Biology and management of the invasive mealybug Phenacoccus peruvianus (Hemiptera: Pseudococcidae) in urban landscapes

Phenacoccus peruvianus (Hemiptera: Pseudococcidae) is an invasive mealybug of Neotropical origin, first reported in the Mediterranean Basin in Almeria (Spain) in 1999. In the following years the mealybug spread into other Mediterranean regions and has also been recorded in Portugal and France, as well as in Sicily, Corsica and the Balearic Islands. Phenacoccus peruvianus is a polyphagous species and damages economically important ornamental plants. Since this was a relatively unknown species, during the first years of invasion, the mealybug was managed by the application of chemical treatments with wide-spectrum pesticides. However, the latest European directive on pesticide use reduces or even forbids pesticide applications in a wide range of urban green areas, giving significant priority to biological control (European Parliament and Council 2009). This thesis sets the basis for introducing biological control into a P. peruvianus management program in urban landscapes, focusing on its characterization, sampling, biology and control. In order to facilitate the identification of this and other mealybug species, we characterised 33 mealybug populations infesting crops and ornamental plants in Eastern Spain, using a combination of molecular and morphological techniques. This characterisation led to the identification of ten mealybug species and made routine identification possible through DNA sequencing or the use of derived species-specific molecular tools. The sequences obtained also add to the phylogenetic knowledge of the Pseudococcidae family and provide insight into the invasion history of some species. Phenacoccus peruvianus populations were high in bougainvillea plants during spring and summer, declining to almost undetectable levels in autumn and winter. The mealybug was mainly found in bracts and there were no significant migrations between plant strata. Phenacoccus peruvianus showed a high aggregated distribution on bracts, leaves and twigs. We recommend a binomial sampling of 200 leaves and an action threshold of 55% infested leaves for IPM purposes in urban landscapes. Its most abundant natural enemies were found to be the primary parasitoids Acerophagus n. sp. near coccois and Leptomastix epona Walker (Hymenoptera: Encyrtidae). We also identified several predator species from the Anthocoridae, Coccinellidae, Chamaemyiidae, and Chrysopidae families. Phenacoccus peruvianus populations were lower during the second and third year of the survey, coinciding with an increase in the parasitoid Acerophagus sp. populations, which displaced the native L. epona. Differential female offspring and resource preemption are discussed as the main reasons for this displacement. To obtain further information on the biology of the new parasitoid Acerophagus sp. we determined some traits of its reproductive and feeding strategies. Acerophagus sp. egg load reached its maximum when it was 5 days old with almost 30 mature eggs. Phenacoccus peruvianus second and third nymphal instars and adults were suitable for parasitism and efficient encapsulation was low (10.76 ± 0.31 %). The parasitoid always preferred older instars when different host instars were available. Acerophagus sp. developed as a solitary parasitoid in the second instar and as a gregarious parasitoid in older instars (2¿4 parasitoids per host). Moreover, it reproduced parthenogenetically and all the emerged offspring were females. Immature development lasted between 20 and 22 days at 25°C and 65% HR. Under these conditions, adults lived for longer than 20 days when fed on honey, but fewer than 3 days when fed on naturally occurring sugar sources (host honeydew and Bougainvillea glabra flowers).Beltrà Ivars, A. (2014). Biology and management of the invasive mealybug Phenacoccus peruvianus (Hemiptera: Pseudococcidae) in urban landscapes [Tesis doctoral no publicada]. Universitat Politècnica de València. https://doi.org/10.4995/Thesis/10251/37233TESI

How a slow-ovipositing parasitoid can succed as a biological control agent of the invasive mealybug Phenacoccus peruvianus: implications for future classical and conservation biological control programs

