject chemically‐defended prey while foraging when non‐defended prey are available; (iii) whether the relative abundance of each prey affects the predator's prey choice; and (iv) whether predators learn to avoid consuming chemically‐defended prey after exposure to both prey species. 3. Consumption of B. brassicae yielded greater C. carnea mortality than M. persicae consumption, but naïve C. carnea did not reject B. brassicae in favour of M. persicae during foraging. When presented at unequal abundances, naïve predators generally consumed each aphid species according to their initial relative abundance, although, predation of non‐defended prey was less than expected when defended prey were initially more abundant, indicating a high consumption of B. brassicae impeded M. persicae consumption. With experience, C. carnea maintained predation of both aphid species but consumed more M. persicae than B. brassicae, indicating a change in behaviour. 4. Although prey choice by C. carnea may change with experience of available prey, prey chemical defences do not appear to influence prey choice by naïve predators. This inability to avoid harmful prey could facilitate wider, indirect interactions. Myzus persicae may benefit where high consumption of B. brassicae hinders predators in the short term, and in the long term, increases predator mortality.     

Indirect competitive effects of stemborers on a gall community

Interspecific competition between phytophagous insects using the same host plant occurs frequently and can strongly affect population densities of competing species. Competition between gallmakers and stemborers could be especially intense because both types of herbivore are unable to avoid competition by relocation during their immature stages. For apical meristem gallmakers the main result of competition is likely to be the interruption of resources to the gall by the stemborers' devouring of stem contents. The proximate effect of such competition could be to reduce gall size, thereby increasing the number of chambers per gall unit volume, and reducing the size and potential reproductive output of the gallformer. In addition, smaller galls may be more susceptible to attack from size‐limited parasitoids, resulting in a second indirect effect of competition. Using a community of galling and stemboring insects on the saltmarsh shrub Iva frutescens L. (Asteraceae), we measured for indirect effects of competition. We examined the primary indirect effect of competition on gall midge crowding and the secondary effects on parasitism rates and parasitoid guild composition. Results indicated that galls co‐occurring with stemborers were smaller, crowding of gall inhabitants was 22% greater, and the composition of the parasitoid guild was altered relative to galls on unbored stems. The overall parasitism rate was not different between galls on bored vs. unbored stems. These results show that competition resulting from the presence of stemborers has the potential to affect the gall midge Asphondylia borrichiae Rossi & Strong (Diptera: Cecidomyiidae) and secondarily to affect its guild of hymenopteran parasitoids.     

Caterpillar‐induced plant volatiles attract conspecific herbivores and a generalist predator

Plants release volatiles in response to caterpillar feeding that attracts natural enemies of the herbivores, a tritrophic interaction which has been considered to be an indirect plant defence against herbivores. On the other hand, the caterpillar‐induced plant volatiles have been reported to either repel or attract conspecific adult herbivores. This work was undertaken to investigate the response of both herbivores and natural enemies to caterpillar‐induced plant volatiles in apple orchards. We sampled volatile compounds emitted from uninfested apple trees, and apple trees infested with generalist herbivore the pandemis leafroller moth, Pandemis pyrusana (Lepidoptera, Tortricidae) larvae using headspace collection and analysed by gas chromatography/mass spectrometry. Infested apple trees uniquely release six compounds (benzyl alcohol, phenylacetonitrile, phenylacetaldehyde, 2‐phenylethanol, indole and (E)‐nerolidol). These compounds were tested on two species of herbivores and one predator in apple orchards. Binary blends of phenylacetonitrile + acetic acid or 2‐phenylethanol + acetic acid attracted a large number of conspecific male and female adult herbivores. The response of pandemis leafroller to herbivore‐induced plant volatiles (HIPVs) was so pronounced that over one thousand and seven hundred conspecific male and female adult herbivores were caught in traps baited with HIPVs in three‐day trapping period. In addition, significantly higher number of male and female obliquebanded leafroller, Choristoneura rosaceana (Lepidoptera, Tortricidae), was caught in traps baited a binary blend of 2‐phenylethanol + acetic acid, or a ternary blend contains 2‐phenylethanol and phenylacetonitrile + acetic acid. This result challenges the current paradigm hypothesized that HIPVs repel herbivores and question the indirect defensive function proposed for these compounds. On the other hand, a ternary blend of phenylacetonitrile and 2‐phenylethanol + acetic acid attracted the largest numbers of the general predator, the common green lacewing, Chrysoperla plorabunda. To our knowledge, this is the first record of the direct attraction of conspecific adult herbivores as well as a predator to the caterpillar‐induced plant volatiles in the field.     

