Electrical penetration graph evidence that pymetrozine toxicity to the rice brown planthopper is by inhibition of phloem feeding

BACKGROUND: Pymetrozine is a valuable novel insecticide for control of sucking insects, including the brown planthopper Nilaparvata lugens (Stål), one of the most serious pests on rice. This study was conducted to elucidate the action mechanisms of pymetrozine on the feeding behaviour of the planthopper. RESULTS: The activity test showed that pymetrozine primarily functioned as an antifeedant that caused starvation and death in N. lugens, rather than having neurotoxicity. Pymetrozine‐treated insects died at a significantly slower speed than insects treated with starvation. Electrical penetration graph (EPG) data indicated that pymetrozine significantly increased the duration of non‐probing periods and had a strong inhibition to phloem ingestion. The inhibition was strongly dose dependent, resulting in a complete suppression of the activity in the phloem region when the pymetrozine concentration was increased to 400 mg L^?1. Starvation caused by inhibition of phloem ingestion might be a major toxicity mechanism of pymetrozine. EPG data also showed that pymetrozine had no significant effect on stylet movement and duration of xylem sap ingestion. CONCLUSION: The study revealed that pymetrozine disturbed the feeding behaviour of N. lugens mainly by increasing the non‐probe period and inhibiting phloem ingestion. The inhibition resulted in a slow death similar to starvation. Copyright © 2011 Society of Chemical Industry     

Translocation of Pymetrozine in Plants

Pymetrozine, a pyridine-azomethine, is a selective biocide against aphids, whiteflies and plant hoppers with a high plant systemic activity. By means of bioassays and autoradiographic techniques it has been shown that this systemic behaviour originates not only from xylem but also from phloem mobility. After foliar application the growing points of plants are protected by pymetrozine imports mainly from leaves. This indicates a high importance of phloem mobility for the systemic activity of pymetrozine against plant-sucking insects. © 1997 SCI.     

Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding

Flonicamid (IKI220; N-cyanomethyl-4-trifluoromethylnicotinamide), a pyridinecarboxamide compound, is a novel systemic insecticide with selective activity against hemipterous pests, such as aphids and whiteflies, and thysanopterous pests. The purpose of this study is to clarify the biological properties of flonicamid against aphids. Flonicamid is very active against aphids, regardless of differences in species, stages and morphs. This compound inhibited the feeding behaviour of aphids within 0.5 h of treatment without noticeable poisoning symptoms such as convulsion, and this antifeeding activity was not recoverable until death. The nymphs born from adults exposed to flonicamid for 3 h showed high mortality. The effect of flonicamid on the feeding activity of an individual aphid was studied using electronic monitoring of insect feeding behaviour (EMIF). Although the treated aphid attached the head of its proboscis to the leaf surface, salivation and sap feeding were strongly inhibited. These results suggest that the main insecticidal mechanism of flonicamid is starvation based on the inhibition of stylet penetration to plant tissues.     

Divergent effects of PVY-infected potato plant on aphids

Host plant selection by aphids can be positively or negatively affected when plants are infected by phytoviruses. Potato plants infected by Potato virus Y (PVY), a non-persistent virus, are reported to affect settling behaviour and growth parameters of Myzus persicae Sulzer and Macrosiphum euphorbiae Thomas. Using the Electrical penetration graph system (EPG), we demonstrated that PVY-infection of potato plants influences the feeding behaviour of these two aphid species. Myzus persicae exhibited increased phloem sap ingestion and reduced non-probing duration. Macrosiphum euphorbiae showed delayed stylet insertion, reduced activity in the phloem vessels and an enhanced non-probing duration. In addition, we showed that these two species exhibited different transmission rates. The opposite effects of PVY-infected potato plant on these two aphids are discussed in terms of PVY spreading in the field.     

