Symbiont‐mediated chemical defense in the invasive ladybird Harmonia axyridis

The volatile alkylpyrazines methyl‐ and methoxypyrazines (MPs) present in the reflex bleeds of coccinellid beetles such as the harlequin ladybird beetle Harmonia axyridis are important semiochemicals that function in antipredatory defense behavior. Pyrazines have also been coadapted from a primarily defensive role into pheromones that function in intraspecific communication, attraction, and aggregation behavior. However, the biosynthesis of MPs in ladybird beetles is poorly understood. Here, we tested the hypothesis that MPs could be produced by microbial symbionts in H. axyridis, which generates four different MPs. The evaluation of tissue‐specific MP production showed that MP concentrations were highest in the gut tissue and hemolymph of the beetles rather than the fat body tissue as the presumed site of MP biosynthesis. Furthermore, manipulation of gut microbiota by antibiotic‐containing diets resulted in a lower MP content in adult beetles. The analysis of the bacterial community of the digestive tract revealed the presence of bacteria of the genera Serratia and Lactococcus which are reportedly able to produce MPs. In line with the known diet‐dependent production of MP in H. axyridis, we determined that the presence or relative abundance of some of the potential MP producers (Enterococcus and Staphylococcus) is also diet‐dependent. We hypothesize a potential role of the microbiota in MP production in H. axyridis as a possible example for outsourcing the synthesis of ecologically important semiochemicals to its gut bacteria.     

Sublethal effect of beta‐cypermethrin on development and fertility of the Asian multicoloured ladybird beetle Harmonia axyridis

The Asian multicoloured ladybird beetle, Harmonia axyridis, is utilized as a major natural enemy of aphids in the field, greenhouses and orchards. However, it has been looked as invasive predator distributing in worldwide. To refine integrated pest management (IPM) against aphids, it is important to evaluate the effects of insecticides on physiology and behaviour of the high adapted predators. Beta‐cypermethrin, a broad‐spectrum insecticide, not only kills aphids at lethal concentrations but also affects natural enemy of aphids. In our study, the age‐stage, two‐sex life table was used to evaluating sublethal effects of beta‐cypermethrin on the predatory ladybird beetle H. axyridis. In the parent generation, the pre‐oviposition period of H. axyridis was significantly shortened (8.93 days) after exposure to LC₅ beta‐cypermethrin (5% lethal concentration) as compared with control (10.06 days). However, the oviposition period was significantly longer (46.17 days instead of 43.90 days), and fecundity (eggs per female) was significantly increased by 49.64% when compared with control. In the F₁ generation, the length of the juvenile stage was not affected, but the oviposition period increased significantly (38.19 days compared to 31.39 days in the control). This positive effect was translated to the fecundity that increased significantly by 62.27% as compared with control. According to the life‐table analysis, the intrinsic rate of increase (r_m) was significantly higher in treatment (0.140 per day) than that in the control (0.123 per day). In addition, the net reproductive rate (R₀) increased significantly by 91.53%. These results would be useful in assessing the overall effects of beta‐cypermethrin on H. axyridis and even for discussing the ecological mechanism of the unexpected extension of H. axyridis during IPM programme.     

Weak photoperiodic response facilitates the biological invasion of the harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae)

Photoperiodic regulation of reproductive diapause in two invasive and two native populations of Harmonia axyridis and in one native population of Harmonia yedoensis was investigated in laboratory at 20°C, five photoperiods (day length of 10, 12, 14, 16 and 18 h) and two diets: (i) eggs of the Angoumois grain moth Sitotroga cerealella and (ii) the green peach aphid, Myzus persicae. Laboratory strains originated from native populations of H. axyridis from Irkutsk province of Siberia and H. yedoensis from South Korea showed a strong photoperiodic response: under short photoperiods (10–14 h and 10–12 h for H. axyridis and H. yedoensis, correspondingly), all females which fed on eggs and most of those fed on aphids did not start to lay eggs during 40 days after emergence, while under long photoperiods, all females fed on aphids and most of those fed on eggs oviposited. The photoperiodic response of H. axyridis from South Korea was less strong: on the both diets, the range of the photoperiodic response (the difference in the proportion of ovipositing females between the treatments with long and short days) was ca 40%. In the European (Czech Republic) and in the Caucasian (Sochi region, Russia) invasive populations of H. axyridis, the photoperiodic response was very weak: the proportion of females that started oviposition (when fed on aphids) or at least reproductive maturation (when fed on eggs) during 40 days after emergence was close to 100%, independently of the photoperiodic conditions. Obviously, instead of a rapid micro‐evolutionary adaptation of the critical day length to a new climate, the invasive populations of the harlequin ladybird decrease their dependence on photoperiod and thus the weak photoperiodic response of SE Asian population of H. axyridis can be considered as a pre‐adaptation further developed during the invasion.     

A one‐step,single tube,duplex PCR to detect predation by native predators on invasive Bemisia tabaci MEAM1 and Frankliniella occidentalis

Bemisia tabaci (Gennadius) MEAM1 (Hemiptera: Aleyrodidae) and Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), two important invasive species, are serious agricultural pests. In this study, a one‐step, single tube, duplex polymerase chain reaction (PCR) procedure was developed to allow rapid, specific, and sensitive identification of B. tabaci MEAM1 and F. occidentalis in predator guts. The system and conditions used for the duplex PCR were optimized. The species specificity of the duplex PCR determined by comparison against non‐targets that might interact with B. tabaci MEAM1 and F. occidentalis showed that oligonucleotide primers amplified nuclear gene target sequences present only in B. tabaci MEAM1 or F. occidentalis. The limits of detection were 9.53 ng μl^?1 for B. tabaci MEAM1 and 8.94 ng μl^?1 for F. occidentalis. Within a field cage study, in which predators Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) and Orius sauteri (Poppius) (Hemiptera: Anthocoridae) were allowed to feed on B. tabaci MEAM1 and F. occidentalis for 10 h, the B. tabaci MEAM1 DNA was detectable in 100% of H. axyridis and O. sauteri, and F. occidentalis DNA was detectable in 80% of H. axyridis and 90% of O. sauteri; this implicated that B. tabaci MEAM1 and F. occidentalis remains could be detected in native predator guts simultaneously. The accuracy and reliability of the assay suggested strongly that the duplex PCR optimized for B. tabaci MEAM1 and F. occidentalis is sensitive and specific for both invasive insects and is therefore useful in early diagnosis and monitoring of B. tabaci MEAM1 and F. occidentalis infections, and can be used to identify domestic predator species and food web relationships.     

A population genetic signature of human releases in an invasive ladybeetle

Biological invasions have been accelerated by a variety of human activities. Propagule pressure, the number of introduced individuals and independent introductions, is probably to be influenced by these human activities and may be an important factor for successful range expansion in new environments. We tested whether the current distribution of the predatory ladybeetle Coccinella septempunctata in the introduced range (USA) is the result of multiple historical human introductions or natural range expansion from the first established populations in the USA. To test this hypothesis, we compared historical records of propagule size, propagule number, specific introduction locations and the date of each introduction, with estimates of genetic variation in mitochondrial DNA (cytochrome oxidase I). Our results indicated that genetic diversity in the introduced range was positively correlated with historical records of propagule size and number and negatively correlated with distance to nearest introduction point, suggesting that multiple human releases were successful. Higher genetic diversity in populations found near introduction points suggest that initial founder effects were limited, but lower genetic diversity found farther from introduction points is probably the result of serial founder effects during secondary range expansion. These results suggest that the current distribution of C. septempunctata in the introduced range is the result of a combination of human releases and short‐range expansion from multiple established populations in the introduced range.     

The effect of past natural enemy activity on host‐plant preference of two aphid species

The selection of a host of high nutritional quality is of great importance to the development of offspring of larvipositing aphids, as is the avoidance of natural enemies. Little is known, however, about their ability to select host plants based on these factors. This article tests the preference of aphids Sitobion avenae (Fabricius) and Rhopalosiphum padi (L.) (both Hemiptera: Aphididae) for different winter wheat cultivars, Triticum aestivum (L.) (Poaceae), and their ability to detect and avoid predators in sacrifice of their most preferred host. In both species a preference was observed for nutritionally superior hosts. The preference of both species then exhibited a change towards a nutritionally inferior host after infestations of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), that had been consuming conspecific aphids. This investigation opens the door to the interesting prospect of the ability of aphids to make complex decisions regarding a compromise between high‐quality nutrition and avoidance of predation.     

Isoalantolactone restores the sensitivity of gram‐negative Enterobacteriaceae carrying MCR‐1 to carbapenems

Polymyxin B has been re‐applied to the clinic as the final choice for the treatment of multidrug‐resistant gram‐negative pathogenic infections, but the use of polymyxin B has been re‐assessed because of the emergence and spread of the plasmid‐mediated mcr‐1 gene. The purpose of this study was to search for an MCR inhibitor synergistically acting with polymyxin to treat the infection caused by this pathogen. In this study, we used the broth microdilution checkerboard method to evaluate the synergistic effect of isoalantolactone (IAL) and polymyxin B on mcr‐1‐positive Enterobacteriaceae. Growth curve analysis, time‐killing assays and a combined disc test were used to further verify the efficacy of the combined drug. Colonization of the thigh muscle in mice, survival experiments and lung tissue section observations was used to determine the effect of synergy in vivo after Klebsiella pneumoniae and Escherichia coli infection. We screened a natural compound, IAL, which can enhance the sensitivity of polymyxin B to mcr‐1‐positive Enterobacteriaceae. The results showed that the combined use of polymyxin B and IAL has a synergistic effect on mcr‐1‐positive Enterobacteriaceae, such as K pneumoniae and E coli, not only in vitro but also in vivo. Our results indicate that IAL is a natural compound with broad application prospects that can prolong the service life of polymyxin B and make outstanding contributions to the treatment of gram‐negative Enterobacteriaceae infections resistant to polymyxin B.     

Efficient distinction of invasive aquatic plant species from non‐invasive related species using DNA barcoding

Biological invasions are regarded as threats to global biodiversity. Among invasive aliens, a number of plant species belonging to the genera Myriophyllum, Ludwigia and Cabomba, and to the Hydrocharitaceae family pose a particular ecological threat to water bodies. Therefore, one would try to prevent them from entering a country. However, many related species are commercially traded, and distinguishing invasive from non‐invasive species based on morphology alone is often difficult for plants in a vegetative stage. In this regard, DNA barcoding could become a good alternative. In this study, 242 samples belonging to 26 species from 10 genera of aquatic plants were assessed using the chloroplast loci trnH‐psbA, matK and rbcL. Despite testing a large number of primer sets and several PCR protocols, the matK locus could not be amplified or sequenced reliably and therefore was left out of the analysis. Using the other two loci, eight invasive species could be distinguished from their respective related species, a ninth one failed to produce sequences of sufficient quality. Based on the criteria of universal application, high sequence divergence and level of species discrimination, the trnH‐psbA noncoding spacer was the best performing barcode in the aquatic plant species studied. Thus, DNA barcoding may be helpful with enforcing a ban on trade of such invasive species, such as is already in place in the Netherlands. This will become even more so once DNA barcoding would be turned into machinery routinely operable by a nonspecialist in botany and molecular genetics.     

Responses of the soil fungal communities to the co‐invasion of two invasive species with different cover classes

• Soil fungal communities play an important role in the successful invasion of non‐native species. It is common for two or more invasive plant species to co‐occur in invaded ecosystems.
• This study aimed to determine the effects of co‐invasion of two invasive species (Erigeron annuus and Solidago canadensis) with different cover classes on soil fungal communities using high‐throughput sequencing.
• Invasion of E. annuus and/or S. canadensis had positive effects on the sequence number, operational taxonomic unit (OTU) richness, Shannon diversity, abundance‐based cover estimator (ACE index) and Chao1 index of soil fungal communities, but negative effects on the Simpson index. Thus, invasion of E. annuus and/or S. canadensis could increase diversity and richness of soil fungal communities but decrease dominance of some members of these communities, in part to facilitate plant further invasion, because high soil microbial diversity could increase soil functions and plant nutrient acquisition. Some soil fungal species grow well, whereas others tend to extinction after non‐native plant invasion with increasing invasion degree and presumably time. The sequence number, OTU richness, Shannon diversity, ACE index and Chao1 index of soil fungal communities were higher under co‐invasion of E. annuus and S. canadensis than under independent invasion of either individual species.
• The co‐invasion of the two invasive species had a positive synergistic effect on diversity and abundance of soil fungal communities, partly to build a soil microenvironment to enhance competitiveness of the invaders. The changed diversity and community under co‐invasion could modify resource availability and niche differentiation within the soil fungal communities, mediated by differences in leaf litter quality and quantity, which can support different fungal/microbial species in the soil.

     

Impact of plant architecture and extraguild prey density on intraguild predation in an agroecosystem

Several models and experimental studies conducted in confined environments have shown that intraguild predation (IGP) can modulate population abundances and structure communities. A number of ecological and abiotic factors determine the nature and frequency of IGP. This study examined the effect of plant architecture and extraguild prey density, and their interactions, on the occurrence of IGP between two species of ladybird, Harmonia axyridis (Pallas) and Propylea quatuordecimpunctata L. (both Coleoptera: Coccinellidae). Theoretical concepts predict that IGP levels would increase with a decrease of both extraguild prey density and plant structural complexity. We conducted a factorial experiment in an open soybean field into which coccinellid larvae were introduced in experimental plots for a period of 5 days. We tested two levels of soybean aphid [Aphis glycines Matsumara (Hemiptera: Aphididae)] density, low and high (100 and 1 000 aphids per plot, respectively), and two levels of plant complexity, low (by removing half of the branches from the soybean plants) and high (by leaving plants intact). We used species‐specific molecular markers to detect the presence of P. quatuordecimpunctata in the digestive tract of H. axyridis. Molecular gut‐content analysis of H. axyridis revealed that rates of IGP were higher (20%) at low aphid density than at high aphid density (<6%). Decreased plant complexity did not impact the frequency of IGP. In accordance with existing literature, this study demonstrates that IGP is amplified at low extraguild prey density. We conclude that considering environmental factors, such as extraguild prey density, is crucial to improve our ability to predict the impact of intraguild predation on community structure and, from an applied perspective, biological control.     

Multi‐trophic impacts of an invasive aquatic plant

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Sex‐specific responses of Asian citrus psyllid to volatiles of conspecific and host‐plant origin

Diaphorina citri Kuwayama (Hemiptera: Psyllidae) is the primary vector of Candidatus Liberibacter spp. bacteria that cause citrus greening, a disease of worldwide importance. Olfactometry was employed to test responses of D. citri to odours from intact citrus plants (Mexican lime, Citrus aurantifolia, sour orange, Citrus aurantium, Marsh grapefruit, Citrus paradisi and Valencia orange, Citrus sinensis), citrus plants previously infested with D. citri, and odours of conspecifics including nymphs, adult insects of same and opposite sex, and their products (honeydew), both alone and in combination. In contrast to other studies, psyllids of both sexes were attracted to volatiles of undamaged Mexican lime leaves, whereas undamaged grapefruit attracted only females, and leaves of Valencia and sour orange did not attract either sex. All four plant species attracted female psyllids when previously infested, but only Mexican lime and sour orange‐attracted males. Thus, Citrus species appear to vary in the production of both constituitive and induced volatiles that attract adult psyllids. Volatiles emitted by nymphs did not attract either sex, but psyllid honeydew was attractive to males, likely due to female pheromone residues. Males oriented to the odour of females, whereas the reverse was not true, and neither males nor females oriented to same‐sex volatiles. The addition of conspecific cues (adults, nymphs or honeydew) did not increase female attraction to previously infested leaves, but male response was increased by the presence of adults and honeydew, regardless of plant species. Thus, female psyllids appear to orient more strongly to volatiles of plant origin, whereas males respond more strongly to cues emanating from females and conspecific excretions. These results suggest that female psyllids drive the initial colonization of host plants, whereas males orient to females and infested plants. Identification of the specific volatiles involved may permit their use in monitoring and management of this pest.     

