Biological control of invasive stink bugs: review of global state and future prospects

Invasive stink bugs (Hemiptera: Pentatomidae) are responsible for high economic losses to agriculture on a global scale. The most important species, dating from recent to old invasions, include Bagrada hilaris (Burmeister), Halyomorpha halys (Stål), Piezodorus guildinii (Westwood), Nezara viridula (L.), and Murgantia histrionica (Hahn). Bagrada hilaris, H. halys, and N. viridula are now almost globally distributed. Biological control of these pests faces a complex set of challenges that must be addressed to maintain pest populations below the economic injury level. Several case studies of classical and conservation biological control of invasive stink bugs are reported here. The most common parasitoids in their geographical area of origin are egg parasitoids (Hymenoptera: Scelionidae, Encyrtidae, and Eupelmidae). Additionally, native parasitoids of adult stink bugs (Diptera: Tachinidae) have in some cases adapted to the novel hosts in the invaded area and native predators are known to prey on the various instars. Improving the efficacy of biocontrol agents is possible through conservation biological control techniques and exploitation of their chemical ecology. Moreover, integration of biological control with other techniques, such as behavioural manipulation of adult stink bugs and plant resistance, may be a sustainable pest control method within organic farming and integrated pest management programs. However, additional field studies are needed to verify the efficacy of these novel methods and transfer them from research to application.     

A new forest pest in Europe: a review of Emerald ash borer (Agrilus planipennis) invasion

In this publication, we review the biology, ecology, invasion history, impacts and management options of Emerald ash borer (EAB) Agrilus plannipennis, with a particular focus on its invasion in Europe. Agrilus planipennis (EAB) is a wood‐boring beetle native to East Asia. Having caused massive damages on ash species in North America in the last decades, it was first recorded in Europe in 2003 in Russia (Moscow). All ash (Fraxinus) species native to Europe and North America are known to be susceptible to EAB attacks, which cause high tree mortality even among formerly healthy trees. Recorded expansion rates are between 2.5 and 80 km/year in North America and between 13 and 41 km/year in European Russia. Given current expansion rates, EAB is expected to reach Central Europe within 15–20 years. A combination of mechanical, biological and chemical control and phytosanitary measures may reduce its impact, which nevertheless most likely will be substantial. There is an urgent need to identify native enemies in Europe, to test suitable biocontrol agents and to develop early detection and management measures. Although it is obvious that EAB will become a major pest in Europe, early and dedicated response will likely be able to reduce the level of ash mortality, and thus improve the opportunity for long‐term survival of ash as an important component in European forests.     

海洋外来物种入侵生态学研究

海洋外来物种入侵已成为最为严重的全球性环境问题之一。海洋生态系统类型多样、环境复杂,其生物入侵的监测、控制与管理难度相对较大。我国对陆地外来生物的入侵已开展了较为深入的研究,但对于海洋外来生物的入侵研究仍处于起步阶段,对其入侵监测、入侵机制、入侵危害的程度以及防治等问题缺乏基础数据。本文在分析国内外海洋外来生物入侵现状的基础上,概述其入侵生态学研究形势及相关成果,包括海洋外来物种的入侵途径、入侵过程、入侵生态效应以及全球变化对入侵的影响等。海洋外来生物的入侵可能对海洋生态系统造成直接或间接的影响,如种间竞争破坏生态环境、与土著种杂交造成遗传污染、病原生物及有毒藻类导致海洋生态灾害加剧等。此外,从政策和法规、入侵风险评估、监测和公共宣传教育、生物信息系统和有效管理机制等方面提出对我国海洋外来物种入侵的防治策略。本研究为我国海洋外来物种的进一步研究提供了参考。     

Ancient and modern colonization of North America by hemlock woolly adelgid,Adelges tsugae (Hemiptera: Adelgidae), an invasive insect from East Asia