吡蚜酮对禾谷缢管蚜的亚致死效应

本文研究了吡蚜酮对禾谷缢管蚜的亚致死效应。试验利用刺探电位图谱(EPG)技术测定了亚致死剂量的吡蚜酮对禾谷缢管蚜成虫取食行为的影响,结果表明:经吡蚜酮处理的蚜虫口针从开始刺探到持续吸食韧皮部和木质部汁液的时间明显延长,分别延长至(199.9±34.0)min和(236.4±29.5)min,对照分别为(155.5±18.1)min和(145.5±27.1)min。并且,经药剂处理的蚜虫口针在韧皮部和木质部中持续取食的时间明显缩短,分别为(44.7±9.4)min和(11.8±2.5)min,对照分别为(93.0±24.9)min和(19.0±3.6)min。通过生长和繁殖试验可知:亚致死剂量的吡蚜酮使禾谷缢管蚜的重量显著减轻,繁殖率明显降低。经药剂处理的蚜虫最大重量和最高繁殖率分别为(1.28±0.025)mg/10头和(2.9±0.2)头/成蚜,而对照分别为(1.56±0.099)mg/10头,(5.2±0.2)头/成蚜。     

Effects of cycloxaprid,a novel cis‐nitromethylene neonicotinoid insecticide,on the feeding behaviour of Sitobion avenae

BACKGROUND: Cycloxaprid with cis‐configuration is a novel neonicotinoid insecticide, developed in China, that has good industrialisation prospects for its high activity against imidacloprid‐resistant pests. Studies were carried out to investigate the biological activity of cycloxaprid and its effect on the feeding behaviour of Sitobion avenae. RESULTS: The results demonstrated that cycloxaprid had good contact and root‐systemic activity. The electrical penetration graph (EPG) revealed that cycloxaprid significantly increased the total time of non‐probing periods and greatly inhibited phloem ingestion of treated aphids because it significantly reduced the total time and the frequency of phloem ingestion. Furthermore, cycloxaprid can increase the phloem salivation of treated aphids by comparison with aphids treated with imdacloprid and distilled water. Consequently, a sublethal dose of cycloxaprid impaired aphid ingestion of phloem sap and thereby reduced the weight of aphids. On the other hand, EPG data showed that a sublethal dose of cycloxaprid had no significant effect on xylem sap ingestion, in contrast to imidacloprid. CONCLUSION: All these tests indicated that cycloxaprid had both contact and root‐systemic activity, with sublethal effects resulting in reduction in Sitobion avenae phloem‐feeding behaviour and growth rate. Copyright © 2012 Society of Chemical Industry     

Effects of pymetrozine, an antifeedant of Hemiptera, on Asian citrus psyllid, Diaphorina citri, feeding behavior, survival and transmission of Candidatus Liberibacter asiaticus

BACKGROUND: Vector‐borne plant disease management can be enhanced by deployment of antifeedants in addition to the use of broad‐spectrum neurotoxic insecticides. The effects of pymetrozine on Asian citrus psyllid (ACP), Diaphorina citri Kuwayama, feeding behaviour, survival and transmission of Candidatus Liberibacter asiaticus (Las), the presumed causal pathogen of huanglongbing, were investigated. RESULTS: Pymetrozine applied at 52 and 104 µg mL^?1 to citrus plants [Swingle citrumelo (X Citroncirus webberi Ingram and Moore)] modified the feeding behavior of ACP and increased the amount of time spent performing non‐penetration behaviors while decreasing the time spent performing ingestion behaviors compared with the controls 1 day after treatment. However, the antifeedant effect of pymetrozine subsided 5 days after application. Pymetrozine reduced the survival of both adults and nymphs on treated plants compared with the control. However, it had a greater impact on survival of nymphs than on survival of adults. Pymetrozine applied at 52 and 104 µg mL^?1 on Las‐infected ‘Valencia’ sweet orange plants [Citrus sinensis L. (Osbeck)] reduced acquisition (12 and 21% respectively) and transmission (11 and 18% respectively) of Las by feeding ACP adults compared with the controls; however, these reductions were not statistically significant. CONCLUSIONS: Pymetrozine exhibited moderate antifeedant effects by modifying the feeding behavior of ACP adults with short residual activity. The impact of pymetrozine on survival of nymphs was greater than on adults at the higher concentrations tested. Pymetrozine also reduced the acquisition and transmission of Las by feeding ACP adults up to 21 and 18%, respectively, compared with untreated controls. Copyright © 2010 Society of Chemical Industry     

