Morphological description of the mouthparts of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)

Scanning (SEM) and transmission (TEM) electron microscopy were used to elucidate the morphology of the rostrum, as well as the mandibular and maxillary stylets of the psyllid Diaphorina citri, vector of phloem-inhabiting bacteria associated with citrus huanglongbing (HLB) disease. D. citri has a cone-shaped rostrum that extends behind the pair of prothoracic coxae. The stylet bundle comprises a pair of mandibular (Md) and maxillary (Mx) stylets with a mean length of 513.3 μm; when retracted, their proximal portions form a loop and are stored in the crumena (Cr). Serial cross-sections of the rostrum revealed that the mandibles are always projected in front of the maxillary stylets. The two maxillary stylets form the food and salivary canals, with diameters of 0.9 μm and 0.4 μm respectively. These two canals merge at the end of the stylets forming a common duct with a length of 4.3 μm and a mean diameter of 0.9 μm. The acrostyle, a distinct anatomical structure present in the common duct of aphid maxillary stylets, was not observed by TEM in the ultrathin cross-sections of the common duct (CD) of D. citri. This study provides new information on D. citri mouthparts that may help to understand the feeding behaviour of this important vector of HLB-associated bacteria.     

Asian citrus psyllid,Diaphorina citri,vector of citrus huanglongbing disease

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is an important pest of citrus because it transmits phloem‐limited bacteria [Candidatus Liberibacter spp., notably Ca. L. asiaticus (LAS)] associated with huanglongbing (HLB; citrus greening disease), currently considered the world's most serious disease of citrus. Asian citrus psyllid transmits LAS in a persistent manner and, although the rate of LAS transmission by ACP individuals usually is low, HLB can spread rapidly in a citrus grove and the geographic range of the disease is expanding, threatening citrus industries in new areas. Intensive chemical control of ACP is the primary management strategy currently advocated for HLB, but this strategy is costly, unsustainable, and generally ineffective. The scientific community is searching aggressively for solutions to HLB on many fronts, but it could still be years before solutions are found and implemented. Plant resistance to LAS is one area of research being pursued, whereby traits that confer resistance are identified and incorporated into citrus germplasm through conventional or transgenic methods. It remains to be seen if a solution to HLB can be found that specifically targets ACP, but research on ACP has been stepped up in a number of areas, notably on ACP–LAS–plant interactions, on host plant resistance to ACP, and on molecular methods of silencing ACP genes to induce mortality or to block its ability to transmit HLB‐causing bacteria. Advancements in these and other research areas may depend greatly on a better understanding of basic ACP biology and vector–pathogen–host plant interactions at the molecular, cellular, and community levels. Here, we present an updated review of ACP and HLB with an emphasis on the problem in Florida.     

Isolation and characterization of an Isaria fumosorosea isolate infecting the Asian citrus psyllid in Florida

A fungal pathogen that killed adult Diaphorina citri Kuwayama (Asian citrus psyllid) (Hemiptera: Psyllidae) in Florida citrus groves during the fall of 2005 was identified and characterized. Investigation of this pathogen is important because D. citri vectors citrus greening disease (Huanglongbing), which was reported in Florida in 2005. The morphological and genetic data generated herein support identification of the fungus as Isaria fumosorosea Wize (Ifr) (=Paecilomyces fumosoroseus) (Hypocreales: Cordycipitaceae) from the Asian citrus psyllid (Ifr AsCP). Koch’s postulates were fulfilled after the fungus was isolated in vitro and transmitted to healthy psyllids, which then exhibited a diseased-phenotype similar to that observed in the field. Both in vitro growth characteristics and two Ifr AsCP-specific molecular markers discriminated the psyllid pathogen from another local Ifr isolate, Ifr 97 Apopka. These molecular markers will be useful to track the dynamics of this disease in D. citri populations. The potential for utilizing Ifr to complement existing psyllid pest management strategies is discussed.     

Suitability of exotic and native lady beetle eggs (Coleoptera: Coccinellidae) for development of lady beetle larvae

Predation upon lady beetle (Coleoptera: Coccinellidae) eggs in the field is most often instances of egg cannibalism by larvae or adults while the majority of the remaining predation events upon coccinellid eggs is done by other species of Coccinellidae. Thus the recent introduction and establishment of Harmonia axyridis in the US could negatively affect native species of Coccinellidae via egg predation. However, little is known regarding the suitability of interspecific coccinellid eggs as a food source for larval development. In this study, it was found that native first or third instar Coleomegilla maculata and Olla v-nigrum larvae were incapable of surviving to the adult stage when provided solely exotic H. axyridis eggs. In stark contrast, H. axyridis larvae survived equally well when cannibalizing eggs or eating eggs of either native species. When C. maculata and O. v-nigrum were grouped as ‘native’ and compared with the exotic H. axyridis, more native eggs were attacked than exotic eggs and a higher percentage of eggs was attacked by H. axyridis larvae. Native and exotic larvae attacked a similar percentage of native eggs but native larvae attacked significantly fewer exotic eggs than did exotic larvae. These data suggest that H. axyridis may prey upon the eggs of these native species, when encountered in the field, compared with the likelihood of the native species preying upon H. axyridis eggs. Therefore, eggs of the native species C. maculata and O. v-nigrum will continue to be subjected to cannibalism and also to possible predation by other native species and the exotic H. axyridis.     

Characterization of electrical penetration graphs of the Asian citrus psyllid, Diaphorina citri, in sweet orange seedlings

Detailed information on probing behavior of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is critical for understanding the transmission process of phloem‐limited bacteria (Candidatus Liberibacter spp.) associated with citrus ‘huanglongbing’ by this vector. In this study, we investigated stylet penetration activities of D. citri on seedlings of Citrus sinensis (L.) Osbeck cv. Pêra (Rutaceae) by using the electrical penetration graph (EPG‐DC system) technique. EPG waveforms were described based on amplitude, frequency, voltage level, and electrical origin of the observed traces during stylet penetration into plant tissues. The main waveforms were correlated with histological observations of salivary sheath termini in plant tissues, to determine the putative location of stylet tips. The behavioral activities were also inferred based on waveform similarities in relation to other Sternorrhyncha, particularly aphids and whiteflies. In addition, we correlated the occurrence of specific waveforms with the acquisition of the phloem‐limited bacterium Ca. Liberibacter asiaticus by D. citri. The occurrence of a G‐like xylem sap ingestion waveform in starved and unstarved psyllids was also compared. By analyzing 8‐h EPGs of adult females, five waveforms were described: (C) salivary sheath secretion and other stylet pathway activities; (D) first contact with phloem (distinct from other waveforms reported for Sternorrhyncha); (E1) putative salivation in phloem sieve tubes; (E2) phloem sap ingestion; and (G) probably xylem sap ingestion. Diaphorina citri initiates a probe with stylet pathway through epidermis and parenchyma (C). Interestingly, no potential drops were observed during the stylet pathway phase, as are usually recorded in aphids and other Sternorrhyncha. Once in C, D. citri shows a higher propensity to return to non‐probing than to start a phloem or xylem phase. Several probes are usually observed before the phloem phase; waveform D is observed upon phloem contact, always immediately followed by E1. After E1, D. citri either returns to pathway activity (C) or starts phloem sap ingestion, which was the longest activity observed.     

Secondary hosts of the Asian citrus psyllid,Diaphorina citri Kuwayama: Survivorship and preference

The Asian citrus psyllid, Diaphorina citri Kuwayama, is the most economically important and difficult to manage citrus pest in Florida due to its role as vector of huanglongbing or citrus greening disease. Spread of the disease is a function of dispersal patterns and thus influenced by availability of suitable hosts. Young leaves of citrus or related plants are required for reproduction, but in their absence, secondary hosts may provide needed resources to enhance survival. Therefore, survivorship on and preference for three abundant weed species was investigated. The suitability of potential secondary host plants Bidens alba (L.), DC, Ludwigia octovalvis (Jacqu.) P. H. Raven, and Eupatorium capillifolium (Lam.) Small was compared to a reproductive host, Murraya paniculata (L.) Jack, in no‐choice tests by assessing survivorship of D. citri adults confined to these plants in cages. Preference was evaluated by choice tests where D. citri adults were released into cages containing all three secondary hosts alone or with M. paniculata. Both B. alba and E. capillifolium increased D. citri survivorship by twofold compared to starvation conditions with only water available. Choice trials revealed no difference in initial selection between true and secondary hosts; however, the true host was favoured over time. This result suggested that hosts were selected initially by sight, and only later by taste and/or smell. While secondary hosts are unable to support reproduction or long‐term survival, these findings establish the ability of D. citri to use secondary hosts that are ubiquitous in Florida citrus groves as temporary reservoirs for food and moisture when ideal host conditions are scarce or absent.     

Twelve polymorphic microsatellite loci from the Asian citrus psyllid,Diaphorina citri Kuwayama,the vector for citrus greening disease,huanglongbing

Twelve polymorphic microsatellite markers were developed from microsatellite‐enriched DNA libraries and mined from an expressed sequence tags library of Diaphorina citri, the vector of the citrus greening disease (huanglongbing). Analysis of 288 individuals from Florida, Texas, and Brazil showed that allelic diversity ranged from three to eight alleles per locus and observed and expected heterozygosities ranged from 0.014 to 0.569 and from 0.052 to 0.653, respectively. These variable microsatellite loci can provide means for assessing overall genetic variation and migration patterns for this agriculturally important pest species. This information can be used to aid in developing successful management strategies.     

Proteomic maps of subcellular protein fractions of the Asian citrus psyllid Diaphorina citri,the vector of citrus huanglongbing

The Asian citrus psyllid Diaphorina citri Kuwayama (Hemiptera: Liviidae) is an insect vector that transmits the bacterial pathogen Candidatus Liberibacter asiaticus (CLas) associated with the destructive citrus disease, citrus huanglongbing (HLB). Currently, D. citri is the major target in HLB management, although insecticidal control and disruption of the D. citri–CLas interactions both face numerous challenges. The present study reports the subcellular proteomic profiles of D. citri, encompassing the three main subcellular protein fractions: cytosol, mitochondria and microsomes. After optimization, subcellular proteins of both high and low abundance are obtained by two‐dimensional gel electrophoresis (2‐DE). A total of 1170 spots are detected in the 2‐DE gels of the three subcellular fractions. One hundred and sixty‐four differentially expressed proteins are successfully identified using liquid chromatography‐dual mass spectroscopy. An efficient protocol for subcellular protein fractionation from D. citri is established and a clear protein separation is achieved with the chosen protein fractionation protocol. The identified cytosolic proteins are mainly metabolic enzymes, whereas a large portion of the identified proteins in the mitochondrial and microsomal fractions are involved in ATP biosynthesis and protein metabolism, respectively. Protein–protein interaction networks are predicted for some identified proteins known to be implicated in pathogen–vector interactions, such as actin, tubulin and ATP synthase, as well as insecticide resistance, such as the cytochrome P450 superfamily. The findings should provide useful information to help identify the mechanism responsible for the CLas–D. citri interactions and eventually contribute to D. citri control.     

Development of an artificial diet and feeding system for juvenile stages of the Asian citrus psyllid,Diaphorina citri

The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is the main vector for the plant pathogen Candidatus Liberibacter asiaticus Jagoueix et al. (CLas). To date, attempts to develop an artificial diet for ACP have focused solely on the adult life stage, ignoring the juvenile stages. We developed a feeding system and artificial diet that is compatible with the juvenile stages of ACP and tested growth rates when exposed to varying concentrations of sucrose and amino acids. We found a surprisingly high tolerance for high sucrose concentrations in ACP when compared to known tolerances of sucrose concentrations in other phloem‐feeding insects. This is indicative that ACP may be physiologically adapted to a broad range of sucrose concentrations and osmotic stresses. The growth rate of juvenile ACP was optimized when amino acids were in a global concentration of 150 mM, with higher concentrations not appreciably impacting growth. This finding corresponds with the optimal amino acid concentrations required in other phloem feeders, notably the pea aphid. The development of this feeding system, with the diet optimized for growth, will allow for future experiments to be undertaken into the uptake of CLas by the psyllid and into the nutritional requirements of ACP. This feeding system will also allow for physiological comparisons among the phloem‐feeding insects.     

Pollen as an alternative food for Harmonia axyridis

The current study examines the potential of the multicoloured Asian lady beetle Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) to use pollen as a food to sustain development and reproduction in the absence of insect prey. Three populations of H. axyridis were used in this study: a long-term laboratory population (since 1998) and a melanic and non-melanic population originating from field collected individuals in Belgium. The insects were allowed to develop and reproduce on frozen eggs of Ephestia kuehniella Zeller (Lepidoptera: Phycitidae), frozen moist bee pollen or an even mixture of the two. Females of the field population offered the mixed diet initiated oviposition sooner than those fed only E. kuehniella eggs, but other developmental and reproductive traits were similar on these diets. A diet of pollen alone allowed 35–48% of the larvae of the field population of H. axyridis to successfully reach adulthood. However, developmental time for these individuals was prolonged by 31–49% and adult body weight was reduced by 37–68%, compared to individuals offered the diets containing E. kuehniella eggs. When fed exclusively on pollen in their larval and adult life, about 40% of the adult females of either field population were able to produce a small number of viable eggs. The laboratory and field strains differed in their response to diet for a number of developmental and reproductive traits. The exploitation of pollen and other plant foods at times when insect prey is scarce, may offer a further competitive advantage to the non-indigenous coccinellid H. axyridis over native European predatory lady beetles that share the same niche and are less capable of using pollen as an alternative food.     

柑橘木虱两地理种群的内共生菌群落组成及传菌能力

柑橘黄龙病（Huanglongbing, HLB）是经柑橘木虱Diaphorina citri传播的最主要柑橘病害之一, 危害严重时能对柑橘产业造成毁灭性的破坏。为了鉴定福建和海南2个地理种群柑橘木虱的内共生菌群落组成, 本研究对16S rRNA部分保守序列进行PCR扩增, 并利用特异性引物对不同内共生菌进行了感染率检测; 另外, 还通过人工接虫的方法, 探索柑橘木虱成虫在带黄龙病菌蕉柑Citrus reticulata cv. Tankan上的获菌能力, 以及带菌柑橘木虱成虫对黄岩蜜橘C. reticulata cv. Subcompressa的传菌能力。研究发现, 这2个地理种群的柑橘木虱含有相同的内共生菌组成, 包括α-Proteobacteria, Wolbachia spp., γ-Proteobacteria, mycetocyte symbionts, β-Proteobacteria, Oxalobacter和β-Proteobacteria, Herbaspirillum, 而且这2个地理种群柑橘木虱的4种内共生菌的携带率均在95%以上。柑橘木虱成虫在带菌蕉柑上饲菌28 d后, 带菌率可达到82%, 而带菌柑橘木虱成虫在黄岩蜜橘上传菌75 d后, 可导致橘树整体带菌。本研究为柑橘木虱的进一步研究和防虫治病途径提供了一些理论依据。     

Evaluation of Isaria fumosorosea (Hypocreales: Cordycipitaceae) for control of the Asian citrus psyllid,Diaphorina citri (Hemiptera: Psyllidae)

A laboratory bioassay was developed to evaluate strains of Isaria fumosorosea Wize, against Diaphorina citri. Up to 100% of adult psyllids were killed at concentrations between 10⁶ and 10⁷ blastospores/ml after 12 days, with derived LC₅₀ values (at 7 days post treatment) between 1.4 × 10⁵ and 2.0 × 10⁶ blastospores/ml for strains ARSEF 3581, FE 9901 and Apopka-97. A significantly higher value (1.5 × 10⁷) was obtained with a conidial formulation of Apopka-97. Average survival times were dosage dependent, i.e. between 10.2 days at 10³ blastospores/ml and 3.5 days at 10⁸ blastospores/ml. Rates of mycosis were also dosage dependent, with up to 100% sporulation on cadavers at 10⁸ blastospores/ml but declining at lower concentrations. The Apopka-97 strain (commercially available as PFR-97) was tested against established D. citri infestations in potted citrus in greenhouse cages. Treatments at label rates reduced psyllid populations by approximately 50% over 3 weeks. The combination of PFR-97 with emulsifiable oils (0.25% v/v) did not increase psyllid mortality compared with either agent alone. Imidacloprid applied as a drench killed 100% of psyllids within 3 weeks. Subsequent greenhouse tests during humid conditions were hampered by natural dissemination of I. fumosorosea to untreated psyllids, suggesting that this fungus is spread by air movement and may be highly effective under very humid conditions. In later tests, a Cladosporium sp. rapidly colonised psyllid cadavers and leaf surfaces, but was not pathogenic in laboratory tests. Our studies confirm the potential of I. fumosorosea to be used in IPM strategies for D. citri that rely on other tactics, such as insecticidal oils and native or introduced biological control agents.     

Morphological and molecular characterization of a Hirsutella species infecting the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), in Florida

The Asian citrus psyllid, Diaphorina citri Kuwayama, is an invasive pest that vectors citrus greening disease, which recently was detected in Florida. Mycosed adult D. citri were collected at four sites in central Florida between September 2005 and February 2006. Observation of the cadavers using scanning electron microscopy revealed that the pathogen had branched synnemata supporting monophiladic conidiogenous cells. A high-fidelity polymerase chain reaction (PCR) assay was used to amplify the 18S rRNA, 28S rRNA and beta-tubulin genes of the pathogen for phylogenetic analysis. The morphological and genetic data indicated that the pathogen was a novel isolate related to Hirsutella citriformis Speare. PCR assays using isolate-specific primers designed from the unique putative intron region of the beta-tubulin sequence distinguished the psyllid pathogen from five related Hirsutella species. The pathogen was maintained in vivo by exposing healthy D. citri to the synnemata borne on field-collected cadavers. Infected psyllids had an abundance of septate hyphal bodies in their hemolymph and exhibited behavioral symptoms of disease. In vitro cultures of the pathogen were slow-growing and produced synnemata similar to those found on mycosed D. citri. In laboratory bioassays, high levels of mortality were observed in D. citri that were exposed to the conidia-bearing synnemata produced in vivo and in vitro.     

Mechanisms of prey finding in the aphidophagous ladybird beetle,Harmonia axyridis [Coleoptera: Coccinellidae]

The mechanism of prey finding in adultHarmonia axyridis was investigated by presenting beetles with small gauze or polyethylene bags containing either aphidinfested leaves or healthy leaves alone together with empty control bags. Beetles were attracted to bags by olfactory and visual cues suggesting the presence of aphids, including the odor of aphid-infested leaves, the odor of aphids, the odor of healthy leaves, and the sight of leaves. Particularly effective in prolonging beetles's stay on bags visited was the odor of aphid-infested leaves. It is suggested that adults ofH. axyridis use olfactory and visual cues to detect prey before actual contact occurs. Use of such cues seems more advantageous than random searching, as has been reported in many previous studies of coccinellid foraging.

