Leaf extrafloral nectaries enhance biological control of a key economic pest, Grapholita molesta (Lepidoptera: Tortricidae), in peach (Rosales: Rosaceae)

Extrafloral nectaries (EFNs) in many plant species produce sugary secretions that commonly attract ants. This research determined the impact of peach (Prunus persica L. Batsch) EFNs on the biological control of the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), a key economic pest in peach orchards, and studied interactions of EFNs and ants. Studies (2002-2005) in peach orchards of the mid-Atlantic United States showed that 'Lovell' peach trees with EFNs supported more parasitic Hymenoptera in the spring and increased the parasitism of G. molesta larvae later in the season than those trees without EFNs. Ant exclusion experiments revealed that trees with EFNs harbored fewer G. molesta larvae when ants were permitted access to the tree canopies. Furthermore, the trees with EFNs had approximately 90% less fruit injury by G. molesta, indicating that EFNs have a protective role for the fruit as well. The results show that the combined actions of ants and parasitic Hymenoptera confer an EFN-mediated protective effect spanning the whole fruit growing season. When EFNs are present, naturally occurring biological control agents can reduce damage by G. molesta in peach orchards without insecticide inputs. The EFNs are an important host-plant characteristic that should be retained in future peach cultivar selections as a means of enhancing biological control.     

Effects of orchard host plants on the oviposition preference of the oriental fruit moth (Lepidoptera: Tortricidae)

Recently, the oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), has emerged as a major problem on apples (Malus spp.) grown in the mid-Atlantic and midwestern United States, despite its historically important and frequent occurrence as a peach (Prunus spp.) pest. It is possible that host-driven biological phenomena may be contributing to changes in G. molesta population dynamics resulting in outbreaks in apple. Studies were designed to examine the effects of host plants on oviposition behavior, in an effort to clarify the host association status of eastern U.S. populations and also to gain insight into how pest modeling and management efforts may be altered to take into account various host-associated effects. G. molesta adults exhibited ovipositional preference for nonbearing peach trees over nonbearing apple trees in close-range choice tests conducted in the field, regardless of the larval host origin. A significant preference for peach shoots over apple shoots was observed on six of 12 sampling dates with a wild G. molesta population at the interface of adjacent peach and apple blocks. Numbers of eggs found on apple fruit were higher after peach fruit were harvested and apple fruit began to approach maturity (during the flight period for third and fourth brood adults). Possible implications for population modeling and integrated management of G. molesta are discussed.     

湖北老河口梨小食心虫成虫发生规律及综合防治效果

【目的】为了寻找湖北省老河口梨小食心虫Grapholita molesta(Busck)的最佳防治时期,推广使用无公害防控技术,减少化学药剂的使用。【方法】分别调查了梨小食心虫在梨园及桃园的发生规律,释放赤眼蜂的生物防治效果,糖醋酒液、三角形诱捕器、黄板的物理防治效果,以及性信息素迷向防治效果。【结果】结果表明,桃园梨小食心虫最佳防治时期在4月中下旬,梨园梨小食心虫最佳防治时期在5月下旬、6月上旬、8月中旬前。防治效果上,释放赤眼蜂生物防治措施、配比为红糖∶白酒∶食用醋:水=3∶1∶3∶80的糖醋酒液诱捕器的物理防治措施、迷向丝及迷向素的迷向措施均有替代化学防治措施的潜力。【结论】综合防治能够有效控制梨园梨小食心虫发生量,减少化学防治频次,为建立稳定的梨园生态系统及生产无公害水果提供了帮助。     

Ontogenetic succession and the ant mosaic: An empirical approach using pioneer trees

Arboreal ant mosaics have been intensively investigated, but what generates these mosaics remains poorly understood. In this paper, we hypothesize that the dynamics of arboreal ant mosaics could be better understood by examining the ontogenetic succession of ants in tropical trees. We used three African pioneer tree species as biological models. Lophira alata (Ochnaceae) is a long-lived species that does not furnish any reward (i.e., extra-floral nectaries [EFNs], shelter) to ants, Anthocleista vogelii (Gentianaceae) bears extremely well-developed EFNs, and Barteria fistulosa (Passifloraceae) is a long-lived myrmecophyte providing both EFNs and domatia. For both L. alata and A. vogelii, we noted a succession of different associated ants as the plants grew and aged. Ground-nesting, arboreal-foraging ant species were the first associates, followed by arboreal species that build nests with the leaves of their host trees, together with some species nesting opportunistically in pre-existing cavities. Carton-building Crematogaster species were the last in this succession. The presence of EFNs on A. vogelii slows species turnover, demonstrating that the plant exerts some control over its ant associates. The comparison with B. fistulosa, which generally remains associated with the same plant-ant species during its entire ontogeny, highlights the importance of the selective attractiveness of the trees for their associated ants – or, perhaps, the existence of plant filters that screen arriving ants.     

