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      Guiding Classical Biological Control of an Invasive Mealybug Using Integrative Taxonomy

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          Abstract

          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.

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          Most cited references 15

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          Integrative taxonomy: a multisource approach to exploring biodiversity.

          Good alpha taxonomy is central to biology. On the basis of a survey of arthropod studies that used multiple disciplines for species delimitation, we evaluated the performance of single disciplines. All included disciplines had a considerable failure rate. Rigor in species delimitation can thus be increased when several disciplines chosen for complementarity are used. We present a flexible procedure and stopping rule for integrative taxonomy that uses the information from different disciplines separately. Disagreement among disciplines over the number and demarcation of species is resolved by elucidating and invoking evolutionary explanations for disagreement. With the identification of further promising study organisms and of new questions for in-depth analysis, evolutionary biology should profit from integrative taxonomy. An important rationale is clarity in researcher bias in the decision-making process. The success of integrative taxonomy will further increase through methodological progress, taxonomic training of evolutionary biologists, and balanced resource allocation.
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            Biological identifications through DNA barcode

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              Skeletal muscle amino acid transporter expression is increased in young and older adults following resistance exercise.

              Amino acid transporters and mammalian target of rapamycin complex 1 (mTORC1) signaling are important contributors to muscle protein anabolism. Aging is associated with reduced mTORC1 signaling following resistance exercise, but the role of amino acid transporters is unknown. Young (n = 13; 28 ± 2 yr) and older (n = 13; 68 ± 2 yr) subjects performed a bout of resistance exercise. Skeletal muscle biopsies (vastus lateralis) were obtained at basal and 3, 6, and 24 h postexercise and were analyzed for amino acid transporter mRNA and protein expression and regulators of amino acid transporter transcription utilizing real-time PCR and Western blotting. We found that basal amino acid transporter expression was similar in young and older adults (P > 0.05). Exercise increased L-type amino acid transporter 1/solute-linked carrier (SLC) 7A5, CD98/SLC3A2, sodium-coupled neutral amino acid transporter 2/SLC38A2, proton-assisted amino acid transporter 1/SLC36A1, and cationic amino acid transporter 1/SLC7A1 mRNA expression in both young and older adults (P < 0.05). L-type amino acid transporter 1 and CD98 protein increased only in younger adults (P < 0.05). eukaryotic initiation factor 2 α-subunit (S52) increased similarly in young and older adults postexercise (P < 0.05). Ribosomal protein S6 (S240/244) and activating transcription factor 4 nuclear protein expression tended to be higher in the young, while nuclear signal transducer and activator of transcription 3 (STAT3) (Y705) was higher in the older subjects postexercise (P < 0.05). These results suggest that the rapid upregulation of amino acid transporter expression following resistance exercise may be regulated differently between the age groups, but involves a combination of mTORC1, activating transcription factor 4, eukaryotic initiation factor 2 α-subunit, and STAT3. We propose an increase in amino acid transporter expression may contribute to enhanced amino acid sensitivity following exercise in young and older adults. In older adults, the increased nuclear STAT3 phosphorylation may be indicative of an exercise-induced stress response, perhaps to export amino acids from muscle cells.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                5 June 2015
                2015
                : 10
                : 6
                Affiliations
                [1 ]Institut Agroforestal Mediterrani, Universitat Politècnica de València, València, Spain
                [2 ]Department of Conservation Ecology and Entomology, Stellenbosch University, Stellenbosch, South Africa
                [3 ]INRA, Univ. Nice Sophia Antipolis, CNRS, UMR 1355–7254 Institut Sophia Agrobiotech, 06900 Sophia Antipolis, France
                [4 ]Istituto per la Protezione Sostenibile delle Piante, Consiglio Nazionale delle Ricerche, Portici, Italy
                [5 ]Centre for Invasion Biology, Department of Botany & Zoology, Stellenbosch University, Stellenbosch, South Africa
                University of Pretoria, SOUTH AFRICA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AB PA FG JG TM CN AS. Performed the experiments: AB JA DC EG JG CN FP. Analyzed the data: AB TM FP AS. Contributed reagents/materials/analysis tools: PA EG JG TM FP. Wrote the paper: AB FP EG. Revised the text: PA FG JG TM CN AS.

                [¤]

                Current address: R&D Department, Biobest Belgium N.V., Westerlo, Belgium

                Article
                PONE-D-15-07628
                10.1371/journal.pone.0128685
                4457817
                26047349

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

                Page count
                Figures: 1, Tables: 4, Pages: 14
                Product
                Funding
                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.
                Categories
                Research Article
                Custom metadata
                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).

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