Hemlock woolly adelgid, Adelges tsugae, is an invasive pest of hemlock trees (Tsuga) in eastern North America. We used 14 microsatellites and mitochondrial COI sequences to assess its worldwide genetic structure and reconstruct its colonization history. The resulting information about its life cycle, biogeography and host specialization could help predict invasion by insect herbivores. We identified eight endemic lineages of hemlock adelgids in central China, western China, Ulleung Island (South Korea), western North America, and two each in Taiwan and Japan, with the Japanese lineages specializing on different Tsuga species. Adelgid life cycles varied at local and continental scales with different sexual, obligately asexual and facultatively asexual lineages. Adelgids in western North America exhibited very high microsatellite heterozygosity, which suggests ancient asexuality. The earliest lineages diverged in Asia during Pleistocene glacial periods, as estimated using approximate Bayesian computation. Colonization of western North America was estimated to have occurred prior to the last glacial period by adelgids directly ancestral to those in southern Japan, perhaps carried by birds. The modern invasion from southern Japan to eastern North America caused an extreme genetic bottleneck with just two closely related clones detected throughout the introduced range. Both colonization events to North America involved host shifts to unrelated hemlock species. These results suggest that genetic diversity, host specialization and host phylogeny are not predictive of adelgid invasion. Monitoring non‐native sentinel host trees and focusing on invasion pathways might be more effective methods of preventing invasion than making predictions using species traits or evolutionary history.     

Landscape composition influences patterns of native and exotic lady beetle abundance

Aim Coccinellid beetles are important predators that contribute to pest suppression in agricultural landscapes. Since the introduction of the exotic coccinellids Coccinella septempunctata L. and Harmonia axyridis Pallas into the USA, several studies have reported a decline of native Coccinellidae in agroecosystems. We aimed to investigate the influence of landscape composition on native and exotic coccinellid abundance within soybean fields. Location Iowa, Michigan, Minnesota and Wisconsin. Methods As part of a 2‐year study (2005–06) on the biological control of the soybean aphid, Aphis glycines Matsumura, we examined coccinellid communities in 33 soybean fields using yellow sticky card traps. Landscape heterogeneity and composition were measured at multiple spatial scales ranging 1–3.5 km from focal soybean fields where coccinellid sampling took place. Results Exotic species made up 90% of the total coccinellid community in Michigan soybean fields followed by Wisconsin (84%), Minnesota (66%) and Iowa (57%). Harmonia axyridis was the dominant exotic coccinellid in all states comprising 45–62% of the total coccinellid community, followed by C. septempunctata (13–30%). Two additional exotic species, Hippodamia variegata (Goeze) and Propylea quatuordecimpunctata (L.) were also found in the region. Overall, the most abundant native coccinellid was Hippodamia convergens Guerin‐Meneville; however, its abundance varied across the region, comprising 0% (Michigan) to 28% (Iowa) of the total coccinellid community. Landscape structure significantly influenced the composition of coccinellid communities in soybean agroecosystems. We found that native coccinellids were most abundant in low‐diversity landscapes with an abundance of grassland habitat while exotic coccinellids were associated with the abundance of forested habitats. Main conclusion We propose that grassland dominated landscapes with low structural diversity and low amounts of forested habitat may be resistant to exotic coccinellid build‐up, particularly H. axyridis and therefore represent landscape‐scale refuges for native coccinellid biodiversity.     

Characterization of microsatellite loci in the European green crab (Carcinus maenas)

Carcinus maenas (Decapoda: Portunidae) has proven a highly successful invasive marine species whose potential economic and ecological impacts are of great concern worldwide. Here, we characterize 14 polymorphic microsatellite loci in C. maenas and its sister species Carcinus aestuarii. These markers will prove useful for fine‐scale genetic analyses of native and introduced populations, for assessment of the sources and routes of invasion and for evaluation of post‐invasion population dynamics.     