The function of extrafloral nectaries in the pollination and reproduction of Sambucus javanica

Sambucus javanica is a perennial herb with extrafloral nectaries (EFNs) on its inflorescences. To explore the ecological functions of EFNs, a factorial combination experiment of ant (access or exclusion) and EFNs (with or without) at the plant level was created in two populations. The role of EFNs in the attraction of ants and flying pollinators, the defensive role of ants against foliar herbivores, the effects of ants on pollinator visitation and the effects of ant–pollinator interactions on fruit production in one or both populations were assessed. Ants were common on the ant-access plants with EFNs, but absent from the ant-access plants without EFNs. Foliar herbivory was independent of ant and EFN treatments and their interactions. The visitation frequency of flying pollinators (honeybees and syrphid flies) and fruit set were significantly higher for plants with EFNs than plants without EFNs, but were not affected by ant treatments or their interactions with EFN treatments. These results suggest that EFNs in S. javanica attracted both ants and flying pollinators, but ants did not present a defensive role against herbivores, did not deter flying pollinators from visiting inflorescences and had no effects on fruit production. In addition, ants were not significant pollen vectors.     

Habitat isolation affects plant–herbivore–enemy interactions on cherry trees

Understanding the interactions between herbivores and natural enemies in fragmented landscapes is essential for conservation biological control. Studies including multiple enemies affecting multiple herbivores, plant damage and growth are needed. Here, we separated independent effects of (1) isolation of cherry trees from woody habitat and (2) the amount of woody habitat in the surrounding landscape (500 m buffers) on interactions between different groups of herbivores with their natural enemies and resulting changes in the growth of young cherry trees. Most predatory arthropods declined with habitat isolation, except some aphid predators (ladybeetles and hoverflies). Herbivores either increased with isolation (herbivorous beetles) or showed no significant response (aphids). In contrast, the amount of woody habitat in the landscape was not relevant for herbivore–enemy interactions at the investigated scale. Plant growth was affected by bottom-up (nutrient availability) and top-down (aphid density) forces but did not change significantly with habitat amount or isolation. We conclude that herbivores can be released from natural enemies at isolated sites, in accordance with the hypothesis that habitat connectivity improves pest control. However, each herbivore group responded differently to the landscape context and had contrasting effects on the same host plant, demonstrating the difficulty to predict landscape effects on plant growth.     

我国梨小食心虫综合防治研究进展

近年来,由于农业产业结构的调整,我国北方果树栽培种类日益增多、种植面积不断扩大。重要果树害虫梨小食心虫Grapholitha molesta(Busck)为害大幅回升、危害逐年增加。针对这一情况,在西北、东北和华北3个北方果树生产代表区域建立50余个监测示范点,开展了梨小食心虫的生物生态学规律及综合防治技术的研究、集成与示范。研究结果表明,气候变化和种植结构对梨小食心虫发生规律有显著影响。全球气候变暖条件下,梨小食心虫年发生世代呈增加趋势;在果树混栽区域,晚熟桃为梨小食心虫的主要越冬场所。防治技术方面,在对梨小食心虫常规农业防治、物理防治、生物防治、化学防治技术组装配套的基础上,重点开展了高效节水诱捕器、国产迷向产品研发及标准化应用技术、优势天敌饲养及释放技术、专用农药研发及农药减量化技术等研究工作。前瞻性地研发了植物源诱捕剂及迷向新剂型等贮备技术。最后针对当前梨小食心虫防治工作中存在的问题和不足,确定了下一步的研究方向:(1)全球气候变暖对梨小食心虫发生动态的影响;(2)梨小食心虫成虫不同寄主间的转移规律;(3)梨小食心虫的抗性监测技术和快速诊断试剂盒研制;(4)梨小食心虫的抗性分子机理与抗性治理技术。     

