Enemy-free Space Research Articles

Plant volatiles: Herbivores shush the chatty tree

Plant-insect interactions can be complex and elusive. A new study shows that sap-feeding herbivores reduce tree emissions of specific volatile organic compounds that attract natural enemies. Sap-feeding insects thereby provide enemy-free space for chewing herbivores living on the same tree.

Gene expression plasticity facilitates different host feeding in Ips sexdentatus (Coleoptera: Curculionidae: Scolytinae)

Host shift is ecologically advantageous and a crucial driver for herbivore insect speciation. Insects on the non-native host obtain enemy-free space and confront reduced competition, but they must adapt to survive. Such signatures of adaptations can often be detected at the gene expression level. It is astonishing how bark beetles cope with distinct chemical environments while feeding on various conifers. Hence, we aim to disentangle the six-toothed bark beetle (Ips sexdentatus) response against two different conifer defences upon host shift (Scots pine to Norway spruce). We conducted bioassay and metabolomic analysis followed by RNA-seq experiments to comprehend the beetle’s ability to surpass two different terpene-based conifer defence systems. Beetle growth rate and fecundity were increased when reared exclusively on spruce logs (alternative host) compared to pine logs (native host). Comparative gene expression analysis identified differentially expressed genes (DEGs) related to digestion, detoxification, transporter activity, growth, signalling, and stress response in the spruce-feeding beetle gut. Transporter genes were highly abundant during spruce feeding, suggesting they could play a role in pumping a wide variety of endogenous and xenobiotic compounds or allelochemicals out. Trehalose transporter (TRET) is also up-regulated in the spruce-fed beetle gut to maintain homeostasis and stress tolerance. RT-qPCR and enzymatic assays further corroborated some of our findings. Taken together, the transcriptional plasticity of key physiological genes plays a crucial role after the host shift and provides vital clues for the adaptive potential of bark beetles on different conifer hosts.

Wax on the surface of Phragmites australis leaves provides enemy-free space for the aphid Hyalopterus pruni

Abstract The waxy layer on leaf surfaces may restrict the range of arthropod species that can grip the leaf, thus affecting biological interactions. Here, we report that the wax on the leaf surface of Phragmites australis leaves provides enemy-free space for the aphid Hyalopterus pruni. In our experiment, aphids had higher survival rates on Ph. australis leaves than on Prunus mume leaves in the presence of ladybirds. In addition, removal of wax from the surface of Ph. australis leaves enabled ladybugs to grip the surface of Ph. australis leaves and decreased the survival rate of aphids. These results indicate that the leaf wax of Ph. australis provides enemy-free space for H. pruni by inhibiting ladybird adhesion.

Geographical variation in parasitoid communities and the cause of enemy-free space in a range-expanding myrmecophilous lycaenid butterfly

Abstract Range expansions of host species are likely to modify host–parasitoid interactions. Observational studies have indicated that host species in recently colonized areas are less frequently attacked by parasitoids; however, these studies did not determine whether traditional parasitoids can still use host populations in these areas. Thus, it is unclear why the host has escaped from their traditional parasitoids in their recently colonized areas. In this study, we examined the interaction between myrmecophilous lycaenid butterfly, Arhopala japonica, and its larval parasitoids in northern Japan, a recently colonised area. This region corresponds to a distribution of A. japonica, a myrmecophilous lycaenid butterfly. No parasitoids emerged from A. japonica larvae collected in the north, whereas six parasitoid species attacked the host larvae in native areas. Attacks from the braconid wasp Cotesia sp. near inducta were the most common; however, parasitism tests revealed that Cotesia sp. near inducta and other parasitoid species completed their development successfully regardless of origin of their butterfly hosts. Population genetic analyses supported the recent range expansion of both A. japonica and Cotesia sp. near inducta. These results suggest that both hosts and parasitoids have experienced recent population expansion; however, the more rapid range expansion of A. japonica has caused escape from the enemy in newly colonized areas.

Genetic variation in disease resistance in Drosophila spp. is mitigated in Drosophila sechellia by specialization to a toxic host

We found that Drosophila species vary in their susceptibility to the broad-spectrum entomopathogen, Metarhizium anisopliae (strain Ma549). Generalist species were generally more resistant than dietary specialists, with the cactophilic Drosophila buzzatii and Drosophila sechellia, a specialist of the Morinda citrifolia (Morinda) fruit, being most susceptible. Morinda fruit is reported to be toxic to most herbivores because it contains Octanoic Acid (OA). We confirmed that OA is toxic to Drosophila spp., other than D. sechellia, and we also found that OA is highly toxic to entomopathogenic fungi including Ma549 and Beauveria bassiana. Drosophilasechellia fed a diet containing OA, even at levels much less than found in Morinda fruit, had greatly reduced susceptibility to Ma549. This suggests that specializing to Morinda may have provided an enemy-free space, reducing adaptive prioritization on a strong immune response. Our results demonstrate that M. anisopliae and Drosophila species with divergent lifestyles provide a versatile model system for understanding the mechanisms of host–pathogen interactions at different scales and in environmental context.

Predator efficacy and attraction to herbivore-induced volatiles determine insect pest selection of inferior host plant

Unlike mammals, most invertebrates provide no direct parental care for their progeny, which makes a well-selected oviposition site crucial. However, little is known about the female evaluation of opportunities and threats during host selection. Leveraging the wide range of host plants used by the polyphagous pest, Spodoptera littoralis, we investigate oviposition choice between two plants of different nutritional quality. Females prefer to lay their eggs on the host plant, which has inferior larval development and more natural enemies but provides lower predation rates. On the superior host plant, a major predator shows more successful search behavior and is more attracted to herbivore-induced volatiles. Our findings show that predator efficacy and odor-guided attraction, rather than predator abundance, determine enemy free space. We postulate that predators' behaviors contribute to the weak correlation between preference and performance during host plant selection in S.littoralis and in polyphagous insects in general.

Effect of ant-attendance on the occurrence of intraguild predation

Parasitoids and predators exploiting similar food resource make aphidophagous guilds especially favourable systems for studying intraguild predation, but ants as third parties protect aphids against their natural enemies and in return obtain carbohydrate-rich honeydew as a nutritional resource. A field experiment on the interrelationship among aphids, ants and predators/parasitoids was conducted on two plants (hoary cress Cardaria draba L. [Brassicaceae) and Canada thistle Cirsium arvense L. [Asteraceae]). Cardaria was infested with the aphid Acyrthosiphon gossypii Mordvilko (Homoptera: Aphididae) tended by the ant Lasius turcicus Santschi (Hymenoptera: Formicidae). Cirsium was infested with the aphid Brachycaudus cardui L. (Homoptera: Aphididae) tended by the ant Crematogaster sordidula Nylander (Hymenoptera: Formicidae). The mean number of predators per aphid colony decreased significantly when the aphids were tended by ants on both host plants. In contrast, the parasitism rate of both aphids decreased significantly without the tending ant. Thus ant attendance can affect the occurrence and intensity of intraguild predation, and consequently provide enemy free space for parasitoids. If a foraging female aphid parasitoid succeeds in ovipositing into patches with guarding ants, then its offspring could be protected from the risk of intraguild predation.

Effects of integrated rice-duck farming on weed pressure, herbivore-predator interactions and economic benefits

ABSTRACT This study was conducted to evaluate whether conventional farming can be replaced by a lower chemical pollution farming system, integrated rice-duck farming in a suburban agricultural area in northern Zhejiang, Southeast China. We comprehensively assessed the impacts of integrated rice-duck farming on weeds and herbivorous insects along with their natural enemies during the rice-growing season. We found that the rice-duck system effectively controlled weeds within the paddy fields. Nevertheless, the abundance of herbivores, particularly planthoppers and leafhoppers was increased in the duck-roaming paddy fields compared to the control and conventional fields, indicating the inefficiency of the rice-duck system in the control of rice main herbivore pests. Rice-duck farming significantly reduced the abundance of predators, especially spiders and dragonflies, therefore an ‘enemy-free space’ was created for herbivores which might be responsible for the observed herbivore increase in the rice-duck fields. Despite the inefficiency of rice-duck farming in the control of rice main herbivore pests, the net income of the rice-duck treatment with an organic certification was 7.6 and 1.4 times higher compared to the conventional and control treatments, respectively. In the view of the favourable results obtained in this study, the integrated rice-duck farming system might be suggested as a high economic return organic farming method suitable for modern farmers.

Social predation by ants as a mortality source for an arboreal gregarious forest pest

Biocontrol of caterpillars by ants is highly variable, and we investigate how the strength of the trophic relationship between ants and an important outbreaking forest pest depends on phenological synchrony and on social foraging. We test the hypothesis that early spring foraging by ants, coupled with eusocial recruitment behavior, could undermine the caterpillar's strategies to achieve either enemy-free space or predator satiation.We use a series of field surveys and experiments in trembling aspen stands (Populus tremuloides) in the boreal forest of eastern Canada to assess the role of ants in early-instar mortality of the outbreaking, gregarious forest tent caterpillar (Malacosoma disstria). We also investigate individual-level mechanisms related to phenology and social behavior that underlie the effectiveness of ants as biocontrol on caterpillars. Our results show that ants climb trees early in the spring and harvest young forest tent caterpillars, suggesting that early phenology does not provide an entirely enemy-free space for caterpillars. Our findings further show that recruitment-based social foraging enables ants to deplete groups of gregarious prey, suggesting that these eusocial insects are particularly effective at generating predation pressure on gregarious herbivores since they do not satiate easily. Finally, a manipulative predator exclusion experiment confirms that ant predation is a significant mortality source for early-instar forest tent caterpillars. Taken together, these results suggest that phenology and sociality could modulate the role of ants as effective caterpillar predators and thus showcase the importance of considering natural history and behavioral traits when studying trophic interactions and their role in population dynamics.

The biological control process and describe the next steps in our international collaboration with researchers in Indonesia to find appropriate natural enemies of albizia

Classical biological control refers to the intentional introduction of a natural enemy from the native range of an invasive species into the presumably enemy-free space of the invaded range. The objective of biocontrol is for introduced agents to establish permanently and provide long-term suppression of an invasive species, as well as the restoration of ecological balance. The island of Hawaii is negatively impacted by an invasive tree native to Indonesia, albizia (Falcataria moluccana, known locally in Indonesia as sengon or salawaku), which destroys native landscapes and threatens Hawaii businesses and homes with many millions of dollars in damage. We have completed exploratory surveys in Indonesia searching for specialist natural enemies of this invasive tree that will eventually undergo extensive host specificity and impact testing prior to release in Hawaii. Two high priority candidates for further study include gall forming eriophyid mites and a stem boring weevil. Also among early prospects is a rust fungus (Uromycladium falcatarium) that galls new growth and is a major problem for albizia plantations in the Philippines and Indonesia. Here we discuss the biological control process and describe the next steps in our international collaboration with researchers in Indonesia to find appropriate natural enemies of albizia.

Caterpillar-induced rice volatiles provide enemy-free space for the offspring of the brown planthopper.

Plants typically release large quantities of volatiles in response to herbivory by insects. This benefits the plants by, for instance, attracting the natural enemies of the herbivores. We show that the brown planthopper (BPH) has cleverly turned this around by exploiting herbivore-induced plant volatiles (HIPVs) that provide safe havens for its offspring. BPH females preferentially oviposit on rice plants already infested by the rice striped stem borer (SSB), which are avoided by the egg parasitoid Anagrus nilaparvatae, the most important natural enemy of BPH. Using synthetic versions of volatiles identified from plants infested by BPH and/or SSB, we demonstrate the role of HIPVs in these interactions. Moreover, greenhouse and field cage experiments confirm the adaptiveness of the BPH oviposition strategy, resulting in 80% lower parasitism rates of its eggs. Besides revealing a novel exploitation of HIPVs, these findings may lead to novel control strategies against an exceedingly important rice pest.

Competition for safe real estate, not food, drives density-dependent juvenile survival in a large herbivore.

Density‐dependent competition for food reduces vital rates, with juvenile survival often the first to decline. A clear prediction of food‐based, density‐dependent competition for large herbivores is decreasing juvenile survival with increasing density. However, competition for enemy‐free space could also be a significant mechanism for density dependence in territorial species. How juvenile survival is predicted to change across density depends critically on the nature of predator–prey dynamics and spatial overlap among predator and prey, especially in multiple‐predator systems. Here, we used a management experiment that reduced densities of a generalist predator, coyotes, and specialist predator, mountain lions, over a 5‐year period to test for spatial density dependence mediated by predation on juvenile mule deer in Idaho, USA. We tested the spatial density‐dependence hypothesis by tracking the fate of 251 juvenile mule deer, estimating cause‐specific mortality, and testing responses to changes in deer density and predator abundance. Overall juvenile mortality did not increase with deer density, but generalist coyote‐caused mortality did, but not when coyote density was reduced experimentally. Mountain lion‐caused mortality did not change with deer density in the reference area in contradiction of the food‐based competition hypothesis, but declined in the treatment area, opposite to the pattern of coyotes. These observations clearly reject the food‐based density‐dependence hypothesis for juvenile mule deer. Instead, our results provide support for the spatial density‐dependence hypothesis that competition for enemy‐free space increases predation by generalist predators on juvenile large herbivores.

Enemy-free space and the distribution of ants, springtails and termites in the soil of one tropical rainforest

The soil fauna of tropical rainforests is difficult to study because of its extreme species richness and taxonomic impediment. Studies of multi-taxon assemblages in the soil of tropical rainforests are relatively rare and studies of interspecific interactions, such as predation, even rarer. Here we attempt to infer prey predator interactions and enemy-free space from the faunal composition of 100 litter/soil samples obtained from Barro Colorado Island in Panama during the dry and wet seasons. We focused on assemblages of ants (assigned to categories of non-predators, potential and confirmed predators), springtails and termites, which were characterized by their Barcode Index Numbers. Overall in 0.2 m3 of soil/litter we collected 2129 ants, 5592 springtails and 260 termites, which represented 80, 104 and 15 species, respectively. The faunal composition of confirmed ant predators was spatially coincident with that of Collembola. However, despite considerable seasonal shifts in the rank abundance of Collembola species, seasonal shifts of confirmed ant predators were low, resulting in a poor match of seasonal shifts between ants and their prey items. No location could be considered as being relatively free of ant enemies for springtails or termites, but the dry season supported higher prey-predator ratios than the wet season. We inferred only 4 possible prey-predator interactions, out of 7616 potential interactions in the study system. The relative dispersion of confirmed ant predators, which only weakly influenced springtail and termite assemblages, suggests low specificity in ant-prey interactions. This confirms that “brown food webs” may be structured by bottom-up effects rather than by top-down effects.

Top-down and bottom-up controls on an herbivore on a native and introduced plant in a tropical agricultural landscape.

The recent introduction in a tropical agricultural environment of a weedy open-habitat plant (Solanum myriacanthum) and subsequent host range expansion of a common forest-edge butterfly (Mechanitis menapis) onto that plant provides an opportunity to examine reconfiguration of tritrophic networks in human-impacted landscapes. The objectives of this study were (1) determine if the caterpillars on the exotic host are more or less limited by plant defenses (bottom-up forces) and if they experience enemy release (decrease of top-down pressure) and (2) define how anthropic open pasture habitat influences the herbivore’s tritrophic niche. Field and laboratory monitoring of larval survival and performance on a native (Solanum acerifolium) host plant and the exotic (S. myriacanthum) host plant were conducted in the Mindo Valley, Ecuador. Plant physical defenses were also measured. Results showed that larval mortality was mostly top-down on S. acerifolium, linked to parasitism, but mostly bottom-up on S. myriacanthum, possibly linked to observed increased plant defenses. Thus, in the absence of co-evolved relationships, herbivores on the exotic host experienced little top-down regulation, but stronger bottom-up pressures from plant defenses. These findings provide a rare empirical example of enemy-free space as a mechanism underlying host-range expansion. S. myriacanthum was less colonized in open pastures than in semi-shaded habitats (forest edges, thickets): fewer eggs were found, suggesting limited dispersal of adult butterflies into the harsh open environments, and the survival rate of first instar larvae was lower than on semi-shaded plants, likely linked to the stronger defenses of sun-grown leaves. These findings show how environmental conditions modulate the rewiring of trophic networks in heavily impacted landscapes, and limit a biocontrol by a native herbivore on an invasive plant in open habitats.

Long-term changes in mole cricket body size associated with enemy-free space and a novel range

Exotic species can cause ecosystem and landscape-level changes in their novel ranges, but factors associated with novel ranges can also change the invaders. By tracking trait changes over space and time, we can learn about the future ecological and economic implications of invasive species’ dispersal. Here, we investigated body size changes of two invasive mole cricket species, Neoscapteriscus borellii and N. vicinus, introduced to the U.S. from South America (≈ 1904) without natural enemies, and later exposed to them (≈ 1980) through classical biological control. We compared body sizes of N. vicinus and N. borellii in the novel range from before biological control and 30 years after, as well as N. borellii in its native range at the same time period. Contrary to expectations, our data suggest that N. borellii and N. vicinus body sizes have increased since re-establishment of interactions with their natural enemies. Our results also suggest that N. borellii body size decreased in enemy-free space after U.S. invasion and prior to biological control. Selection or reduced intraspecific competition, both likely associated with biological control, may explain the changes in body size over time. Although these results warrant further research, they provide valuable insights into the long-term effects of invasion and classical biological control.

Patch Size as a Niche Dimension: Aquatic Insects Behaviorally Partition Enemy-Free Space across Gradients of Patch Size.

Positive correlation of species richness with area is ubiquitous in nature, but the processes driving that relationship, as well as those constraining typical patterns, remain elusive. Patch size variation is pervasive in natural systems, and it is thus critical to understand how variation in patch size, as well as its potential interaction with factors like predation and isolation, affects community assembly. We crossed patch quality (fish presence/absence) with patch size to the examine effects of quality, size, and their interaction on colonization by aquatic insects. Overall, beetles favored small, fishless patches, but individual species sorted across patch size while hemipterans aggregated into large, fishless patches, producing sorting between Coleoptera and Hemiptera. Both patch size and predation risk generated significant variation in community structure and diversity. Patch size preferences for the 14 most abundant species and preeminence of species turnover in patterns of β-diversity reinforce patch size as a driver of regional species sorting via habitat selection. Species sorting at the immigration stage plays a critical role in community assembly. Identifying patch size as a component of perceived quality establishes patch size as a critical niche dimension and alters our view of its role in assembly dynamics and the maintenance of local and regional diversity.

Generalism in Nature…The Great Misnomer: Aphids and Wasp Parasitoids as Examples.

In the present article we discuss why, in our view, the term ‘generalism’ to define the dietary breadth of a species is a misnomer and should be revised by entomologists/ecologists with the more exact title relating to the animal in question’s level of phagy—mono-, oligo, or polyphagy. We discard generalism as a concept because of the indisputable fact that all living organisms fill a unique ecological niche, and that entry and exit from such niches are the acknowledged routes and mechanisms driving ecological divergence and ultimately speciation. The term specialist is probably still useful and we support its continuing usage simply because all species and lower levels of evolutionary diverge are indeed specialists to a large degree. Using aphids and parasitoid wasps as examples, we provide evidence from the literature that even some apparently highly polyphagous agricultural aphid pest species and their wasp parasitoids are probably not as polyphagous as formerly assumed. We suggest that the shifting of plant hosts by herbivorous insects like aphids, whilst having positive benefits in reducing competition, and reducing antagonists by moving the target organism into ‘enemy free space’, produces trade-offs in survival, involving relaxed selection in the case of the manicured agro-ecosystem.

Changing Host Plants Causes Structural Differences in the Parasitoid Complex of the Monophagous Moth Yponomeuta evonymella, but Does Not Improve Survival Rate.