Diversity of spiders after spring sowing – influence of farming system and habitat type

Spiders contribute considerably to diversity in agroecosystems and are important components of natural pest control. Farming system and adjacent habitats may influence spider diversity. In this study, diversity of the spider families Lycosidae and Linyphiidae was studied after spring sowing until the time when a common pest (Rhopalosiphum padi) colonizes cereal fields. The spiders were collected with pitfall traps at eight organically or conventionally managed farms around Uppsala, Sweden, in three different habitats at each site: field margin, crop field and the edge between the two. The effects of farming system and habitat type on diversity of lycosids and linyphiids were considered using three different measures (activity density, species richness and composition). The most dominant species of each spider family, Pardosa agrestis (Lycosidae) and Oedothorax apicatus (Linyphiidae), had higher activity density at organic sites, and farming systems also contained different species compositions of both lycosid and linyphiid spiders. Also, linyphiid species richness was higher on conventional sites and linyphiid species composition was influenced by habitat type, in contrast with lycosids. Activity density and species richness of lycosid spiders were, on the other hand, more associated with field margins than linyphiid spiders.     

Is salinity an obstacle for biological invasions?

Invasions of freshwater habitats by marine and brackish species have become more frequent in recent years with many of those species originating from the Ponto‐Caspian region. Populations of Ponto‐Caspian species have successfully established in the North and Baltic Seas and their adjoining rivers, as well as in the Great Lakes–St. Lawrence River region. To determine if Ponto‐Caspian taxa more readily acclimatize to and colonize diverse salinity habitats than taxa from other regions, we conducted laboratory experiments on 22 populations of eight gammarid species native to the Ponto‐Caspian, Northern European and Great Lakes–St. Lawrence River regions. In addition, we conducted a literature search to survey salinity ranges of these species worldwide. Finally, to explore evolutionary relationships among examined species and their populations, we sequenced the mitochondrial cytochrome c oxidase subunit I gene (COI) from individuals used for our experiments. Our study revealed that all tested populations tolerate wide ranges of salinity, however, different patterns arose among species from different regions. Ponto‐Caspian taxa showed lower mortality in fresh water, while Northern European taxa showed lower mortality in fully marine conditions. Genetic analyses showed evolutionary divergence among species from different regions. Due to the geological history of the two regions, as well as high tolerance of Ponto‐Caspian species to fresh water, whereas Northern European species are more tolerant of fully marine conditions, we suggest that species originating from the Ponto‐Caspian and Northern European regions may be adapted to freshwater and marine environments, respectively. Consequently, the perception that Ponto‐Caspian species are more successful colonizers might be biased by the fact that areas with highest introduction frequency of NIS (i.e., shipping ports) are environmentally variable habitats which often include freshwater conditions that cannot be tolerated by euryhaline taxa of marine origin.     

Evaluation of the sea anemone Anthothoe albocincta as an augmentative biocontrol agent for biofouling on artificial structures

Augmentative biocontrol, defined as the use of indigenous natural enemies to control pest populations, has not been explored extensively in marine systems. This study tested the potential of the anemone Anthothoe albocincta as a biocontrol agent for biofouling on submerged artificial structures. Biofouling biomass was negatively related to anemone cover. Treatments with high anemone cover (>35%) led to significant changes in biofouling assemblages compared to controls. Taxa that contributed to these changes differed among sites, but included reductions in cover of problematic fouling organisms, such as solitary ascidians and bryozoans. In laboratory trials, A. albocincta substantially prevented the settlement of larvae of the bryozoan Bugula neritina when exposed to three levels of larval dose, suggesting predation as an important biocontrol mechanism, in addition to space pre-emption. This study demonstrated that augmentative biocontrol using anemones has the potential to reduce biofouling on marine artificial structures, although considerable further work is required to refine this tool before its application.     