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Résumé Le mécanisme de découverte de la proie chez l'adulte d'Harmonia axyridis est étudié en donnant aux Coccinelles de petits sacs en gaze ou en polyéthylène contenant soit des feuilles infestées de pucerons, soit des feuilles saines seules, avec des sacs vides comme témoins. Les coccinelles sont attirées vers les sacs par des indicateurs olfactifs ou visuels suggérant la présence de pucerons, incluant l'odeur des feuilles infestées de pucerons, l'odeur des pucerons, l'odeur des feuilles saines et la vue des feuilles. L'odeur des feuilles infestées de pucerons est particulièrement efficace en prolongeant le séjour des Coccinelles sur le sac visité. Il est suggéré que les adultes d'H. axyridis utilisent des indicateurs olfactifs et visuels pour détecter leur proie avant que s'établisse le véritable contact. L'emploi de tels indicateurs semble plus avantageux que la recherche au hasard, comme cela a été indiqué dans de nombreuses études antérieures sur la quête alimentaire des Coccinelles.

     

Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae), and huanglongbing disease do not exist in the Stapleton Station area of the Northern Territory of Australia

Abstract  A series of specimens of the Asian citrus psyllid, Diaphorina citri , collected from the Northern Territory (NT) in 1915 was recently rediscovered in the Natural History Museum, London. Surveys were conducted in 2002 on suitable hosts in the locality of the 1915 collections to see if the infestation had persisted. These failed to detect either D. citri or the bacterium that it transmits and that causes huanglongbing disease in citrus. It is presumed that D. citri was eradicated fortuitously by the removal of all citrus plants above latitude 19°S during an eradication program for citrus canker in the NT from 1916 until 1922.     

nC22矿物油及其与吡虫啉混用对柑橘木虱的室内毒力评价

【目的】室内评价nC22矿物油单独使用,以及与吡虫啉混用对柑橘木虱Diaphorina citri的毒力,并筛选nC22矿物油对吡虫啉防治柑橘木虱具有增效作用的混配比例,为矿物油防治柑橘木虱的应用提供科学依据。【方法】使用nC22矿物油以及阳性对照nC23和nC28矿物油,采用浸渍法和喷雾法分别检测矿物油对柑橘木虱卵和低龄若虫、高龄若虫、成虫的致死作用,以处理后第7天(卵)和第1天(若虫和成虫)的LC₅₀值评估毒力。将nC22矿物油与吡虫啉以不同配比混配,测定混配液对低龄若虫的毒力,使用交互测定法、共毒因子(co-toxicity factor, CTF)法和共毒系数(co-toxicity coefficient, CTC)法评价矿物油对吡虫啉的增效作用。【结果】单独使用时,nC22矿物油对卵的LC₅₀值低于nC23和nC28矿物油;对低龄若虫和高龄若虫的LC₅₀值与nC23矿物油相当,都低于nC28矿物油;对成虫的LC₅₀值与nC28矿物油相当,都低于nC23矿物油。与吡虫啉混用时,nC22矿物...     

Patterns of habitat use by the Asian citrus psyllid,Diaphorina citri,as influenced by abiotic and biotic growing conditions

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Establishment of multicolored Asian lady beetle in Eastern North Carolina: Seasonal abundance and crop exploitation within an agricultural landscape

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Biological control of citrus mealybug,Planococcus citri with an introduced parasite,Leptomastix dactylopii in India

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Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana

The exotic multicolored Asian lady beetle, Harmonia axyridis, became established and recently spread across much of North America and southern Canada. In a habitat now used by both the invading H. axyridis and a native lady beetle, Olla v-nigrum, we discovered that the native lady beetle was commonly infected by Beauveria bassiana; whereas, the exotic H. axyridis, was not. Laboratory assays revealed that B. bassiana isolates collected from naturally infected O. v-nigrum were pathogenic to adult O. v-nigrum but not to adult H. axyridis. In contrast, the GHA strain of B. bassiana was not significantly pathogenic to O. v-nigrum nor H. axyridis. Late-season field collections revealed significantly higher B. bassiana infection of O. v-nigrum than H. axyridis. Our results lead us to hypothesize that low susceptibility of H. axyridis to B. bassiana (found to infect O. v-nigrum) may provide an intraguild advantage to H. axyridis over O. v-nigrum; this may also occur with other species of native lady beetles and other endemic entomopathogens in different habitats and regions.