Insights into a novel three-partner interaction between ants,coreids (Hemiptera: Coreidae) and extrafloral nectaries: implications for the study of protective mutualisms

Extrafloral nectar of plants and honeydew of hemipterans are the common mediators of facultative interactions that involve ants as a mobile strategy of defence. The outcome of these interactions can vary from mutualistic to commensalistic or even antagonistic, depending on the ecological context and the interacting species. Here, we explore a novel, three-partner interaction involving ants, the coreid Dersagrena subfoveolata (Hemiptera) and the extrafloral nectaries (EFNs) bearing plant Senna aphylla (Fabaceae) in semi-arid Northwest Argentina. We surveyed natural areas and conducted ant exclusion experiments, to understand how each pairwise interaction influences the overall outcome among the three interacting parts. The outcome of the interactions was assessed for experimental plants as the reproductive output and herbivore abundances and for coreids as predator abundances. We found that the coreids occurred exclusively on S. aphylla plants and that at least nine ant species interacted with the EFNs as well as with the coreids. Coreid occurrence and abundance depended on ant densities, which in turn, was determined by the presence of actively secreting EFNs. Coreid and ant presence did not influence plant reproductive success, and ants provided to coreids some biotic defence, mainly against vespid wasp predators, but had no effect on non-coreid herbivores. We conclude that the interaction outcome is commensalistic between ants and plants (assuming that EF nectar is not costly for the plant), antagonistic between coreids and plants, and mutualistic between coreids and ants. The sum of all outcomes is net positive effect for ants and coreids, and net slightly negative to neutral for plants.     

Effects of orchard host plants (apple and peach) on development of oriental fruit moth (Lepidoptera: Tortricidae)

Studies were designed to examine the effects of host plants (apple, Malus domestica Borkh., and peach, Prunus persica L.) on the development of oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae). Oriental fruit moth larvae developed faster on peach than on apple, both on fruit as well as on growing terminal shoots. On fruit, these differences were shown to cause significant changes in both the rate (approximately 20-60 degree-days earlier emergence on peach than on apple) and patterns of adult emergence among several cultivars of peaches and apples. Slopes of female emergence plots varied by host in 2003, with emergence occurring over a longer period on peach cultivars than on apple cultivars (with one exception). Slopes of male emergence curves did not differ by cultivar in 2003. These host-driven effects could impact the efficacy of traditional pest management approaches and probably complicate efforts to predictively model G. molesta populations in mixed cultivar orchards. Such developmental effects may help to explain previously observed differences in patterns of pheromone trap captures in peach versus apple orchards. Host-associated effects should be incorporated into future models to develop more realistic predictive tools and thus improve integrated pest management efforts.     

Plant-attracted ants affect arthropod community structure but not necessarily herbivory

Abstract.  1. The effectiveness of ants as plant defenders is equivocal for plants that attract ants via extrafloral nectaries (EFNs).
2. This study focused on the myrmecophilic savannah tree Pseudocedrela kotschyi that attracts ants to EFNs and on the arthropod fauna associated with P. kotschyi . Herbivory and arthropod community composition were compared between trees that were dominated by one of three congeneric ant species, Camponotus acvapimensis , C. rufoglaucus , and C. sericeus , and between trees where ants were experimentally excluded and untreated control trees.
3. Short-term ant-exclusion experiments failed to demonstrate a consistent effect of ants on herbivory.
4. Plants dominated by different ant species differed significantly in leaf damage caused by herbivorous insects. The relative ranking of herbivory levels of the trees dominated by different ant species was persistent in three consecutive years.
5. Ants significantly reduced the abundance of different arthropod groups (Araneae, Blattodea, Coleoptera, Homoptera, non-ant Hymenoptera). Other groups, including important herbivores, seemed not to be affected (Lepidoptera, Orthoptera, Thysanoptera, Heteroptera).
6. The study suggests that the presence of ants only benefits plants when specific ant species are attracted, and protection by these ants is not counterbalanced by their negative effect on other beneficial arthropods.     

