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      Parasitism, sexual dimorphism and effect of host size on Apocephalus attophilus offspring, a parasitoid of the leaf-cutting ant Atta bisphaerica

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          Abstract

          Atta bisphaerica (Forel) is a leaf-cutting ant that specializes on grass and causes productivity losses in sugar cane fields and pastures. Three phorid species, Apocephalus attophilus (Borgmeier), Myrmosicarius grandicornis (Borgmeier) and Eibesfeldtphora bragancai (Brown), have been found parasitizing A. bisphaerica workers. These parasitoids can reduce plant material transported into the nests and ant traffic on the trails. Therefore, phorid flies have been considered potential biological control agents for leaf-cutting ants. Here, we evaluated which parasitoid species attack the leaf-cutting ant A. bisphaerica in pasture areas of a Brazilian Savannah-Atlantic Forest ecotone, parasitism rate, effect of host size, sexual dimorphism and sex ratio of the emerged parasitoids. Four nests of A. bisphaerica were selected in pasture areas from August 2016 to August 2017, with 400 workers collected from each colony monthly. A total of 23,714 A. bisphaerica workers were collected during the study, of which 236 (0.99%) were parasitized by phorid parasitoids. Apocephalus attophilus, E. bragancai and M. grandicornis parasitized 217, 17 and 2 ants, respectively. The higher parasitism rate was found in the hottest/rainy season of the year. Non-parasitized ants survived longer than those parasitized by A. attophilus. The larval and pupal periods of this parasitoid were 2.2 ± 0.8 and 16 ± 1.4 days, respectively, and the number of pupae per parasitized ant ranged from 1 to 7. The number of A. attophilus pupae per host increased with the host head size. Likewise, the size of the adult parasitoids also increased according to the host ant. Apocephalus attophilus females were larger than males and the sex ratio (male: female) did not differ from 1: 1. Our results showed that A. attophilus would be a potential biocontrol agent of leaf-cutting ants because it produces multiple larvae per host, allowing a great production of parasitoids with short developmental time and kills the host ant faster than other phorids.

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          Most cited references 48

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          Pesticide Exposure, Safety Issues, and Risk Assessment Indicators

          Pesticides are widely used in agricultural production to prevent or control pests, diseases, weeds, and other plant pathogens in an effort to reduce or eliminate yield losses and maintain high product quality. Although pesticides are developed through very strict regulation processes to function with reasonable certainty and minimal impact on human health and the environment, serious concerns have been raised about health risks resulting from occupational exposure and from residues in food and drinking water. Occupational exposure to pesticides often occurs in the case of agricultural workers in open fields and greenhouses, workers in the pesticide industry, and exterminators of house pests. Exposure of the general population to pesticides occurs primarily through eating food and drinking water contaminated with pesticide residues, whereas substantial exposure can also occur in or around the home. Regarding the adverse effects on the environment (water, soil and air contamination from leaching, runoff, and spray drift, as well as the detrimental effects on wildlife, fish, plants, and other non-target organisms), many of these effects depend on the toxicity of the pesticide, the measures taken during its application, the dosage applied, the adsorption on soil colloids, the weather conditions prevailing after application, and how long the pesticide persists in the environment. Therefore, the risk assessment of the impact of pesticides either on human health or on the environment is not an easy and particularly accurate process because of differences in the periods and levels of exposure, the types of pesticides used (regarding toxicity and persistence), and the environmental characteristics of the areas where pesticides are usually applied. Also, the number of the criteria used and the method of their implementation to assess the adverse effects of pesticides on human health could affect risk assessment and would possibly affect the characterization of the already approved pesticides and the approval of the new compounds in the near future. Thus, new tools or techniques with greater reliability than those already existing are needed to predict the potential hazards of pesticides and thus contribute to reduction of the adverse effects on human health and the environment. On the other hand, the implementation of alternative cropping systems that are less dependent on pesticides, the development of new pesticides with novel modes of action and improved safety profiles, and the improvement of the already used pesticide formulations towards safer formulations (e.g., microcapsule suspensions) could reduce the adverse effects of farming and particularly the toxic effects of pesticides. In addition, the use of appropriate and well-maintained spraying equipment along with taking all precautions that are required in all stages of pesticide handling could minimize human exposure to pesticides and their potential adverse effects on the environment.
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            Sex ratio evolution in a variable environment.

            We develop a natural selection model for sex ratio control in a spatially variable environment. Predictions of sex ratio alteration as a function of environmental change are tested in laboratory experiments with two parasitic wasps. Field data from a variety of other organisms also support the model. Finally, we discuss possibilities and difficulties for testing this type of evolutionary model.
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              Resource acquisition, allocation, and utilization in parasitoid reproductive strategies.

              Parasitoids display remarkable inter- and intraspecific variation in their reproductive and associated traits. Adaptive explanations have been proposed for many of the between-trait relationships. We present an overview of the current knowledge of parasitoid reproductive biology, focusing on egg production strategies in females, by placing parasitoid reproduction within physiological and ecological contexts. Thus, we relate parasitoid reproduction both to inter- and intraspecific patterns of nutrient allocation, utilization, and acquisition, and to key aspects of host ecology, specifically abundance and dispersion pattern. We review the evidence that resource trade-offs underlie several key intertrait correlations and that reproductive and feeding strategies are closely integrated at both the physiological and the behavioral levels. The idea that parasitoids can be divided into capital-breeders or income-breeders is no longer tenable; such terminology is best restricted to the females' utilization of particular nutrients.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: Methodology
                Role: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: ResourcesRole: SupervisionRole: Validation
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                3 December 2018
                2018
                : 13
                : 12
                Affiliations
                [1 ] Departament of Entomology, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
                [2 ] Institute of Biological Sciences, Federal University of Viçosa Campus, Florestal, Florestal, Minas Gerais, Brazil
                [3 ] Departament of Zoology, University of São Paulo, São Paulo, São Paulo, Brazil
                [4 ] Postgraduate Program in Environmental Sciences, Federal University of Mato Grosso C ampus, Sinop, Sinop, Mato Grosso, Brazil
                Arizona State University, UNITED STATES
                Author notes

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

                Article
                PONE-D-18-08450
                10.1371/journal.pone.0208253
                6277103
                30507956
                © 2018 Farder-Gomes et al

                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: 3, Tables: 0, Pages: 10
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100002322, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004901, Fundação de Amparo à Pesquisa do Estado de Minas Gerais;
                Award ID: EDITAL 01/2014 - DEMANDA UNIVERSAL-FAPEMIG - PROCESSO N. : CAG - APQ-01842-14
                Award Recipient :
                The research was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Fundação de Amparo à Pesquisa do Estado de Minas Gerais (EDITAL 01/2014 - DEMANDA UNIVERSAL-FAPEMIG - PROCESSO N. : CAG - APQ-01842-14) and Conselho Nacional de Desenvolvimento Científico e Tecnológico. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Ants
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Social Sciences
                Sociology
                Social Systems
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Pupae
                Biology and Life Sciences
                Population Biology
                Population Metrics
                Sex Ratio
                Biology and Life Sciences
                Agriculture
                Pest Control
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Biology and Life Sciences
                Psychology
                Behavior
                Animal Behavior
                Animal Sociality
                Social Sciences
                Psychology
                Behavior
                Animal Behavior
                Animal Sociality
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Sociality
                Custom metadata
                All relevant data are within the paper.

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