Sex and occupation time influence niche space of a recovering keystone predator

Predators exert strong effects on ecological communities, particularly when they re‐occupy areas after decades of extirpation. Within species, such effects can vary over time and by sex and cascade across trophic levels. We used a space‐for‐time substitution to make foraging observations of sea otters (Enhydra lutris) across a gradient of reoccupation time (1–30 years), and nonmetric multidimensional scaling (nMDS) analysis to ask whether (a) sea otter niche space varies as a function of occupation time and (b) whether niche space varies by sex. We found that niche space varied among areas of different occupation times. Dietary niches at short occupation times were dominated by urchins (Mesocentrotus and Strongylocentrotus spp; >60% of diets) in open habitats at 10–40 m depths. At longer occupation times, niches were dominated by small clams (Veneroida; >30% diet), mussels (Mytilus spp; >20% diet), and crab (Decapoda; >10% diet) in shallow (<10 m) kelp habitats. Diet diversity was lowest (H′ = 1.46) but energy rich (~37 kcal/min) at the earliest occupied area and highest, but energy poor (H′ = 2.63, ~9 kcal/min) at the longest occupied area. A similar transition occurred through time at a recently occupied area. We found that niche space also differed between sexes, with bachelor males consuming large clams (>60%), and urchins (~25%) from deep waters (>40 m), and females and territorial males consuming smaller, varied prey from shallow waters (<10 m). Bachelor male diets were less diverse (H′ = 2.21) but more energy rich (~27 kcal/min) than territorial males (H′ = 2.54, ~13 kcal/min) and females (H′ = 2.74, ~11 kcal/min). Given recovering predators require adequate food and space, and the ecological interactions they elicit, we emphasize the importance of investigating niche space over the duration of recovery and considering sex‐based differences in these interactions.     

Reciprocal intraguild predation and predator coexistence

Intraguild predation is a mix of competition and predation and occurs when one species feeds on another species that uses similar resources. Theory predicts that intraguild predation hampers coexistence of species involved, but it is common in nature. It has been suggested that increasing habitat complexity and the presence of alternative food may promote coexistence. Reciprocal intraguild predation limits possibilities for coexistence even further. Habitat complexity and the presence of alternative food are believed to promote coexistence. We investigated this using two species of predatory mites, Iphiseiodes zuluagai and Euseius concordis, by assessing co‐occurrence in the field and on arenas differing in spatial structure in the laboratory. The predators co‐occured on the same plants in the field. In the laboratory, adults of the two mites fed on juveniles of the other species, both in the presence and the absence of a shared food source, showing that the two species are involved in reciprocal intraguild predation. Adults of I. zuluagai also attacked adults of E. concordis. This suggests limited possibilities for coexistence of the two species. Indeed, E. concordis invariably went extinct extremely rapidly on arenas without spatial structure with populations consisting of all stages of the two predators and with a shared resource. Coexistence was prolonged on host plant leaves with extra food sources, but E. concordis still went extinct. On small, intact plants, coexistence of the two species was much longer, and ended with the other species, I. zuluagai, often going extinct. These results suggest that spatial structure and the presence of alternative food increase the coexistence period of intraguild predators.     