Recently in Poland, cases of host expansion have frequently been observed in the typically monophagous bird-cherry ermine moth (Yponomeuta evonymella), which has moved from its native host plant, bird cherry (Prunus padus), to a new, widely distributed plant that is invasive in Europe, black cherry (P. serotina). We attempted to verify the reasons behind this host change in the context of the enemy-free space hypothesis by focusing on parasitoids attacking larval Y. evonymella on one of three host plant variants: The primary host, P. padus; initially P. padus and later P. serotina (P. padus/P. serotina); or the new host, P. serotina. This experiment investigated if changing the host plant could be beneficial to Y. evonymella in terms of escaping from harmful parasitoids and improving survival rate. We identified nine species of parasitoids that attack larval Y. evonymella, and we found that the number of parasitoid species showed a downward trend from the primary host plant to the P. padus/P. serotina combination to the new host plant alone. We observed a significant difference among variants in relation to the percentage of cocoons killed by specific parasitoids, but no effects of non-specific parasitoids or other factors. Total mortality did not significantly differ (ca. 37%) among larval rearing variants. Changing the host plant caused differences in the structure of the parasitoid complex of Y. evonymella but did not improve its survival rate. This study does not indicate that the host expansion of Y. evonymella is associated with the enemy-free space hypothesis; we therefore discuss alternative scenarios that may be more likely.

The Importance of Shifting Disturbance Regimes in Monarch Butterfly Decline and Recovery

The Eastern migratory monarch butterfly has declined in recent decades, partly because widespread adoption of herbicide-resistant corn and soybean has nearly eliminated common milkweed from crop fields in the US Midwest. We argue that in addition to milkweed loss, monarch declines were likely exacerbated by shifting disturbance regimes within their summer breeding range. Monarchs prefer to lay eggs on younger, vegetative milkweed stems. They also benefit from enemy-free space, as most eggs and early-instar larvae succumb to predators. Historically, ecological disturbances during the growing season could have provided these conditions. During most of the 19th and 20th centuries, milkweed was abundant in crop fields where manual weeding and mechanical cultivation set milkweed back, but rather than killing it would often stimulate regrowth later in the summer. Before European settlement, large mammals and fires (natural and anthropogenic) perturbed grasslands during the summer and could have had similar effects. However, presently most remaining milkweed stems in the Midwest are in perennial grasslands like roadsides, old-fields, parks, and conservation reserves, which often lack growing season disturbance. As a result, monarchs may be left with limited options for oviposition as the summer progresses and could have lower survival in grasslands where predation pressure is high. Our recent work has shown that targeted disturbance during the growing season produces milkweed stems that are attractive to ovipositing monarchs and harbor fewer arthropod predators. Targeted disturbance in perennial grasslands could improve habitat heterogeneity and phenologic diversity of milkweeds, and should be explored as a monarch conservation strategy.

Grassland disturbance increases monarch butterfly oviposition and decreases arthropod predator abundance

Many species of conservation concern depend on disturbance to create or maintain suitable habitat. We evaluated effects of disturbance on the eastern migratory monarch butterfly (Danaus plexippus L.), which has declined markedly in recent decades, primarily attributed to the loss of milkweed host plants from annual crop fields in the US Midwest. Currently, remaining milkweeds in this region primarily occur in perennial grasslands, where disturbance is infrequent, predatory arthropods are abundant, and seasonal patterns of plant phenology differ from crop fields. In a two-year study in Michigan, USA, we applied three treatments to 23 patches of common milkweed (Asclepias syriaca L.); one-third of each patch was left undisturbed, while the remaining thirds were mowed in either mid-June or mid-July, respectively, and allowed to regenerate. We subsequently measured effects on monarch oviposition, predator abundance, survival of sentinel eggs and larvae, and tested how milkweed phenology and aphid colonization—both of which are reset by disturbance—structure predation risk for immature monarchs. Monarchs laid more eggs on regenerating versus undisturbed stems under both mowing regimes. Predators were strongly suppressed by mowing treatments, requiring 2–4 weeks to recolonize milkweed after disturbance, and were more abundant on flowering or aphid-infested stems. We found no significant differences in monarch egg/larval survival, although it tended to be higher in mowed plots. Overall, monarchs laid more eggs on regenerating stems where their offspring may also experience enemy-free space. Future work should focus on testing grassland disturbance as a management tool to improve productivity of existing monarch breeding habitat.