Sugar secretion and ant protection in Ficus benguetensis: Toward a general trend of fig–ant interactions

The relationship between plants and ants is often mediated by the presence of extrafloral nectaries (EFNs) that attract ants and provide rewards by protecting plants from herbivores or parasites. Ficus trees (Moraceae) and their pollinators (Hymenoptera: Agaonidae) are parasitized by many nonpollinating fig wasp species (Hymenoptera: Chalcidoidea) that decrease the reproductive output of the mutualistic partners. Previous studies have shown that ants living on and patrolling Ficus species can efficiently deter parasitic wasps. The aim of this study was to verify the presence of EFNs on figs of Ficus benguetensis and test the hypothetical protection service provided by ants. Figs in different developmental stages were collected from Fu-Yang Eco Park, Taipei, Taiwan. Sugars on the fig surface were collected and analyzed through high-performance anion-exchange chromatography. Moreover, ants were excluded from the figs to determine the effect of ants on the nonpollinating fig wasps. We identified three oligosaccharides whose relative proportions varied with the fig developmental phase. In addition, results showed that the ant-excluded figs were heavily parasitized and produced three times less pollinators than did the control figs. Finally, the specific interactions of Ficus benguetensis with ants and the relationship between figs and ants in general are discussed.     

Extrafloral nectary-bearing plant Mallotus japonicus uses different types of extrafloral nectaries to establish effective defense by ants

Extrafloral nectary (EFN)-bearing plants attract ants to gain protection against herbivores. Some EFN-bearing plants possess different types of EFNs, which might have different effects on ants on the plants. Mallotus japonicus (Thunb.) Muell. Arg. (Euphorbiaceae) bears two types of EFNs, including a pair of large EFNs at the leaf base and many small EFNs along the leaf edge. This study aimed to determine the different roles of the two types of EFNs in biotic defense by ants. A field experiment was conducted to investigate the effect of leaf damage on EFN production and on the distribution pattern of ants. After leaf damage, the number of leaf edge EFNs increased in the leaves first-produced. The number of ants on the leaves also increased, and the foraging area of ants extended from the leaf base to the leaf tip. An EFN-covering field experiment revealed that leaf edge EFNs had a greater effect than leaf base EFNs on ant dispersal on leaves. The extended foraging area of ants resulted in an increase of encounter or attack rate against an experimentally placed herbivore, Spodoptera litura. These results suggest that M. japonicus plants control the foraging area of ants on their leaves using different types of EFNs in response to leaf damage, thus achieving a very effective biotic defense against herbivores by ants.

     

Do weaver ants affect arthropod diversity and the natural‐enemy‐to‐pest ratio in horticultural systems?

High biodiversity is an important component of sustainable agricultural systems, and previous studies have found that increases in the diversity of the natural enemies of pests are associated with decreases in pest populations. Weaver ants are well known for their highly territorial and aggressive behaviour and for their control efficiency of many insect pests in tropical crop trees. Because of this, the ants have been used as a key component in integrated pest management (IPM) programmes for tropical crop trees. In implementing the IPM programmes, we received a number of enquiries related to whether weaver ants have negative effects on arthropod diversity and other natural enemies in orchard systems due to their aggressive behaviour. To answer these questions, we regularly sampled canopy arthropods in cashew and mango orchards in the Northern Territory of Australia in 1996, 2002 and 2003. We sampled, using a vacuum sampler, orchards with and without weaver ants. Cashew and mango plots with abundant weaver ants had similar or higher canopy arthropod and natural enemy diversity and similar ratios of natural enemies to insect pests, compared with plot where the weaver ant was absent. The study also showed that the application of insecticides reduced arthropod diversity and the ratio of natural enemies to insect pests in a mango orchard. However, insecticide spray did not affect natural enemy diversity and abundance, which may be related to a high immigration rate of natural enemies in small plots surrounded by areas that were not sprayed.     

Interaction between ants, extrafloral nectaries and insect herbivores in Neotropical coastal sand dunes: herbivore deterrence by visiting ants increases fruit set in Opuntia stricta (Cactaceae)

1. This study examines the anti-herbivore effect of ants visiting the extrafloral nectaries (EFNs) of Opuntia stricta (Cactaceae) and its possible influence on the plant's reproductive output in Mexican coastal sand dunes. Opuntia 's EFNs are located in the areoles of the developing tissue of emerging cladodes and flower buds.
2. Ants visited the EFNs of O . stricta on a round-the-clock basis. The associated ant assemblage was formed by nine species distributed in four subfamilies, and the species composition of the principal ant visitors changed markedly from day to night period.
3. Cladodes of control (ants present) and treatment (ants excluded) plants of Opuntia were equally infested by sucking bugs and mining dipterans. Damage to buds by a pyralid moth, however, was significantly higher on treatment than on control plants. Ant visitation to Opuntia 's EFNs translated into a 50% increase in the plant's reproductive output, as expressed by the number of fruits produced by experimental control and treatment branches. Moreover, fruit production by ant-visited branches was positively and significantly associated with the mean monthly rate of ant visitation to EFNs.
4. This is the first demonstration of ant protection leading to increased fruit set in the Cactaceae under natural conditions. Although the consequences of damage by sucking and mining insects remain unclear for Opuntia , the results show how the association of EFNs with vulnerable reproductive plant organs can result in a direct ant-derived benefit to plant fitness.     

Development and implementation of a reduced risk peach arthropod management program in New Jersey

We implemented a 2-yr program to reduce organophosphorus and carbamate insecticide use and mitigate their associated risks as they relate to peach production in New Jersey and elsewhere. The main thrust integrated mating disruption with ground cover management practices to reduce oriental fruit moth, Grapholita molesta (Busck) (Lepidoptera: Tortricidae), and tarnished plant bug, Lygus lineolaris (Palisot de Beauvois) (Heteroptera: Miridae), abundance and damage. This Reduced Risk Peach Arthropod Management Program was compared with adjacent conventionally managed peach orchards. In 1999, we found 2.3 times fewer L. lineolaris and stink bugs (Euschistus servus (Say), E. tristigmus (Say), Acrostemum hilare (Say) (Heteroptera: Pentatomidae) and 2.0 times less heteropteran damaged peaches in reduced-risk orchards when compared with conventionally managed orchards. In 2000, we observed 4.9 times fewer heteropteran insects in reduced-risk orchards but damage levels were not significantly different between the two programs. In both years, G. molesta mating disruption gave at least 4 mo of noninsecticidal control of this major pest. The reduced-risk program provided a level of pest control that was equal to or better than conventional peach pest management programs while using fewer organophosporus and carbamate insecticides.     

Jumping spiders (Salticidae) enhance the seed production of a plant with extrafloral nectaries

Many plants secrete nectar from extrafloral nectaries (EFNs), specialized structures that usually attract ants which can act as plant defenders. We examined the nectar-mediated interactions between Chamaecrista nictitans (Caesalpineaceae) and jumping spiders (Araneae, Salticidae) for 2 years in old fields in New Jersey, USA. Previous research suggests that spiders are entirely carnivorous, yet jumping spiders (Eris sp. and Metaphidippus sp.) on C. nictitans collected nectar in addition to feeding on herbivores, ants, bees, and other spiders. In a controlled-environment experiment, when given a choice between C. nictitans with or without active EFNs, foraging spiders spent 86% of their time on plants with nectar. C. nictitans with resident jumping spiders did set significantly more seed than plants with no spiders, indicating a beneficial effect from these predators. However, the presence of jumping spiders did not decrease numbers of Sennius cruentatus (Bruchidae), a specialist seed predator of C. nictitans. Jumping spiders may provide additional, unexpected defense to plants possessing EFNs. Plants with EFNs may therefore have beneficial interactions with other arthropod predators in addition to nectar-collecting ants. Received: 27 May 1998 / Accepted: 23 December 1998     