Transgenerational plasticity of inducible defences: Combined effects of grand‐parental,parental and current environments

Phenotypic plasticity can occur across generations (transgenerational plasticity) when environments experienced by the previous generations influenced offspring phenotype. The evolutionary importance of transgenerational plasticity, especially regarding within‐generational plasticity, is a currently hot topic in the plasticity framework. How long an environmental effect can persist across generations and whether multigenerational effects are cumulative are primordial—for the evolutionary significance of transgenerational plasticity—but still unresolved questions. In this study, we investigated how the grand‐parental, parental and offspring exposures to predation cues shape the predator‐induced defences of offspring in the Physa acuta snail. We expected that the offspring phenotypes result from a three‐way interaction among grand‐parental, parental and offspring environments. We exposed three generations of snails without and with predator cues according to a full factorial design and measured offspring inducible defences. We found that both grand‐parental and parental exposures to predator cues impacted offspring antipredator defences, but their effects were not cumulative and depended on the defences considered. We also highlighted that the grand‐parental environment did alter reaction norms of offspring shell thickness, demonstrating an interaction between the grand‐parental transgenerational plasticity and the within‐generational plasticity. We concluded that the effects of multigenerational exposure to predator cues resulted on complex offspring phenotypic patterns which are difficult to relate to adaptive antipredator advantages.     

Both local presence and regional distribution of predator cues modulate prey colonisation in pond landscapes

Recent work on habitat selection has shown that the perceived quality of habitat patches may depend on the quality of adjacent patches. However, it is still unclear how local habitat selection cues can alter distribution patterns in metacommunities at a larger (regional) scale. We studied mosquito oviposition in pond landscapes that differed in the proportion of bad patches with fish predation risk. Our experiment provided conclusive evidence for two local and two regional types of habitat selection. Good patches near bad patches were avoided (local risk contagion) while more distant good patches experienced increased oviposition (regional compression). Oviposition in bad patches increased when located next to good patches (reward contagion) or when there were no good patches regionally present (regional compromise). This complex colonisation behaviour involving compromises at different spatial scales forces experimenters to reconsider the independence of spatial replicates and challenges available theories to predict species distribution patterns.     

Mobbing behaviour in a passerine community increases with prevalence in predator diet

Mobbing behaviour against predators is well documented but less is known about the factors influencing variation in behavioural response between prey species. We conducted a series of playback experiments to examine how the mobbing responses of prey species differed according to their relative risk of predation by the Eurasian Pygmy Owl Glaucidium passerinum, a predator of passerines. We found that mobbing among 22 passerine prey species was positively correlated with their prevalence in the Pygmy Owl diet. To compare mobbing behaviour between two seasons, we conducted playback experiments during spring (breeding season) and autumn (non‐breeding season). Contrary to previous studies, we found that mobbing intensity was greater during autumn than in spring. Our study shows a differential mobbing response of 22 species to the calls from one predator species and underscores the importance of considering seasonal variation in mobbing behaviour. Mobbing response differences observed among bird species strongly suggest different cooperation behaviour at the community level.     

Size selection by a gape‐limited predator of a marine snail: Insights into magic traits for speciation

The intertidal snail Littorina saxatilis has repeatedly evolved two parallel ecotypes assumed to be wave adapted and predatory shore crab adapted, but the magnitude and targets of predator‐driven selection are unknown. In Spain, a small, wave ecotype with a large aperture from the lower shore and a large, thick‐shelled crab ecotype from the upper shore meet in the mid‐shore and show partial size‐assortative mating. We performed complementary field tethering and laboratory predation experiments; the first set compared the survival of two different size‐classes of the crab ecotype while the second compared the same size‐class of the two ecotypes. In the first set, the large size‐class of the crab ecotype survived significantly better than the small size‐class both on the upper shore and in the laboratory. In the second set, the small size‐class of the crab ecotype survived substantially better than that of the wave ecotype both on the upper shore and in the laboratory. Shell‐breaking predation on tethered snails was almost absent within the lower shore. In the laboratory shore crabs (Pachygrapsus marmoratus) with larger claw heights selected most strongly against the small size‐class of the crab ecotype, whereas those with medium claw heights selected most strongly against the thin‐shelled wave ecotype. Sexual maturity occurred at a much larger size in the crab ecotype than in the wave ecotype. Our results showed that selection on the upper shore for rapid attainment of a size refuge from this gape‐limited predator favors large size, thick shells, and late maturity. Model parameterization showed that size‐selective predation restricted to the upper shore resulted in the evolution of the crab ecotype despite gene flow from the wave ecotype snails living on the lower shore. These results on gape‐limited predation and previous ones showing size‐assortative mating between ecotypes suggest that size may represent a magic trait for the thick‐shelled ecotype.     

Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission

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Interactions between a pollinating seed predator and its host plant: the role of environmental context within a population

Plant–insect interactions often are important for plant reproduction, but the outcome of these interactions may vary with environmental context. Pollinating seed predators have positive and negative effects on host plant reproduction, and the interaction outcome is predicted to vary with density or abundance of the partners. We studied the interaction between Silene stellata, an herbaceous perennial, and Hadena ectypa, its specialized pollinating seed predator. Silene stellata is only facultatively dependent upon H. ectypa for pollination because other nocturnal moth co‐pollinators are equally effective at pollen transfer. We hypothesized that for plants without conspecific neighbors, H. ectypa would have higher visitation rates compared to co‐pollinators, and the plants would experience lower levels of H. ectypa pollen deposition. We predicted similar oviposition throughout the study site but greater H. ectypa predation in the area without conspecific neighbors compared to plants embedded in a naturally high density area. We found that H. ectypa had consistently higher visitation than moth co‐pollinators in all host plant contexts. However, H. ectypa pollinator importance declined in areas with low conspecific density because of reduced pollen deposition, resulting in lower seed set. Conversely, oviposition was similar across the study site independent of host plant density. Greater likelihood of very high fruit predation combined with lower pollination by H. ectypa resulted in reduced S. stellata female reproductive success in areas with low conspecific density. Our results demonstrate local context dependency of the outcomes of pollinating seed predator interactions with conspecific host plant density within a population.     

Consumptive and non‐consumptive effects of wolf spiders on cotton bollworms

Larvae of the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) that survive on genetically modified Bt cotton (Gossypium hirsutum L., Malvaceae) contribute to the risk of widespread resistance to Bt toxins. Current resistance management techniques include pupae busting, which involves deep tilling of the soil to kill overwintering pupae. Unfortunately, pupae busting runs counter to soil and water conserving techniques, such as minimum tillage. This problem could be relieved with biological control methods, whereby predators attack either larvae going to ground to pupate or moths emerging from the ground. We found that the wolf spider Tasmanicosa leuckartii (Thorell) (Araneae: Lycosidae), a common inhabitant of Australian cotton agroecosystems, is an effective predator of H. armigera, attacking and killing most larvae (66%) and emerging moths (77%) in simple laboratory arenas. Tasmanicosa leuckartii also reduced the number of emerging moths by 66% on average in more structurally complex glasshouse arenas. Males, females, and late‐instar juveniles of T. leuckartii were similarly effective. Tasmanicosa leuckartii also imposed non‐consumptive effects on H. armigera, as when a spider was present larvae in the laboratory areas spent less time on the cotton boll and more time on the soil and more mass was lost from the cotton boll. Increased loss of boll mass likely reflects changes in H. armigera foraging behavior induced by the presence of spiders (indirect non‐consumptive effects). Helicoverpa armigera spent more time as pupae when the spider was present in simple laboratory arenas, but not in more complex glasshouse enclosures. Overall, results indicate that T. leuckartii spiders can be effective predators of H. armigera late instars and moths but also suggest that, under some conditions, the presence of spiders could increase the damage to individual cotton bolls.     