外来入侵杂草的生物防治及生防因子对本地非目标种的影响

随着生物入侵所引起的生态及经济问题日益严重,对有害入侵生物的防治问题也备受人们关注。生物防治因具有持续、高效、安全等优点,已成为防治有害入侵生物的重要方法。传统生防是防治有害入侵杂草的一种重要方法。在简单介绍生物防治的基础上,重点阐述了传统生物防治的理论基础——天敌逃逸假说,生防因子对外来人侵种的影响及其对本地非目标种的直接和间接效应,并针对这些问题,对我国开展生物防治工作提出几点建议。     

Marine trophic niche use and life history diversity among Arctic charr Salvelinus alpinus in southwestern Greenland

Life history strategies and potential marine niche use of Arctic charr Salvelinus alpinus (n = 237, 84–652 mm, total body length, L_T) were determined during the ice-free season (2012) at three different watercourses in south-western Greenland. All Arctic charr were collected from freshwater habitats. Based on stable isotopes of δ³⁴S, the Arctic charr were categorized as either marine- or freshwater-dependent feeders. The use of time-integrated trophic tracers (stable isotopes of δ¹³C, δ¹⁵N, δ³⁴S) suggested that several trophic groups of Arctic charr operate alongside within each fjord system. The groups suggested were one group that specialized in the marine habitat, in addition to two freshwater resident morphs (small-sized resident and/or large-growing cannibalistic individuals). Stomach contents consisted entirely of freshwater and terrestrial prey (i.e., insects), indicating that marine-dependent feeders also fed in freshwater habitats after return from their marine migration. Growth and maturity patterns further supported variable life history strategies within each watercourse. The life history strategy patterns and marine trophic niche use were consistent across the watercourses along several hundred kilometres of coastline. This study represents the first ecological baseline for partially anadromous populations of Greenland Arctic charr.     

Marine management affects the invasion success of a non‐native species in a temperate reef system in California,USA

Despite promises that ‘healthy’ marine systems show increased resilience, the effects of ecosystem management strategies on invasion success in marine systems is still unclear. We show that resistance to the invasive alga, Sargassum horneri, in a temperate reef system occurs through alternate mechanisms in different ecosystem states. In an old marine protected area (MPA), invasion of S. horneri was suppressed, likely due to competitive pressure from native algae, resulting from protection of urchin predators. In a nearby fished urchin barren, invasion of S. horneri was also suppressed, due to herbivory by urchins whose predators are fished. Within newer MPAs with intermediate levels of interacting species, S. horneri was abundant. Here, neither competition from native algae nor herbivory was sufficient to prevent invasion. We confirm that invasion in marine systems is complex and show that multiple mechanisms in single systems must be considered when investigating biotic resistance hypotheses.     

Life history of peracarid species in South‐western Atlantic: Comparison of population traits between native and exotic species

Life‐history traits of exotic species are important to understand the process involved in their settlement and their potential impact on native biodiversity. In this context, the seasonal density, the population structure and the reproductive patterns of exotic and native peracarid species of two natural marine environments of Southwestern Atlantic were studied in order to determine the traits that favour the invasion success of exotic species. Five samples, consisted of algal patches (0.20 × 0.20 m quadrants), were collected seasonally from 2016 to 2017 in two intertidal environments (La Estafeta and Cerro Avanzado). Both environments presented high richness of cryptogenic and exotic species (Tanais dulongii, Monocorophium insidiosum, Ampithoe valida, Melita palmata and Jassa marmorata), and only two native species were recorded (Apohyale grandicornis and Exosphaeroma lanceolatum). The comparison of life‐history traits suggested that the distribution, dominance and the highest densities of some exotic species are closely related to their continuous reproductive and recruitment periods, their capability to adapt their life‐history strategies to different environmental conditions and to a more efficient distribution of resources during reproduction; however, in native species, only A. grandicornis registered similar life‐history traits than exotic populations, suggesting that their distribution could be limited by a latitudinal gradient. We expect that these results provide essential information to understand the invasion pattern of exotic species and their potential impact on native biodiversity in Southwestern Atlantic.     