果实种类及发育阶段对梨小食心虫幼虫钻蛀率和蛹重的影响

【目的】明确梨小食心虫Grapholitha molesta在寄主果实上的钻蛀率和蛹重与寄主种类和果实发育阶段的关系,为其田间预测预报和综合防控提供技术依据。【方法】在室内条件下测定了接卵后72 h梨小食心虫初孵幼虫在不同发育阶段的3个种共6个品种水果［苹果Malus pumila (嘎啦苹果), 桃Amygdalus persica (大久保毛桃、丰白毛桃和霞光油桃), 梨Pyrus bretschneideri (砀山酥梨和玉露香梨)］果实上的钻蛀率以及在不同果实状态的4个水果品种(大久保毛桃、丰白毛桃、砀山酥梨和玉露香梨)果实上72 h的钻蛀率;比较了接卵后24 h和72 h初孵幼虫在不同发育阶段的3个苹果品种(嘎啦苹果、富士苹果和金冠苹果)果实上的钻蛀率;并测定了不同发育阶段的金冠苹果、富士苹果、嘎啦苹果、砀山酥梨和丰白毛桃上的梨小食心虫蛹重。【结果】接卵后72 h梨小食心虫初孵幼虫在6个不同水果品种果实上的钻蛀率从高到低依次为：霞光油桃＞嘎啦苹果＞砀山酥梨＞玉露香梨＞大久保毛桃＞丰白毛桃;除霞光油桃外,其他5个水果品种果实的发育阶段显著影响初孵幼虫钻蛀率。对于嘎啦苹果,接卵后72 h初孵幼虫在其幼果上的钻蛀率最高(73.69%),在其着色期果实上钻蛀率最低(32.51%);在大久保毛桃、丰白毛桃、砀山酥梨和玉露香梨上,接卵后72 h初孵幼虫的钻蛀率均随果实生长发育而增加。初孵幼虫在3 个苹果品种着色期和成熟期果实上的钻蛀率随处理时间的增加而显著下降,而在其幼果上变化不显著。寄主种类及其发育阶段也显著影响梨小食心虫蛹重,成熟毛桃和梨饲养的雌、雄蛹重显著高于未成熟果实饲养的蛹重,着色期苹果不利于蛹重的增加。【结论】果实种类及发育阶段显著影响梨小食心虫初孵幼虫钻蛀率和蛹重,取食成熟期梨和桃的梨小食心虫初孵幼虫钻蛀率和蛹重显著高于取食未成熟果实的个体。     

The influence of Lasius neoniger (Hymenoptera: Formicidae) on population growth and biomass of Aphis glycines (Hemiptera: Aphididae) in soybeans

In the United States, the soybean aphid, Aphis glycines Matsumura (Hemiptera: Aphididae), are often tended by the aphid-tending ant, Lasius neoniger Emery (Hymenoptera: Formicidae). In this study, we examined the effects of tending by ants on the density and biomass of soybean aphids on soybeans in Kentucky. We performed cage studies that limited access by ants and/or natural enemies. We used a split-plot design with natural enemy access as the main plot and ant attendance as the sub plot. We found that natural enemy access negatively affected aphid population density in the presence of tending ants, seen as a three- to four-fold increase in aphid density when natural enemies were excluded. In addition, we found that ant tending positively affected aphid biomass, both when natural enemies were given access to aphids or when natural enemies were excluded, seen by a two-fold increase in aphid biomass when ants tended aphids, both in the presence or absence of natural enemies. Biomass accumulation is seen as an important measurement for assessing aphid performance, and we argue that aphid-tending by ants can have an influence on natural field populations of soybean aphids. Agronomic practices that affect ant abundance in soybeans may influence the performance and hence pest outbreaks for this economically important pest.     

The ontogeny of plant indirect defenses

Plants frequently attract natural enemies of their herbivores, resulting in a reduction in tissue damage and often in enhanced plant fitness. While such indirect defenses can dramatically change as plants develop, only recently have ecologists begun to explore such changes and evaluate their role in mediating plant–herbivore–natural enemy interactions. Here we review the literature documenting ontogenetic patterns in plant rewards (i.e. extrafloral nectaries (EFNs), food bodies (FBs) and domatia) and volatile organic compounds (VOCs), and identify links between ontogenetic patterns in such traits and the attraction of natural enemies (ants). In the case of reward traits we concentrate in ant–plant studies, which are the most numerous. We report that all indirect defensive traits commonly vary with plant age but ontogenetic trajectories differ among them. Myrmecophytic species, which provide both food and shelter to their defenders, do not produce rewarding traits until a minimum size is reached. Then, a pronounced increase in the abundance of food rewards and domatia often occurs as plants develop, which explains the temporal succession or colony size increase of mutualistic ant species and, in some cases, leads to a reduction in herbivore damage and enhanced fitness as plants age. In contrast, ontogenetic patterns were less consistent in plant species that rely on VOC emissions to attract natural enemies or those that provide only food rewards (EFNs) but not nesting sites to their associated ants, showing an overall decline or lack of trend with plant development, respectively. Future research should focus on uncovering: (i) the costs and mechanisms underlying ontogenetic variation in indirect defenses, (ii) the relative importance of environmental and genetic components shaping these ontogenetic trajectories, and (iii) the consequences of these ontogenetic trajectories on plant fitness. Advances in this area will shed light on the context dependency of bottom-up and top-down controls of herbivore populations and on how natural selection actually shapes the ontogenetic trajectories of these traits.     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.