[EN] Phenaccocus peruvianus Granara de Willink (Hemiptera: pseudococcidae) is an invasive mealybug that has become a pest of ornamental plants in Europe and has recently been detected in California, USA. In this work, we studied the tritrophic interaction among this mealybug, its main parasitoid Acerophagus n. sp. near coccois (Hymenoptera: Encyrtidae) and tending ants to disclose the success of this parasitoid controlling P. peruvianus. Acerophagus n. sp. near coccois accepted mealybugs for parasitism regardless of their size but did not hostfeed. We recorded three active defenses of P. peruvianus. Host handling time-consuming process that required more than 30 min. Tending ants, Lasius grandis (Hymenoptera: Encyrtidae), reduced the time spent by parasitoids in a patch and disrupted oviposition attempts. The low numbers of ants tending mealybugs colonies in Spain and France could explain why this parasitoid, with a long handling time, is an efficient biological control agent for P. peruvianus.Beltrà Ivars, A.; Soto Sánchez, AI.; Tena Barreda, A. (2015). How a slow-ovipositing parasitoid can succed as a biological control agent of the invasive mealybug Phenacoccus peruvianus: implications for future classical and conservation biological control programs. BioControl. 60(4):473-484. https://doi.org/10.1007/s10526-015-9663-6S473484604Arakelian G (2013) Bougainvillea mealybug (Phenacoccus peruvianus). Factsheet 2013. County of Los Angeles. Department of agricultural commissioner/weights and measures, USABartlett BR (1961) The influence of ants upon parasites, predators, and scale insects. Ann Entomol Soc Am 54:543–551Bartlett BR (1978) Pseudococcidae. In: Clausen CP (ed) Introduced parasites and predators of arthropod pests and weeds: a world review, 1st edn. 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The Bougainvillea mealybug Phenacoccus peruvianus, a rapid invader from South America to Europe

Τα κοκκοειδή έντομα εμφανίζονται συχνά ως εισβολείς σε νέες περιοχές. Το είδος Phenacoccus peruvianus Granara de Willink, 2007, γνωστό και ως ψευδόκοκκος της βουκαμβίλιας παρατηρήθηκε για πρώτη φορά στην Ευρώπη το 1999 στην Ισπανία (Αλμερία) και αργότερα το 2002 στην Ιταλία (Σικελία). Αρχικά το είδος είχε αναγνωριστεί ως Phenacoccus sp. Κατα- γραφές του είδους έγιναν συχνότερες και σε άλλες περιοχές της Ισπανίας (συμπεριλαμβανομέ- νων και των Βελεαρίδων νήσων), στη Μ. Βρετανία, τη Γαλλία (συμπεριλαμβανομένης και της Κορσικής), το Μονακό και την Πορτογαλία. Τα φυτά ξενιστές ήταν στις περισσότερες περι- πτώσεις του γένους Bougainvillea.Scale insects are frequent invaders of new territories. The Bougainvillea mealybug, Phenacoccus peruvianus Granara de Willink, 2007, was recorded in Europe for the first time in 1999 in Spain (Almeria) and later in 2002 in Italy (Sicily). Initially, this unknown species was identified provisionally as Phenacoccus sp. Records of this species became frequent later when it was found in other localities in Spain (including the Balearic Islands), Great Britain, France (including Corsica), Monaco, and Portugal. The host plants of this mealybug were in most cases species of Bougainvillea

Association between ants (Hymenoptera: Formicidae) and the vine mealybug (Hemiptera: Pseudococcidae) in table-grape vineyards in Eastern Spain