An invasive tree facilitates the persistence of native rodents on an over‐grazed floodplain in tropical Australia

In an ecosystem under simultaneous threat from multiple alien species, one invader may buffer the impact of another. Our surveys on a remote floodplain in the Kimberley region of north western Australia show that invasive chinee apple trees (Ziziphus mauritiana) provide critical refuge habitat for native rodents (pale field rats, Rattus tunneyi). Feral horses (Equus caballus) have trampled most of the remaining floodplain, but are excluded from the area around each chinee apple tree by thorny foliage. Although chinee apple trees constituted <10% of trees along our transects, they represented >50% of trees that harboured rat burrows. The mean number of burrows under each chinee apple tree was twice as high as under most other tree species, and we trapped more than seven times as many rats under chinee apple trees as under other types of trees. The extensive burrow systems under chinee apple trees contained female as well as male rats, whereas we only captured males around the smaller burrow systems under other tree species. Our data suggest that this invasive tree plays a critical role in the persistence of pale field rat populations in this degraded ecosystem, and that managers should maintain these trees (despite their alien origins) at least until feral horses have been removed.     

Cofeeding intra‐ and interspecific transmission of an emerging insect‐borne rickettsial pathogen

Cat fleas (Ctenocephalides felis) are known as the primary vector and reservoir of Rickettsia felis, the causative agent of flea‐borne spotted fever; however, field surveys regularly report molecular detection of this infectious agent from other blood‐feeding arthropods. The presence of R. felis in additional arthropods may be the result of chance consumption of an infectious bloodmeal, but isolation of viable rickettsiae circulating in the blood of suspected vertebrate reservoirs has not been demonstrated. Successful transmission of pathogens between actively blood‐feeding arthropods in the absence of a disseminated vertebrate infection has been verified, referred to as cofeeding transmission. Therefore, the principal route from systemically infected vertebrates to uninfected arthropods may not be applicable to the R. felis transmission cycle. Here, we show both intra‐ and interspecific transmission of R. felis between cofeeding arthropods on a vertebrate host. Analyses revealed that infected cat fleas transmitted R. felis to naïve cat fleas and rat fleas (Xenopsylla cheopis) via fleabite on a nonrickettsemic vertebrate host. Also, cat fleas infected by cofeeding were infectious to newly emerged uninfected cat fleas in an artificial system. Furthermore, we utilized a stochastic model to demonstrate that cofeeding is sufficient to explain the enzootic spread of R. felis amongst populations of the biological vector. Our results implicate cat fleas in the spread of R. felis amongst different vectors, and the demonstration of cofeeding transmission of R. felis through a vertebrate host represents a novel transmission paradigm for insect‐borne Rickettsia and furthers our understanding of this emerging rickettsiosis.     