基于EPG分析无翅型和有翅型柑橘蚜虫的取食行为

为明确无翅型、有翅型柑橘蚜虫取食行为的差异,采用EPG技术对褐色橘蚜Toxoptera citricida(Kirkaldy)和棉蚜Aphis gossypii Glover的有翅型、无翅型成蚜在柑橘苗上的取食行为进行测定。结果表明,褐色橘蚜无翅型和有翅型的EPG均记录到7种取食波形,依次为非刺探波np、路径波A、B和C、电位下降波pd、韧皮部取食波E1和E2;棉蚜无翅型和有翅型的EPG记录到9种取食波形,除上述7种外,还包括木质部主动吸食波G和口针阻碍波F。褐色橘蚜有翅型和无翅型的np波持续时间为25.73 min和8.39 min,二者间差异显著;棉蚜有翅型的np波持续时间、刺探次数、C波次数分别为27.34 min、19.16次、20.21次,显著高于无翅型,而刺探总持续时间为332.66 min,显著低于无翅型。棉蚜的C波次数及总持续时间、刺探次数、pd波次数及总持续时间均显著高于褐色橘蚜,而E2波总持续时间及平均持续时间均显著小于褐色橘蚜。表明棉蚜无翅型比有翅型在柑橘上更容易取食,影响有翅型蚜虫取食的抗性因子可能位于柑橘表面;褐色橘蚜比棉蚜对柑橘的适应性更强。     

Systemic action of novel neonicotinoid insecticide IPP‐10 and its effect on the feeding behaviour of Rhopalosiphum padi on wheat

BACKGROUND: IPP‐10 is a novel neonicotinoid insecticide recently developed in China and has good activity against sucking insects. Studies were carried out to investigate the activity of IPP‐10 against Rhopalosiphum padi L. RESULTS: The results demonstrated that IPP‐10 had both contact and systemic activity, including acropetal and basipetal translocation in wheat vascular bundles. Starved R. padi were allowed to stay on wheat treated with a sublethal dose of IPP‐10. The results of studying their feeding behaviour from an electrical penetration graph (EPG) revealed a decrease in total time and bout duration of xylem and phloem ingestion, but the total time and bout duration of phloem salivation were significantly prolonged. The frequency (7.03 ± 0.49 Hz) of the xylem ingestion waveform produced by aphids on wheat treated with IPP‐10 was significantly lower than that of blank control aphids (8.20 ± 0.30 Hz). Consequently, aphids born on wheat treated with IPP‐10 were obviously lighter and less fecund than the control aphids. CONCLUSION: These tests indicated that IPP‐10 had both contact and systemic activity, with sublethal effects resulting in reduction in R. padi feeding behaviour, growth rate and fecundity. Copyright © 2010 Society of Chemical Industry     

蚜虫传播非持久性病毒的取食行为调控机制

蚜虫能够传播上百种植物病毒,是最重要的农业介体昆虫之一。蚜虫在刺探和取食植物过程中,唾液组分会连同附着在口针中的病毒粒子一同被分泌进入植物内,在调节植物诱导抗性、病毒侵染扩散、介体昆虫行为等过程中均有重要作用。本文围绕蚜虫传播病毒和获取病毒2个关键过程,总结分析了蚜虫独特的刺吸取食行为与传毒效率和获毒效率之间的联系;针对取食活动中关键的唾液蛋白在调控植物免疫抗性、帮助病毒侵染过程中的功能,阐述了蚜虫高效传播非持久病毒的分子基础;针对蚜虫的获毒过程,综述了病毒侵染植物间接调控蚜虫趋向和行为的作用方式。这些研究的开展将为解释蚜虫和病毒协同侵染的分子机制以及有效开展基于蚜虫取食行为调控的病虫害防控新技术提供思路。     

Behaviour modifying effects of low systemic concentrations of imidacloprid on Myzus persicae with special reference to an antifeeding response

With a combination of biological, analytical, electrophysiological, and video-optical methods, it was possible to show that low concentrations of the new chloronicotinyl insecticide, imidacloprid, strongly affect the behaviour of Myzus persicae (Sulz.), leading eventually to the death of the aphids. Tests to elucidate the biological properties were performed under laboratory conditions with cabbage leaf petioles placed in insecticidal solutions over different periods of time. LC_15(24h) values were considered as low concentrations and calculated for imidacloprid and pirimicarb, respectively. Imidacloprid at low concentrations depressed the honeydew excretion of apterous adults of M. persicae by almost 95% within 24 h without affecting the vitality of the majority of aphids, whereas, at equitoxic concentrations, pirimicarb showed much weaker effects on honeydew excretion, which strongly coincided with mortality. In choice experiments with alate morphs of M. persicae over 48 h, their larvae almost always occurred on the untreated control leaf, and were not found on the leaf which was treated systemically with low concentrations of imidacloprid. Apterous aphids placed on cabbage leaves systemically treated with low concentrations of imidacloprid showed nearly the same decrease in weight as untreated starving aphids, suggesting that their death was caused by starvation. Aphids that were moved from imidacloprid-treated to untreated leaves after 24 h began feeding on the latter and showed a steady increase in weight and honeydew production. This suggests that the behavioural response is reversible. Aphids on pirimicarb-treated (equitoxic dose) leaves showed no decrease in weight. Electrical penetration graphs revealed that M. persicae on artificial membranes containing imidacloprid probed more often before feeding than aphids on control sachets. Time-lapse videofilming of apterous adults placed on cabbage leaves revealed a migration from the leaf treated with low concentrations of imidacloprid to an untreated leaf. From the results of these experiments and the observed symptomatology it is possible to postulate two different and dose-dependent modes of action of imidacloprid on M. persicae: (1) the well-known mode of action with visually obvious irreversible symptoms (paralysis, tremor, uncoordinated leg-movement) at field rates, and (2) the reversible starvation response as an antifeedant effect, which is not coupled with typical symptoms of neuronal disorder, at lower concentrations.     

内共生菌Buchnera协助蚜虫抑制寄主植物的防御反应

为明确蚜虫内共生细菌Buchnera能否协助蚜虫抑制植物的防御反应,采用混合抗生素除去瓜蚜Aphis gossypii体内的Buchnera,采用刺吸电位技术和生命表方法比较除菌瓜蚜和正常瓜蚜在黄瓜上的适合度,并测定被除菌瓜蚜和正常瓜蚜预侵染黄瓜叶片中H₂O₂、茉莉酸和水杨酸的含量变化以及抗蚜特性变化。结果表明,除菌瓜蚜体重较正常瓜蚜极显著下降了71.15%,净增殖率极显著下降了95.60%,但寿命延长了2.34倍;刺吸电位图谱显示除菌瓜蚜几乎不产生代表唾液分泌的E1波和韧皮部被动吸食的E2波。在黄瓜叶片中,除菌瓜蚜比正常瓜蚜能激发产生更高水平的H₂O₂;在为期14 d的侵染中,除菌瓜蚜侵染诱发总茉莉酸含量持续升高、总水杨酸含量持续下降,而正常瓜蚜侵染诱发总茉莉酸含量先升高后降低、总水杨酸含量先降低后升高。在被除菌瓜蚜预侵染黄瓜上,瓜蚜进入稳定取食的时间显著滞后于正常瓜蚜预侵染处理,且前3 d的产蚜量显著低于正常瓜蚜预侵染处理。表明Buchnera除了可为蚜虫提供必需的营养外,还有调控和抑制寄主植物防御反应的功能。     

O3浓度升高对棉蚜取食行为的影响

在加倍O3浓度的开顶式气室(OTC)中培养抗虫棉GK12幼苗30 d,正常O3浓度处理为对照。应用刺探电位图谱(EPG)技术,对棉蚜(Aphis gossypii Glover)在苗期棉花上的取食行为进行了比较研究。结果表明：蚜虫在加倍O3浓度下生长的棉苗上取食的过程中,C波数量显著减少,pd波首次出现时间明显提前,被动取食持续时间(E2波的总时间)明显拉长。棉蚜的取食适合度明显提高的原因可能是加倍O3浓度对棉花叶片组织结构和体内营养物质的变化有影响。     

Feeding behavior of sedentary plant parasitic nematodes

With the aid of video-enhanced contrast light microscopy the feeding behavior of the cyst nematodeHeterodera schachtii and the root-knot nematodeMeloidogyne incognita has been studied in roots of various cruciferous plants, especially inArabidopsis thaliana, a model plant for molecular studies. The juvenile stage 2 (J2) nematodes ofH. schachtii migrate intracellularly with destructive stylet thrusts before establishing their permanent feeding site (syncytium) within the vascular cylinder. After the selection of the initial syncytial cell (ISC) they undergo a preparation period before they start feeding from the ISC. During all developmental stages feeding occurs in cycles, composed of three distinct phases. In contrast, the J2 ofMeloidogyne incognita reach their permanent feeding site by intercellular migration, first towards the apex of the root, where they turn round, and move towards the differentiating vascular cylinder. A characteristic behavioral pattern, composed of continuous head and stylet movements, interspersed by periods of stylet-tip protrusion and metacorpal bulb pumping is maintained during all phases of parasitism, i.e., root invasion, intercellular migration and feeding from the giant-cells.     

柑橘三种蚜虫取食行为的EPG分析

为探究柑橘3种蚜虫取食行为差异,利用刺吸电位图谱(electrical penetration graph,EPG)技术对褐色橘蚜Toxoptera citricida(Kirkaldy)、棉蚜Aphis gossypii Glover和绣线橘蚜Aphis citricola van der Goot在椪柑上的取食行为进行了测定。结果表明:3种蚜虫均产生8种取食波形,依次为非刺探波(np波)、路径波(A、B、C波)、电位下降波(pd波)、韧皮部分泌唾液波(El波)、韧皮部被动吸食波(E2波)以及木质部主动吸食波(G波)。棉蚜开始取食的第1次刺探时间最早,绣线橘蚜刺探的次数最多,且C波时间最长。褐色橘蚜pd波出现的次数最少,棉蚜次之,绣线橘蚜最多,显著高于褐色橘蚜。与其它2种蚜虫相比,绣线橘蚜于木质部主动吸食汁液(G波)时间最长,有G波的个体比例最高。3种蚜虫E1波次数和总持续时间差异均不显著,但褐色橘蚜E2波的持续时间217.01±27.56 min显著长于棉蚜142.49±27.85 min和绣线橘蚜116.64±20.05 min。初步推断3种蚜虫对柑橘衰退病毒的传毒效率与E2波有关。     

我国主要农作物蚜虫生物防治的研究进展、应用与展望

蚜虫是农业生产上的重大害虫,不仅通过取食韧皮部直接为害植物,还会传播很多植物病毒病,严重影响农作物产量和品质。目前防治蚜虫仍以化学农药为主,然而生物防治作为绿色环保、可持续的防治策略在这几十年中也得到了长足发展。该文对我国近60年关于主要农作物蚜虫生物防治的研究进展进行概述,包括主要农作物蚜虫的天敌资源（主要寄生性天敌196种,主要捕食性天敌16种,主要病原微生物6种）、蚜虫主要天敌生物学和生态学研究、人工扩繁及应用技术及植物抗蚜机制和抗蚜种质资源挖掘,并对目前蚜虫生物防治中存在的问题及未来的研究方向进行展望,以期为蚜虫生物防治技术的发展和推广应用提供参考。     

Intraspecific variation in Capsella bursa-pastoris in plant quality traits for insect herbivores

The arable plant Capsella bursa‐pastoris is phenotypically variable in many life history traits, particularly time from germination to flowering. The hypothesis was investigated that, associated with this variation, there are differences in traits that influence plant quality for insect herbivores. Significant within‐species variation was found in plant growth, leaf surface characteristics and tissue nutrient composition among 21 accessions of Capsella. Short flowering time plants exhibited slow vegetative growth, relatively large shoot nitrogen content, high leaf hair densities and differences in phloem composition, compared with long flowering time plants. Insect herbivore response to distinctive trait combinations was assessed on a subset of seven accessions using the phloem‐feeding aphids Aphis fabae and Myzus persicae. Variation in aphid performance was small but significant, with 15–25% fewer nymphs produced on plant variants that exhibited greater tissue water content and low tissue C:N ratio (A. fabae) or on variants with less phloem nitrogen (M. persicae). The differential responses exhibited by the two aphid species to the test accessions confirmed that quantifying intraspecific plant variation is a necessary first step in understanding plant functional diversity and its impact on consumers in arable systems.     

