No CrossRef data available.
Article contents
Bioecology of Anagyrus saccharicola (Hymenoptera: Encyrtidae), a parasitoid of the pink sugarcane mealybug Saccharicoccus sacchari (Hemiptera: Pseudococcidae)
Published online by Cambridge University Press: 21 December 2020
Abstract
Parasitoids can be used as biological agents of pest control. Anagyrus saccharicola Timberlake (Hymenoptera: Encyrtidae) is a parasitoid of the pink sugarcane mealybug Saccharicoccus sacchari (Cockerell) (Hemiptera: Pseudococcidae). Although this mealybug is present in all sugarcane-producing countries, there is limited information regarding this pest and its parasitoid. Aiming to elucidate information on bioecological parameters of A. saccharicola, were evaluated the survival of parasitoid females and males at three temperatures, the host preference of the parasitoid, and the fecundity and longevity of the host. In addition, the parasitism rate of A. saccharicola was estimated based on three factors, feeding, mating, and time. Survival was evaluated at 20, 25, and 30°C. Host preference was conducted on 15-, 20-, and 30-day-old mealybugs. And the parasitism rate was evaluated in fed and unfed, mated and unmated parasitoids and with 24 h and newly emerged. The temperature of 20°C was the most favorable for parasitoid survival. Parasitism occurred at all evaluated ages of the mealybug; however, the preference was for those that were 30-days-old. The parasitized mealybugs longevity was approximately 8 additional days after parasitization, and non-parasitized mealybugs lived for an additional 20 days for mealybugs aged 30 and 20 days at the outset of the tests, and a further 13 days for the 15 days. Feeding and mating after 24 h of emergence resulted in a higher parasitism rate. These findings can contribute to more efficient rearing of A. saccharicola and in the planning of the biological control of S. sacchari in the integrated pest management programs.
- Type
- Research Paper
- Information
- Copyright
- Copyright © The Author(s), 2020. Published by Cambridge University Press
References
Abd-Rabou, S (2002) Efficacy of the imported parasitoid, Anagyrus saccharicola (Hymenoptera: Encyrtidae) for the biological control of Saccharicoccus sacchari (Hemiptera: Pseudococcidae) attacking sugar cane in Egypt. Sugar Cane International 5, 24–26.Google Scholar
Abd-Rabou, S (2007) Biological control of Saccharicoccus sacchari (Coccoidea: Pseudococcidae) on sugar cane in Egypt using imported and indigenous natural enemies. pp. 277–284 in Proceedings of the XI International Symposium on Scale Insect Studies, Oeiras, 2007 Portugal, International Symposium on Scale Insect Studies.Google Scholar
Alam, MM (1972) The establishment of Anagyrus saccharicola Timb. [Hymenoptera: Encyrtidae] in Barbados, West Indies, against the sugarcane mealybug, Saccharicoccus sacchari (Ckll.) (Hemiptera: Coccidae). Entomophaga 17, 357–363.CrossRefGoogle Scholar
Bahar, MH, Soroka, JJ and Dosdall, LM (2012) Constant versus fluctuating temperatures in the interactions between Plutella xylostella (Lepidoptera: Plutellidae) and its larval parasitoid Diadegma insulare (Hymenoptera: Ichneumonidae). Environmental Entomology 41, 1653–1661.CrossRefGoogle Scholar
Barbosa, MHP, Resende, MDV, Dias, LAS, Barbosa, GVS, Oliveira, RA, Peternelli, LA and Daros, E (2012) Genetic improvement of sugar cane for bioenergy: the Brazilian experience in network research with RIDESA. Crop Breeding and Applied Biotechnology S2, 87–98.CrossRefGoogle Scholar
Beardsley, JW (1959) Observations on sugar cane mealybugs in Hawaii. pp. 954–960 in Proceedings of the tenth Congress International Society of Sugar Cane Technologists, 1959 Hawaii, International Society of Sugar Cane Technologists.Google Scholar
Beardsley, JW (1962) Notes on the biology of the pink sugar cane mealybug, Saccharicoccus sacchari (Cockerell), in Hawaii (Homoptera: Pseudococcidae). pp. 55–59 in Proceedings of the tenth Pacific Science Congress organized by the Hawaiian Entomological Society, Honolulu, 21 Aug–6 Sept 1962 Hawaii, Hawaiian Entomological Society.Google Scholar
Borges Filho, RC, Sturza, VS, Nava, DE and Guedes, JVC (2016) Bioecologia e manejo de pragas. In Silva, SDA, Montero, CRS, Santos, RC and Nava (eds), Sistema de produção da cana-de-açúcar para o Rio Grande do Sul. