Herbivory limits success of vegetation restoration globally.

Restoring vegetation in degraded ecosystems is an increasingly common practice for promoting biodiversity and ecological function, but successful implementation is hampered by an incomplete understanding of the processes that limit restoration success. By synthesizing terrestrial and aquatic studies globally (2594 experimental tests from 610 articles), we reveal substantial herbivore control of vegetation under restoration. Herbivores at restoration sites reduced vegetation abundance more strongly (by 89%, on average) than those at relatively undegraded sites and suppressed, rather than fostered, plant diversity. These effects were particularly pronounced in regions with higher temperatures and lower precipitation. Excluding targeted herbivores temporarily or introducing their predators improved restoration by magnitudes similar to or greater than those achieved by managing plant competition or facilitation. Thus, managing herbivory is a promising strategy for enhancing vegetation restoration efforts.

Herbivory by European Earwigs (Forficula auricularia; Dermaptera: Forficulidae) on Citrus Species Commonly Cultivated in California.

Agricultural plant species differ in susceptibility to herbivores; therefore, identifying natural resistances or tolerances to pests can be leveraged to develop preventative, integrated pest management approaches. While many Citrus species are grown in California, most pest management guidelines are based upon research conducted on navel oranges [Citrus sinensis (L.) Osbeck; Sapindales: Rutaceae]. A recent study has established European earwigs (Forficula auricularia L.; Dermaptera: Forficulidae) as herbivores of young navel orange fruit, causing damage ranging from small bite marks to large chewed holes. It is unknown whether earwigs damage fruit of other citrus species. We conducted field experiments in which we caged earwigs to branch terminals bearing young fruit to explore potential differences in susceptibility of Citrus species to European earwigs. Specifically, we tested whether three species, navel oranges, clementines (C. clementina hort. ex Tanaka), and true mandarins (C. reticulata Blanco) exhibit differences in: 1) feeding deterrence to earwigs; 2) suitability as food for earwigs; 3) preferential abscission of damaged fruit; and 4) healing of damaged fruit. Earwigs caused heavy damage on navel orange and clementine fruit, whereas heavy damage was rare on true mandarin fruit. There was little evidence of preferential abscission of damaged fruit or healing of seriously damaged fruit. Consequently, several heavily damaged navel orange and one clementine fruit were retained to harvest and developed large scars. Overall, we found that Citrus fruit vary in their susceptibility to earwigs, and pest management strategies for earwigs should be refined to consider their varying effects on different Citrus species.

Characterizing Herbivory by European Earwigs (Dermaptera: Forficulidae) on Navel Orange Fruit with Comparison to Forktailed Bush Katydid (Orthoptera: Tettigoniidae) Herbivory.

In establishing Integrated Pest Management (IPM) plans for understudied pests, it is crucial to understand the nature of their herbivory and resulting damage. European earwig (Forficula auricularia L.; Dermaptera: Forficulidae) densities are increasing in citrus orchards in Central California. Field observations suggest that earwigs feed on young, developing citrus fruit, but this hypothesis had not been examined with formal experimentation. Forktailed bush katydid nymphs (Scudderia furcata Brunner von Wattenwyl; Orthoptera: Tettigoniidae) are well-known citrus herbivores that feed on young citrus fruit, and it is possible that earwig damage may be misdiagnosed as katydid damage. Here we report findings from two field experiments in navel oranges (Citrus sinensis (L.) Osbeck; Sapindales: Rutaceae) that together tested: (1) whether earwigs damage young citrus fruit; (2) whether the amount of damage earwigs generate differs across developmental stage or sex of adult earwigs; (3) the window of time during which fruit are most sensitive to earwig damage; (4) whether damaged fruit are retained to harvest; and (5) the resulting damage morphology caused by earwigs relative to katydids. Earwigs, particularly nymphs, chewed deep holes in young citrus fruit from 0 to 3 wk after petal fall. Fruit damaged by earwigs were retained and exhibited scars at harvest. The morphology and distribution of scars on mature fruit only subtly differed between earwigs and katydids. This study establishes that earwigs can be direct pests in mature navel orange trees by generating scars on fruit and likely contribute to fruit quality downgrades.

Rare plant species are at a disadvantage when both herbivory and pollination interactions are considered in an alpine meadow.

Rare plant species often suffer less damage than common species because of positive density-dependent herbivory, and it has been suggested that this 'rare species advantage' fosters plant species coexistence. However, it is unknown whether rare species have an advantage when pollination interactions are also considered. We hypothesized that a 'positive density-dependent pollination success' across plant species would result in common plants experiencing higher seed set rates compared to rare species, and that positive density-dependent effects would negate or even override the positive density-dependent damage due to herbivory resulting in higher seed loss rates in common plant species. We tested this hypothesis by concurrently examining a plant-predispersal seed predator system and a plant-pollinator system for 24 Asteraceae species growing in an alpine meadow community (Sichuan Province, China). Having previously reported a positive density-dependent effect on seed loss rates due to seed predators, we here focus on the density-dependent effects on pollination success by investigating pollinator species richness, visitation frequencies and seed set rates for each plant species. We also estimated the seed output rate of each plant species as the product of seed set rate and the rate of surviving seeds (i.e. 1 - the seed loss rate). Consistent with our hypothesis, a positive density-dependent effect was observed for pollinator species richness, visitation frequencies and seed set rates across plant species. Moreover, the positive effect overrode the negative density-dependent effect of herbivores on seed production, such that common species tended to have a higher seed output rate than rare species (i.e. we observed a 'rare species disadvantage'). These results indicate that the low seed output rate of rare species might result from a pollination limitation, and that both mutualistic and antagonistic interactions should be examined simultaneously to fully understand plant species coexistence in local communities.

Profile of Fork-Tailed Bush Katydid (Orthoptera: Tettigoniidae) Feeding on Fruit of Clementine Mandarins.

Sweet oranges (Citrus sinensis (L.) Osbeck Sapindales: Rutaceae) dominated commercial citrus production in California until recently when there has been a shift to mandarins, mostly Citrus reticulata (Blanco) mandarins and Citrus clementina (hort. ex Tanaka) clementines. Past analyses of commercial field scouting and harvest data indicated that fork-tailed bush katydids (Scudderia furcata Brunner von Wattenwyl), a major pest in oranges, are present in clementine groves, but that fruit scarring attributed to katydids is rare. Conversely, jagged or web-like scarring attributed to caterpillars was more prevalent than expected. We used two field experiments in four representative cultivars of clementines to test four explanatory hypotheses for this observation: 1) katydids do not feed on clementine fruit, 2) damaged clementine fruit recover, 3) damaged clementine fruit preferentially abscise, and 4) katydid scars on clementine fruit have a different, undocumented morphology, not recognized as katydid damage. We find support for the latter two hypotheses. Katydids fed readily on the clementine fruit of all cultivars tested, chewing irregular holes that developed into jagged or web-like scars of a range of shapes and often led to splitting and abscission of maturing fruit. The katydid scars often more closely resembled chewing caterpillar damage than the round katydid scars in oranges, suggesting that katydid damage is being misclassified in clementines. The resistance documented in some other mandarins was not observed. Katydids are clearly a frugivorous pest causing previously unrecognized scarring in clementines.

Metacommunity robustness of plant-fly-wasp tripartite networks with specialization to habitat loss.