Masting behaviour in a Mediterranean pine tree alters seed predator selection on reproductive output

• Context‐dependency in species interactions is widespread and can produce concomitant patterns of context‐dependent selection. Masting (synchronous production of large seed crops at irregular intervals by a plant population) has been shown to reduce seed predation through satiation (reduction in rates of seed predation with increasing seed cone output) and thus represents an important source of context‐dependency in plant‐animal interactions. However, the evolutionary consequences of such dynamics are not well understood.
• Here we describe masting behaviour in a Mediterranean model pine species (Pinus pinaster) and present a test of the effects of masting on selection by seed predators on reproductive output. We predicted that masting, by enhancing seed predator satiation, could in turn strengthen positive selection by seed predators for larger cone output. For this we collected six‐year data (spanning one mast year and five non‐mast years) on seed cone production and seed cone predation rates in a forest genetic trial composed by 116 P. pinaster genotypes.
• Following our prediction, we found stronger seed predator satiation during the masting year, which in turn led to stronger seed predator selection for increased cone production relative to non‐masting years.
• These findings provide evidence that masting can alter the evolutionary outcome of plant‐seed predator interactions. More broadly, our findings highlight that changes in consumer responses to resource abundance represent a widespread mechanism for predicting and understanding context dependency in plant‐consumer evolutionary dynamics.

     

Hybridization could be a common phenomenon within the highly diverse lizard genus Liolaemus

Hybridization is likely to occur more often between closely related taxa that have had insufficient time to diverge to the point of reproductive incompatibility; hybridization between deeply divergent lineages is rare. In squamate reptiles, hybridization has been proposed as a possible explanation for the extensive paraphyly observed in mitochondrial gene trees in several species complexes of the South American lizard genus Liolaemus. One of the best‐documented cases is within the L. boulengeri and L. rothi complexes, which diverged ~5.5 million years ago. Here, we describe a comprehensive study for approaching the hybridization hypothesis between these lizard species complexes. We explored the level of gene tree discordance using the novel ‘extra lineage contribution’ statistics (XLC, presented in this study) that quantifies the level of gene tree discordance contribution per individual within a species. We included molecular data (12 nuclear and two mitochondrial genes) from 127 individuals, and results of a coalescent model‐based analysis show that the most likely explanation for the gene tree‐species tree discordance is interspecific hybridization. Our best‐supported hypothesis suggests current and past hybridization between L. rothi (rothi complex) and L. tehuelche (boulengeri complex), and independently between L. rothi and L. boulengeri and L. telsen (boulengeri complex). The hybrid descendants are characterized by intermediate phenotypes between the parental species, but are more similar to L. rothi in body size. We discuss the possible role of hybridization in Liolaemus evolution.     

Biodiversity friend or foe: land use by a top predator,the dingo in contested landscapes of the Australian Wet Tropics

Dingoes (Canis dingo) in the coastal lowlands of Australia's Wet Tropics are perceived as a major threat to biodiversity and subjected to broad‐spectrum lethal control. However, evidence of their impacts is equivocal, and control programmes generally ignore the ecological benefits that dingoes might provide. Previous diet analysis has shown that dingoes in the Wet Tropics primarily prey on common, terrestrial mammals. However, little is known of dingo habitat use or prey acquisition in the region despite these activities having major implications for biodiversity conservation. We investigated land use by dingoes in the lowland Wet Tropics to enable predictions of potential prey types, relative prey use and modes of prey acquisition. Nine dingoes were tracked for 3–6 months. Home ranges and resting areas were estimated using multiple estimators, and habitat use was analysed using compositional analysis of habitat use and generalized additive models. Dingo ranging behaviour suggested that anthropogenic food subsidies were infrequently used. Each territory comprised several sclerophyll forest rest areas with adjacent sugarcane‐grassland high activity areas. Individuals used each rest‐activity area for extended durations before moving on to another. Sclerophyll and rainforests, which contain the fauna species of primary conservation concern, were generally used for rest/sleep, or movement between rest‐activity areas. Activity patterns were consistent with dingoes hunting in open sugarcane‐grassland habitats during daylight hours. Dingo activity was low in areas where fauna species of conservation concern occur, which suggests that dingoes do not pose a threat to their survival. Consequently, current broad‐spectrum lethal control may have minimal benefits or even incur costs for biodiversity. Maximizing the ecosystem services provided by dingoes while simultaneously minimizing their negative impacts requires a more targeted location‐specific management approach, one that assesses and mitigates impacts specifically where background circumstances suggest particular packs may be either a conservation or economic threat.