[EN] BACKGROUNDThe vine mealybug, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae) is a key pest of grapevine in the Mediterranean Basin. Some honeydew collecting ant species are known to increase mealybug populations in other grape-growing regions. However, there is scarce information on either the ant species present in Mediterranean vineyards or their impact on mealybugs. We conducted a study in four commercial vineyards in Eastern Spain in order to i) identify the ant species foraging on the vine canopies, ii) study the association among ant activity, vine mealybug abundance and fruit damage, and iii) test a novel method for ant management, distracting ants from guarding vine mealybugs by providing sugar dispensers. RESULTSWe recorded three ant species native to the Mediterranean foraging on the vine canopies: Lasius grandis (Forel), Pheidole pallidula (Nylander) and Plagiolepis schmitzii (Forel). The mean percentage of damaged fruits per vine was positively correlated with the number of vine mealybugs captured in traps placed at the trunk. We detected a positive but weak relationship between ant activity, vine mealybug abundance and fruit damage. The provisioning of sugar dispensers reduced the number of ants foraging on the vines by 23.4% although this reduction was not statistically significant. Vine mealybug abundance was significantly reduced (72%) after sugar provisioning. CONCLUSIONOur results suggest that the ant species native to vineyards in eastern Spain induce population increases of the vine mealybug. Moreover, the provisioning of sugars can be a valuable tool for ant management and mealybug control. (c) 2017 Society of Chemical IndustryWe are grateful to two anonymous reviewers for their comments. This research was supported by the European grants FP7-IAPP #324475 'Colbics' and FP7-IRSES #612566 'Biomodics'.Beltrà Ivars, A.; Navarro Campos, C.; Calabuig Gomar, A.; Estopa, L.; Wäckers, F.; Pekas, A.; Soto Sánchez, AI. (2017). Association between ants (Hymenoptera: Formicidae) and the vine mealybug (Hemiptera: Pseudococcidae) in table-grape vineyards in Eastern Spain. Pest Management Science. 73(12):2473-2480. https://doi.org/10.1002/ps.4640S247324807312Ramzi, M., Kaouthar, G.-L., Pompeo, S., Gaetana, M., & Agatino, R. (2017). Key scale insects (Hemiptera: Coccoidea) of high economic importance in a Mediterranean area: host plants, bio-ecological characteristics, natural enemies and pest management strategies – a review. Plant Protection Science, 53(No. 1), 1-14. doi:10.17221/53/2016-ppsDaane, K. M., Almeida, R. P. P., Bell, V. A., Walker, J. T. S., Botton, M., Fallahzadeh, M., … Zaviezo, T. (2012). Biology and Management of Mealybugs in Vineyards. 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A Rat Immobilization Model Based on Cage Volume Reduction: A Physiological Model for Bed Rest?

Bed rest has been an established treatment in the past prescribed for critically illness or convalescing patients, in order to preserve their body metabolic resource, to prevent serious complications and to support their rapid path to recovery. However, it has been reported that prolonged bed rest can have detrimental consequences that may delay or prevent the recovery from clinical illness. In order to study disuse-induced changes in muscle and bone, as observed during prolonged bed rest in humans, an innovative new model of muscle disuse for rodents is presented. Basically, the animals are confined to a reduced space designed to restrict their locomotion movements and allow them to drink and eat easily, without generating physical stress. The animals were immobilized for either 7, 14, or 28 days. The immobilization procedure induced a significant decrease of food intake, both at 14 and 28 days of immobilization. The reduced food intake was not a consequence of a stress condition induced by the model since plasma corticosterone levels –an indicator of a stress response– were not altered following the immobilization period. The animals showed a significant decrease in soleus muscle mass, grip force and cross-sectional area (a measure of fiber size), together with a decrease in bone mineral density. The present model may potentially serve to investigate the effects of bed-rest in pathological states characterized by a catabolic condition, such as diabetes or cancer

The Skeletal Muscle as an Active Player Against Cancer Cachexia

The management of cancer patients is frequently complicated by the occurrence of cachexia. This is a complex syndrome that markedly impacts on quality of life as well as on tolerance and response to anticancer treatments. Loss of body weight, wasting of both adipose tissue and skeletal muscle and reduced survival rates are among the main features of cachexia. Skeletal muscle wasting has been shown to depend, mainly at least, on the induction of protein degradation rates above physiological levels. Such hypercatabolic pattern is driven by overactivation of different intracellular proteolytic systems, among which those dependent on ubiquitin-proteasome and autophagy. Selective rather than bulk degradation of altered proteins and organelles was also proposed to occur. Within the picture described above, the muscle is frequently considered a sort of by-stander tissue where external stimuli, directly or indirectly, can poise protein metabolism toward a catabolic setting. By contrast, several observations suggest that the muscle reacts to the wasting drive imposed by cancer growth by activating different compensatory strategies that include anabolic capacity, the activation of autophagy and myogenesis. Even if muscle response is eventually ill-fated, its occurrence supports the idea that in the presence of appropriate treatments the development of cancer-induced wasting might not be an ineluctable event in tumor hosts

Heritability of symbiont density reveals distinct regulatory mechanisms in a tripartite symbiosis