Recent observations have found plant-species-specific fly-host selection (i.e., specialization) of wasp parasitoids (wasps) in plant-fly-wasp (P-F-W) tripartite networks, yet no study has explored the dynamical implications of such high-order specialization for the persistence of this network. Here we develop a patch-dynamic framework for a unique P-F-W tripartite network with specialization observed in eastern Tibetan Plateau and explore its metacommunity robustness to habitat loss. We show that specialization in parasitoidism promotes fly species diversity, while the richness of both plant and wasp decreases. Compared to other two null models, real network structure favors plant species coexistence but increases the extinction risk for both flies and wasps. However, these effects of specialization and network structure would be weakened and ultimately disappear with increasing habitat loss. Interestingly, intermediate levels of habitat loss can maximize the diversity of flies and wasps, while increasing or decreasing habitat loss results in more species losses, supporting intermediate disturbance hypothesis. Finally, we observe that high levels of habitat loss initiate a bottom-up cascade of species extinction from plants to both flies and wasps, resulting in a rapid collapse of the whole tripartite networks. Overall, this theoretical framework is the first attempt to characterize the dynamics of whole tripartite metacommunities interacting in realistic high-order ways, offering new insights into complex multipartite networks.

Asymmetric interactions of seed-predation network contribute to rare-species advantage.

Although the asymmetry of species linkage within ecological networks is now well recognized, its effect on communities has scarcely been empirically investigated. Based on theory, we predicted that an asymmetric architecture of antagonistic plant-herbivore networks would emerge at the community level and that this asymmetry would negatively affect community-common plants more than rare ones. We tested this prediction by analyzing the architectural properties of an alpine plant and pre-dispersal seed-predator network and its effect on seed loss rate of plants in the Tibetan Plateau. This network showed an asymmetric architecture, where the common plant species (with a larger aboveground biomass per area) were infested by a higher number of predator species. Moreover, they asymmetrically interacted with specialized herbivores, presumably because of greater seed resource abundance. In turn, the asymmetric interactions led to a higher proportion of seed loss in the common plants at the species level. Our results suggest that asymmetric antagonistic networks may improve species coexistence by contributing to a mechanism of rare-species advantage.

Domestic honeybees affect the performance of pre-dispersal seed predators in an alpine meadow.

Flowering plants interact simultaneously with mutualistic pollinators and antagonistic herbivores such that plant-mediated interactions between pollinators and herbivores must exist. Although the effects of herbivores on pollinator behavior have been investigated extensively, the effect of pollinators on herbivore performance has seldom been explored. We hypothesized that insect pollinators could improve the survival and growth of pre-dispersal seed predators by increasing seed production. We tested this hypothesis along three transects radiating from well-established apiaries in an alpine meadow by supplementing pollination in sites close to and distant from apiaries and subsequently examining seed production of the dominant nectariferous plant species Saussurea nigrescens (Asteraceae) and the performance of three dominant pre-dispersal seed predators (tephritid fly species). Pollen supplementation (1) significantly increased seed set and mass of developed seed per capitulum (i.e., flowerhead) in the distant but not the close sites, (2) did not change the survival and growth rates of the smaller-bodied species (Tephritis femoralis and Campiglossa nigricauda) at either site, but (3) improved the performance of the larger-bodied seed predator (Terellia megalopyge) at distant sites but not close sites. In addition, the larger-bodied tephritid fly showed higher infestation rates and relative abundance in the close sites than in the distant sites, whereas the smaller-bodied species had lower relative abundances in the close sites and similar infestation rates in both site types. These observations demonstrate contrasting effects of plant mutualists on the performance of antagonists with potential consequences for population sizes of insect herbivores.

Differential responses of body growth to artificial warming between parasitoids and hosts and the consequences for plant seed damage.

Temperature increase may disrupt trophic interactions by differentially changing body growth of the species involved. In this study, we tested whether the response of body growth to artificial warming (~2.2 °C) of a solitary koinobiont endo-parasitoid wasp (Pteromalus albipennis, Hymenoptera: Pteromalidae) differed from its main host tephritid fly (Tephritis femoralis, Diptera: Tephritidae; pre-dispersal seed predator), and whether the plant seed damage caused by wasp-parasitized and unparasitized maggots (larval flies) were altered by warming. In contrast to the significant and season-dependent effects of warming on body growth of the host tephritid fly reported in one of our previous studies, the effect of artificial warming on body growth was non-significant on the studied wasp. Moreover, the warming effect on seed damage due to unparasitized maggots was significant and varied with season, but the damage by parasitized maggots was not altered by warming. Distinct responses of body growth to warming between parasitoids studied here and hosts assessed in a previous study indicate that temperature increase may differentially affect life history traits of animals along food chains, which is likely to affect trophic interactions.

Plant-mediated resource partitioning by coexisting parasitoids.

Although it has been frequently suggested that resource partitioning of species coexisting at the same trophic level can be mediated by interactions with species at non-adjacent trophic levels, empirical evidence supporting this claim is scarce. Here we demonstrate that plants may mediate resource partitioning for two parasitoids that share the same herbivorous host. The tephritid fly Tephritis femoralis is the primary pre-dispersal seed predator of two Asteraceae species, Saussurea nigrescens and Anaphalis flavescens, both of which dominate the plant community in the alpine meadows of the Tibetan Plateau. Field surveys and molecular barcoding analyses showed that the identity of the fly's main predator depended on the plant in which the fly developed. Tephritid flies that developed in S. nigrescens were preyed upon mainly by the parasitoid wasp Pteromalus albipennis, while the parasitoid Mesopolobus sp. was the main predator of flies that developed in A. flavescens. Microcosm experiments revealed that P. albipennis could not exploit the host flies within the capitula of A. flavescens due to food limitation (capitula are too small), while Mesopolobus sp. could not exploit the host flies within the capitula of S. nigrescens due to its inability to reach the host with its ovipositor (capitula are too large). Such bottom-up control of plant species traits may facilitate the coexistence of parasitoid wasps sharing a common host in this system. We suggest that interactions between non-adjacent trophic levels may potentially promote species coexistence and diversity in biological communities.

Soil drainage facilitates earthworm invasion and subsequent carbon loss from peatland soil.

1. Human activities have been a significant driver of environmental changes with tremendous consequences for carbon dynamics. Peatlands are critical ecosystems because they store ~30% of the global soil organic carbon pool and are particularly vulnerable to anthropogenic changes. The Zoige peatland on the eastern Tibet Plateau, as the largest alpine peatland in the world, accounts for 1‰ of global peat soil organic carbon storage. However, this peatland has experienced dramatic climate change including increased temperature and reduced precipitation in the past decades, which likely is responsible for a decline of the water table and facilitated earthworm invasion, two major factors reducing soil organic carbon (SOC) storage of peatlands. 2. Because earthworms are often more active in low- than in high- moisture peatlands, we hypothesized that the simultaneous occurrence of water table decline and earthworm invasion would synergistically accelerate the release of SOC from peatland soil. We conducted a field experiment with a paired split-plot design, i.e. presence vs. absence of the invasive earthworms (Pheretima aspergillum) nested in drained vs. undrained plots, respectively, for three years within the homogenous Zoige peatland. 3. Water table decline significantly decreased soil water content and bulk density, resulting in a marked reduction of SOC storage. Moreover, consistent with our hypothesis, earthworm presence dramatically reduced SOC in the drained but not in the undrained peatland through the formation of deep burrows and decreasing bulk density of the lower soil layer over three years. The variation in SOC likely was due to changes in aboveground plant biomass, root growth, and earthworm behavior induced by the experimental treatments. 4. Synthesis and applications. We suggest that incentive measures should be taken to prevent further water table decline and earthworm invasion for maintaining the soil C pool in Zoige peatland. Artificial filling of drainage canals should be implemented to increase the water table level, facilitating the recovery of drained peatlands. Moreover, the dispersal of earthworms and their cocoons attached to the roots of crop plants and tree saplings from low-lying areas to the Zoige region should be controlled and restricted.

Experimental warming and precipitation interactively modulate the mortality rate and timing of spring emergence of a gallmaking Tephritid fly.

Global climate change is mostly characterized by temperature increase and fluctuating precipitation events, which may affect the spring phenology and mortality rate of insects. However, the interaction effect of temperature and precipitation on species performance has rarely been examined. Here we studied the response of the gall-making Tephritid fly Urophora stylata (Diptera: Tephritidae) to artificial warming, changes in precipitation, and the presence of galls. Our results revealed a significant interaction effect of warming, precipitation, and galls on the life-history traits of the focal species. Specifically, when the galls were intact, warming had no effect on the phenology and increased the mortality of the fly under decreased precipitation, but it significantly advanced the timing of adult emergence and had no effect on the mortality under increased precipitation. When galls were removed, warming significantly advanced the timing of emergence and increased fly mortality, but precipitation showed no effect on the phenology and mortality. In addition, gall removal significantly increased adult fresh mass for both females and males. Our results indicate that the effect of elevated temperature on the performance of species may depend on other environmental conditions, such as variations in precipitation, and species traits like the formation of galls.

The sign of cascading predator effects varies with prey traits in a detrital system.

Theory and experiments show that the nature of 'green' trophic cascades, between predators, herbivores and plants, varies with several key species traits: predator hunting mode and predator and prey habitat domains. Meanwhile, 'brown' cascades between predators, environment-modifying detritivores and plants have been largely overlooked and the roles of species traits, particularly prey traits, in determining the nature of these cascades remains unclear. We hypothesize that, in predator-detritivore-plant interaction chains, the burrowing ability of plant-facilitating detritivores determines their response to predators and thus the sign of indirect effect transmitted. In the dung-decomposer food web of an alpine meadow, we predicted that in the presence of above-ground predacious beetles: (i) non-burrowing detritivores will suffer mortality due to predation and transmit negative indirect effects to plants, whereas (ii) burrowing detritivores will escape predation by retreating deeper into the soil, transmitting positive indirect effects to plants. In support of predictions, experiments showed that a single species of predacious beetle (i) reduced the density of the non-burrowing species and indirectly reduced dung loss rate, soil nutrient concentrations and plant biomass, but (ii) drove the burrowing species deeper, indirectly improved soil conditions and increased plant biomass. These results show that the burrowing ability of a detritivore can determine whether it transmits a negative indirect effect mediated by a reduction in its density, or a positive indirect effect mediated by its behavioural response to predation risk. We call for further tests of our detritivore-trait hypothesis in different regions and ecosystems to further develop a general trait-based framework for trophic cascades in detrital food webs. We further advance the general hypothesis that the locomotion traits of prey species (e.g. burrowing/flying ability) may help explain their behavioural response to predation risk and the nature of indirect effect they transmit from predators to plants.

Artificial asymmetric warming reduces nectar yield in a Tibetan alpine species of Asteraceae.

BACKGROUND AND AIMS: Asymmetric warming is one of the distinguishing features of global climate change, in which winter and night-time temperatures are predicted to increase more than summer and diurnal temperatures. Winter warming weakens vernalization and hence decreases the potential to flower for some perennial herbs, and night warming can reduce carbohydrate concentrations in storage organs. This study therefore hypothesized that asymmetric warming should act to reduce flower number and nectar production per flower in a perennial herb, Saussurea nigrescens, a key nectar plant for pollinators in Tibetan alpine meadows. METHODS: A long-term (6 years) warming experiment was conducted using open-top chambers placed in a natural meadow and manipulated to achieve asymmetric increases in temperature, as follows: a mean annual increase of 0·7 and 2·7 °C during the growing and non-growing seasons, respectively, combined with an increase of 1·6 and 2·8 °C in the daytime and night-time, respectively, from June to August. Measurements were taken of nectar volume and concentration (sucrose content), and also of leaf non-structural carbohydrate content and plant morphology. KEY RESULTS: Six years of experimental warming resulted in reductions in nectar volume per floret (64·7 % of control), floret number per capitulum (8·7 %) and capitulum number per plant (32·5 %), whereas nectar concentration remained unchanged. Depletion of leaf non-structural carbohydrates was significantly higher in the warmed than in the ambient condition. Overall plant density was also reduced by warming, which, when combined with reductions in flower development and nectar volumes, led to a reduction of ∼90 % in nectar production per unit area. CONCLUSIONS: The negative effect of asymmetric warming on nectar yields in S. nigrescens may be explained by a concomitant depletion of leaf non-structural carbohydrates. The results thus highlight a novel aspect of how climate change might affect plant-pollinator interactions and plant reproduction via induction of allocation shifts for plants growing in communities subject to asymmetric warming.

Parasitoid wasps indirectly suppress seed production by stimulating consumption rates of their seed-feeding hosts.

In parasitoid-herbivore-plant food chains, parasitoids may be simultaneously linked with both herbivore hosts and plants, as occurs when herbivores attacked by parasitoids continue to consume plants although they are destined to die. This peculiar property may cause parasitoids to confer a differential trophic cascading effect on plants than that known for typical predators. We hypothesized that larval koinobiont parasitoids would confer an immediate negative effect on plant seed production by stimulating consumption of their seed-predator hosts. We tested this hypothesis in an alpine parasitic food chain of plant seeds, pre-dispersal seed predators (tephritid fly larvae) and koinobiont parasitoids using field observations, a field experiment and a microcosm study. We first compared observed seed production in (i) non-infected capitula, (ii) capitula infected only by seed predators (tephritid flies) and (iii) capitula infected by both seed predators and their parasitoids in five Asteraceae species. Consistent with our hypothesis, seed loss in the capitula with both seed predators and parasitoids was significantly greater than in the capitula infested only by seed predators. This effect was replicated in a controlled field experiment focusing on the most common parasitoid-seed predator-plant interaction chain in our system, in which confounding factors (e.g. density and phenology) were excluded. Here, we show that parasitoids indirectly decreased plant seed production by changing the behaviour of seed predators. In a microcosm study, we show that larval parasitoids significantly extended the growth period and increased the terminal size of their host tephritid maggots. Thus, parasitoids suppressed plant seed production by stimulating the growth and consumption of the fly maggots. In contrast to the typical predator-induced trophic cascade, we highlight the significance of parasitoids indirectly decreasing plant fitness by stimulating consumption by seed predators. Future studies on trophic interactions should consider the net effect of both increased consumption by seed predators and their death after development of parasitoids.

Artificial warming facilitates growth but not survival of plateau frog (Rana kukunoris) tadpoles in presence of gape-limited predatory beetles.

BACKGROUND: Global warming has been frequently demonstrated to increase growth rate in larval amphibians that have considerable phenotypic plasticity; this may lead to an increase in larval survival because large larvae are less likely to be captured by gape-limited predators. This study is to test whether warming could improve tadpole growth and thereby enhance the tadpole survival in plateau frog Rana kukunoris. METHODOLOGY: We conducted an experiment involving growing tadpoles under two contrasting temperatures, i.e. ambient temperature vs. warming by 3.8°C, with and without their major predators--the gape-limited predaceous diving beetles Agabus sp. in eastern Tibetan Plateau, in a factorial arrangement. We recorded the survival and measured body fresh weight and morphological characteristics of the tadpoles. PRINCIPAL FINDINGS: Warming significantly increased body fresh weight in the presence of predators after three weeks of treatments. However, the predators imposed significant and similar effects on the survival of tadpoles under both ambient and elevated temperatures, with the effects mostly occurring in the first three weeks of the experiment. Changes in the body form, i.e. the greater whole length at a given fresh weight and the longer tail at a given body length, could have acted as mechanisms of defense and escape for the tadpoles. CONCLUSIONS/SIGNIFICANCE: Warming did not increase tadpole survival with or without presence of predators. Moreover, an increased growth rate (due to warming in the presence of predators) was not a major factor contributing to the tadpole survival. We postulate that even if warming increases the tadpole growth rate in the plateau frog, it does not necessarily improve their survival in the presence of gape-limited predators.