Invasive alien predator causes rapid declines of native European ladybirds

Aim Invasive alien species (IAS) are recognized as major drivers of biodiversity loss, but few causal relationships between IAS and species declines have been documented. In this study, we compare the distribution (Belgium and Britain) and abundance (Belgium, Britain and Switzerland) of formerly common and widespread native ladybirds before and after the arrival of Harmonia axyridis, a globally rapidly expanding IAS. Location Europe Methods We used generalized linear mixed‐effects models (GLMMs) to assess the distribution trends of eight conspicuous and historically widespread and common species of ladybird within Belgium and Britain before and after the arrival of H. axyridis. The distribution data were collated largely through public participatory surveys but verified by a recognized expert. We also used GLMMs to model trends in the abundance of ladybirds using data collated through systematic surveys of deciduous trees in Belgium, Britain and Switzerland. Results Five (Belgium) and seven (Britain) of eight species studied show substantial declines attributable to the arrival of H. axyridis. Indeed, the two‐spot ladybird, Adalia bipunctata, declined by 30% (Belgium) and 44% (Britain) over 5 years after the arrival of H. axyridis. Trends in ladybird abundance revealed similar patterns of declines across three countries. Main conclusion Together, these analyses show H. axyridis to be displacing native ladybirds with high niche overlap, probably through predation and competition. This finding provides strong evidence of a causal link between the arrival of an IAS and decline in native biodiversity. Rapid biotic homogenization at the continental scale could impact on the resilience of ecosystems and severely diminish the services they deliver.     

A preliminary assessment of the response of a native reptile assemblage to spot‐spraying invasive Bitou Bush with glyphosate herbicide

During recent work examining the effects of Bitou Bush (Chrysanthemoides monilifera ssp. rotundata) invasion on native reptile assemblages in coastal heathland vegetation in Eastern Australia, unplanned spot‐spraying of glyphosate occurred at some of our experimental sites invaded by Bitou Bush. We used this unexpected herbicide application as an opportunity to provide a preliminary assessment of the short‐term impacts on reptiles of glyphosate spot‐spraying of Bitou Bush. Using an M‐BARCI design, we compared reptile assemblages among uninvaded (reference) sites, invaded (control) sites and invaded and sprayed (impact) sites before and after spraying. We found no significant short‐term (7 – 10 months) differences in reptile abundance, species richness or assemblage composition among invaded, uninvaded and sprayed sites before and after glyphosate application. We cautiously interpret our results to generate a preliminary finding that spot‐spraying of Bitou Bush with glyphosate appears not to have a deleterious effect on reptile assemblages at seven and ten months following herbicide application. While we would not recommend basing management decisions on the outcomes of our study alone, we suggest that our findings can be used to assist in the development of strategic analyses of glyphosate impacts on native flora and fauna.     

Pre‐ and post‐ingestive defenses affect larval feeding on a lethal invasive host plant

Evolutionary traps arise when organisms use novel, low‐quality or even lethal resources based on previously reliable cues. Persistence of such maladaptive interactions depends not only on how individuals locate important resources, such as host plants, but also the mechanisms underlying poor performance. Pieris macdunnoughii (Remington) (Lepidoptera: Pieridae) lays eggs on a non‐native mustard, Thlaspi arvense (L.) (Brassicaceae), which is lethal to the larvae. We first tested whether larval feeding behavior was affected before (pre‐) ingestion or following (post‐) ingestion of leaf material, indicating activity of feeding deterrents, toxins, or both in this evolutionary trap. Neonates were less likely to start feeding and eventually fed more slowly on T. arvense than on the native host plant Cardamine cordifolia (Gray) (Brassicaceae) in both laboratory and field. Starvation was a primary cause of mortality, indicating the role of a feeding deterrent. Feeding did not differ between larvae from invaded and uninvaded population. Second, T. arvense defensive chemistry is dominated by the glucosinolate sinigrin (allyl or 2‐propenyl glucosinolate). Adding sinigrin to the leaves of T. arvense and native hosts C. cordifolia and Descurainia incana (Bernhardi ex Fischer & Meyer) (Brassicaceae) delayed the onset of feeding, caused larvae to feed more slowly, and decreased survival on the native hosts. This evolutionary trap may not be driven by a novel deterrent, but rather by a change in the concentration of a deterrent found in native hosts. Many insects have adapted to evolutionary traps posed by invasive plants, incorporating the new plant into their diets. Thlaspi arvense remains lethal to P. macdunnoughii, and pre‐ingestive deterrents such as excess sinigrin may contribute to persistent maladaptation.