Feeding behavior of<Emphasis Type="Italic">Aphis gossypii</Emphasis> on resistant accessions of different melon genotypes (<Emphasis Type="Italic">Cucumis melo</Emphasis>)

The feeding behavior of the melon aphidAphis gossypii Glover (Homoptera: Aphididae) was monitored using the electrical penetration graph (EPG) technique on different melon (Cucumis melo L.) genotypes showing resistance to the aphid. The aphid-resistant genotypes used were PI-161375 and PI-414723, sources of theVat andAgr genes, respectively. TGR-1551, a newC. melo accession from Zimbabwe, was also tested. Our goal was to localize the tissues where the resistance factors are expressed and to determine if the resistance mechanisms operating in the three aphid-resistant accessions were the same. Our results indicated that the three selected lines have resistant factors located at the epidermis, mesophyll and vascular tissues. However, the behavior ofA. gossypii on TGR-1551 was different from the two other resistant accessions, as indicated by a longer phloem salivation phase (E1 phase). Many of the E1 phases observed for aphids feeding on TGR-1551 were not followed by phloem ingestion (E2 phase). These results suggest that TGR-1551 has a resistance mechanism that preventsA. gossypii from initiating ingestion from the phloem. Preference tests under free choice conditions also showed that aphids rejected accessions TGR-1551 or PI-414723 faster than PI-161375. Our results support the hypothesis thatAgr andVat are coding for different kinds of resistance strategies. Comparisons of aphid life history parameters also indicated that TGR-1551 is a very promising new source to breed for resistance againstA. gossypii. http://www.phytoparasitica.org posting Jan. 16, 2002.     

Early intracellular punctures by two aphid species on near-isogenic melon lines with and without the virus aphid transmission (Vat) resistance gene

The Vat resistance gene (in Cucumis melo L.) inhibits the transmission of non-persistent viruses by Aphis gossypii Glover, but does not affect transmission by Myzus persicae (Sulz.). To see whether this difference was behaviourally determined, we investigated the stylet penetration behaviour of these two aphid species by recording EPGs (Electrical Penetration Graphs) of 8 and 20 min on two sets of susceptible and resistant isogenic melon lines. During the 20 min EPG study, inoculation with CMV (Cucumber Mosaic Virus) was also investigated. For both sets of isogenic lines, the two aphid species were able to detect the presence of Vat. The mean duration of individual intracellular punctures on the resistant genotypes was significantly reduced for both M. persicae and A. gossypii (-10% and -8% respectively for duration of pattern ‘pd’ in the 20 min experiment); this reaction appeared faster for M. persicae, a species for which melon was not a suitable host-plant. Therefore, in contrast to Vat's anti-transmission effect, this behavioural effect was not aphid species-specific. Also, the frequency of intracellular punctures on the resistant genotypes was significantly reduced in A. gossypii (but not in M. persicae): on average, this frequency dropped from ≈0.65 pd.min^-1 on the susceptible genotypes to ≈0.5 pd.min^-1 on the resistant ones. It was concluded that (intracellular?) chemical cues were detected very early by aphids probing on the resistant genotypes carrying the Vat gene. However, a comprehensive analysis of the behavioural traits of both aphids on the two genotypes could not alone account for the complete inhibition of transmission which was found only to occur for A. gossypii on resistant genotypes. None of the differences detected (between aphid species or between plant genotypes) could account for the Vat phenotype, although they may explain quantitative differences in transmission efficiencies between aphid species. It was thus concluded that Vat effect was primarily chemically mediated. Finally, some intracellular punctures bearing typical subphases have been identified in both aphid species and were designated as ‘long potential drops’ (pd-L). For A. gossypii, these were observed early after plant contact and their mean duration was twice that of standard intracellular punctures (≈8.5 s vs ≈4.2 s). Although not necessary for CMV inoculation, the duration of such phases was positively correlated with a high transmission efficiency by A. gossypii on the susceptible genotype. The nature of this pattern and a putative mechanism of action of the Vat gene are discussed.     

Aphid feeding rates on healthy and beet curly top virus-infected plants

Based on the frequency of honeydew droplet excretion, the feeding rate of green peach aphids,Myzus persicae (Sulz.), on the swollen leaf veins of beet curly top virus-infectedAmsinckia douglasiana DC. plants was found to be almost twice as high as on the veins of uninfectedAmsinckia plants. Radiochemical analysis of the honeydew indicated that the phloem sap in the swollen veins has a higher sucrose concentration than that in uninfected plants. Although disease-associated changes in the anatomy and in the level of gustatory nutrients in the phloem sap may contribute to the enhanced feeding rate, a higher turgor pressure of the phloem sap in the swollen veins may be responsible for the higher feeding rate as well as for the occasional exudation of sap from such veins.