Beneficial eukaryotic–bacterial partnerships are integral to animal and plant evolution. Understanding the density regulation mechanisms behind bacterial symbiosis is essential to elucidating the functional balance between hosts and symbionts. Citrus mealybugs, Planococcus citri (Risso), present an excellent model system for investigating the mechanisms of symbiont density regulation. They contain two obligate nutritional symbionts, Moranella endobia, which resides inside Tremblaya princeps, which has been maternally transmitted for 100–200 million years. We investigate whether host genotype may influence symbiont density by crossing mealybugs from two inbred laboratory-reared populations that differ substantially in their symbiont density to create hybrids. The density of the M. endobia symbiont in the hybrid hosts matched that of the maternal parent population, in keeping with density being determined either by the symbiont or the maternal genotype. However, the density of the T. princeps symbiont was influenced by the paternal host genotype. The greater dependency of T. princeps on its host may be due to its highly reduced genome. The decoupling of T. princeps and M. endobia densities, in spite of their intimate association, suggests that distinct regulatory mechanisms can be at work in symbiotic partnerships, even when they are obligate and mutualistic

Guiding Classical Biological Control of an Invasive Mealybug Using Integrative Taxonomy

The analysed sequences were deposited in Genbank under accession numbers KP771926-KP771972. Mealybug slides are available at the Polytechnic University of Valencia (Valencia, Spain). Parasitoid slides are deposited at Università degli Studi di Napoli Federico II (Portici, Italy).[EN] Delottococcus aberiae De Lotto (Hemiptera: Pseudococcidae) is a mealybug of Southern African origin that has recently been introduced into Eastern Spain. It causes severe distortions on young citrus fruits and represents a growing threat to Mediterranean citrus production. So far, biological control has proven unsatisfactory due to the absence of efficient natural enemies in Spain. Hence, the management of this pest currently relies only on chemical control. The introduction of natural enemies of D. aberiae from the native area of the pest represents a sustainable and economically viable alternative to reduce the risks linked to pesticide applications. Since biological control of mealybugs has been traditionally challenged by taxonomic misidentification, an intensive survey of Delottococcus spp. and their associated parasitoids in South Africa was required as a first step towards a classical biological control programme. Combining morphological and molecular characterization (integrative taxonomy) a total of nine mealybug species were identified in this study, including three species of Delottococcus. Different populations of D. aberiae were found on wild olive trees, in citrus orchards and on plants of Chrysanthemoides monilifera, showing intra-specific divergences according to their host plants. Interestingly, the invasive mealybug populations from Spanish orchards clustered together with the population on citrus from Limpopo Province (South Africa), sharing COI haplotypes. This result pointed to an optimum location to collect natural enemies against the invasive mealybug. A total of 14 parasitoid species were recovered from Delottococcus spp. and identified to genus and species level, by integrating morphological and molecular data. A parasitoid belonging to the genus Anagyrus, collected from D. aberiae in citrus orchards in Limpopo, is proposed here as a good biological control agent to be introduced into Spain.This work was supported by the European Union Seventh Framework Programme FP7-IRSES #269196 "IPRABIO" and FP7-IAPP #324475 "COLBICS" and FP7-IRSES #612566 "BIOMODICS". The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.Beltrà Ivars, A.; Addison, P.; Ávalos Masó, JA.; Crochard, D.; García Mari, F.; Guerrieri, E.; Giliomee, JH.... (2015). Guiding Classical Biological Control of an Invasive Mealybug Using Integrative Taxonomy. PLoS ONE. 10(6):1-14. https://doi.org/10.1371/journal.pone.0128685S11410

A rat immobilization model based on cage volume reduction: a physiological model for bed rest?

Bed rest has been an established treatment in the past prescribed for critically illness or convalescing patients, in order to preserve their body metabolic resource, to prevent serious complications and to support their rapid path to recovery. However, it has been reported that prolonged bed rest can have detrimental consequences that may delay or prevent the recovery from clinical illness. In order to study disuse-induced changes in muscle and bone, as observed during prolonged bed rest in humans, an innovative new model of muscle disuse for rodents is presented. Basically, the animals are confined to a reduced space designed to restrict their locomotion movements and allow them to drink and eat easily, without generating physical stress. The animals were immobilized for either 7, 14, or 28 days. The immobilization procedure induced a significant decrease of food intake, both at 14 and 28 days of immobilization. The reduced food intake was not a consequence of a stress condition induced by the model since plasma corticosterone levels-an indicator of a stress response- were not altered following the immobilization period. The animals showed a significant decrease in soleus muscle mass, grip force and cross-sectional area (a measure of fiber size), together with a decrease in bone mineral density. The present model may potentially serve to investigate the effects of bed-rest in pathological states characterized by a catabolic condition, such as diabetes or cancer