Effects of simulated herbivory and resource availability on the invasive plant, Alternanthera philoxeroides in different habitats

In biological control programs, the insect natural enemy’s ability to suppress the plant invader may be affected by abiotic factors, such as resource availability, that can influence plant growth and reproduction. Understanding plant tolerance to herbivory under different environmental conditions will help to improve biocontrol efficacy. The invasive alligator weed (Alternanthera philoxeroides) has been successfully controlled by natural enemies in many aquatic habitats but not in terrestrial environments worldwide. This study examined the effects of different levels of simulated leaf herbivory on the growth of alligator weed at two levels of fertilization and three levels of soil moisture (aquatic, semi-aquatic, and terrestrial habitats). Increasing levels of simulated (manual) defoliation generally caused decreases in total biomass in all habitats. However, the plant appeared to respond differently to high levels of herbivory in the three habitats. Terrestrial plants showed the highest below–above ground mass ratio (R/S), indicating the plant is more tolerant to herbivory in terrestrial habitats than in aquatic habitats. The unfertilized treatment exhibited greater tolerance than the fertilized treatment in the terrestrial habitat at the first stage of this experiment (day 15), but fertilizer appears not to have influenced tolerance at the middle and last stages of the experiment. No such difference was found in semi-aquatic and aquatic habitats. These findings suggest that plant tolerance is affected by habitats and soil nutrients and this relationship could influence the biological control outcome. Plant compensatory response to herbivory under different environmental conditions should, therefore, be carefully considered when planning to use biological control in management programs against invasive plants.     

Earthworm invasions in the tropics

The effects and implications of invasive species in belowground terrestrial ecosystems are not well known in comparison with above-ground terrestrial and marine environments. The study of earthworm invasions in the tropics is limited by a lack of taxonomic knowledge and the potential for loss of species in native habitats due to anthropogenic land use change. Alteration of land use plays a major role in determining the abundance and community structure of earthworms and the establishment of exotic earthworms in areas previously inhabited by worms. Once an exotic species has become established into a new place, site and species characteristics seem to be key factors determining their spread. We reviewed the literature on the distribution and effects of exotic earthworms to understand the interactions of earthworm invasion and land use history in the tropics. Patterns in the abundance, effects and mechanisms of earthworm invasions on ecosystem processes in the tropics are elucidated using Pontoscolex corethrurus as a case study.     

A native predator utilising the invasive brown marmorated stink bug,Halyomorpha halys (Hemiptera: Pentatomidae) as a food source

The nest provisions of a native predator species Bicyrtes quadrifasciata (Say) (Hymenoptera: Crabronidae) were surveyed and examined for the presence of nymphs of Halyomorpha halys, which is an invasive pest of many economically important agricultural crops in the U.S.A. We found 96% of the nest provisions of B. quadrifasciata were H. halys indicating the potential of B. quadrifasciata in biocontrol of this pest. Potential of B. quadrifasciata in regulating population dynamics of H. halys is discussed.     

入侵植物马缨丹研究进展

马缨丹原产于热带美洲,现已扩散至世界热带和亚热带地区,并严重威胁入侵地本地植物的生长。马缨丹因具有观赏价值而被我国大量引进,但由于疏于管理,发展成为入侵杂草,对我国农业、畜牧业及生态环境造成严重危害。目前对马缨丹的入侵机制还没有全面系统的认识。本文从马缨丹的生物学特性、入侵机制、生态学效应、防治与应用等方面进行综述,总结其研究进展,以期为马缨丹的防治工作提供依据。研究结果显示:马缨丹成功入侵的关键因素源于其独特的生物学性征;对农林业造成的危害的原因主要为它的化感作用;马缨丹的防治方法主要包括物理、化学和生物防治;马缨丹在防虫除虫、污染修复、药用价值等方面有所应用。此外,分析当前研究中的不足后发现,今后应加强马缨丹在自然环境中的适应机制、应用潜力、防治方法等的研究。     

Prey consumption and development of the indigenous lacewing Chrysoperla externa feeding on two exotic Eucalyptus pests

ABSTRACT

The green lacewing Chrysoperla externa is a widespread species in the Neotropical region that occurs in different habitats. Its presence in Eucalyptus plantations infested with Glycaspis brimblecombei (Hemiptera: Aphalaridae) and Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae) suggests that this lacewing might feed on one or both exotic pest species. In order to evaluate C. externa as a potential biocontrol agent of the eucalyptus pests, the prey consumption, development, survival and reproduction of the predator were evaluated under laboratory conditions. C. externa larvae consumed nymphs of both pest species. Developmental time and reproduction parameters of C. externa fed G. brimblecombei were similar to those obtained with the factitious prey Sitotroga cerealella. When fed on T. peregrinus, C. externa showed a delay in its developmental time and the emerged adults were malformed. The results of this study suggest that the green lacewing is a good candidate to be used in augmentative or conservative biological control programmes against G. brimblecombei. Further research is necessary to analyse the potential of this predator as a biocontrol agent under field conditions.     

Biology of Polypedilum n. sp. (Diptera: Chironomidae), a promising candidate agent for the biological control of the aquatic weed Lagarosiphon major (Hydrocharitaceae) in Ireland

Lagarosiphon major (Ridl.) Moss ex Wager (Hydrocharitaceae), an aquatic macrophyte native to Southern Africa that has become invasive in several countries worldwide, is a potential target for biological control. Biology studies were conducted on Polypedilum (Pentapedilum) n. sp. near reei Oyewo & Sæther (Diptera: Chironomidae), a midge whose larvae were discovered mining the plant's shoot tips in its native range. Field surveys indicated that the midge occurred only at a small number of sites but attained high densities (up to 370 shoots damaged/m²) that prevented further growth from the shoot tips. A population of the midge was imported into quarantine in Ireland to evaluate its potential as a candidate biological control agent. The adult stage is terrestrial and short-lived (4–5 d), with females depositing one–two egg packets into the water bodies. First-instar larvae fed externally on the stems and leaflets. Later instars fed on the apical meristems and burrowed into the shoot tips, with resultant damage stunting the apical growth. Larvae moved readily between shoots to complete their development and pupated within the tunnels excavated by the late instar larvae. Developmental time to adulthood ranged from 31 to 49 days at 20.7°C and a 15 L:9-D cycle. This is the first time that a chironomid has been imported and successfully cultured for consideration as a classical biological control agent. Several aspects of the midge's biology suggest that host specificity testing is warranted to determine its potential as a biocontrol agent of L. major.     

Impacts of biological control and invasive species on a non-target native Hawaiian insect

The potential for classical biological control to cause unintended harm to native species was evaluated in the case of the endemic Hawaiian koa bug, Coleotichus blackburniae White (Hemiptera: Scutelleridae), and parasitoids introduced to Hawaii for control of an agricultural pest, the southern green stink bug, Nezara viridula (L.) (Hemiptera: Pentatomidae). Parasitism of C. blackburniae eggs, nymphs and adults by biocontrol agents was quantified across a wide range of habitats and compared to other sources of mortality. Egg mortality due to the biocontrol agent Trissolcus basalis Wollaston (Hymenoptera: Scelionidae) was low (maximum 26%) and confined to elevations below 500 m on a single host plant. Predation, mainly by alien spiders and ants, was the greatest source of egg mortality (maximum 87%). Parasitism of adult C. blackburniae by the biocontrol agent Trichopoda pilipes (F.) (Diptera: Tachinidae) was near zero at 21 of 24 sites surveyed. Three sites with high bug density had higher levels of T. pilipes parasitism, reaching maxima of 70% among adult female bugs, 100% among males and 50% among fifth instars. Male-biased parasitism indicated that T. pilipes is adapted to using male aggregation pheromone for finding C. blackburniae hosts. The relative impacts of biocontrol agents and other sources of mortality were compared using life tables. Invasive species, particularly generalist egg predators, had the greatest impacts on C. blackburniae populations. Effects of intentionally introduced parasitoids were relatively minor, although the tachinid T. pilipes showed potential for large impacts at individual sites. In retrospect, non-target attacks by biological control agents on C. blackburniae were predictable, but the environmental range and magnitude of impacts would have been difficult to foresee.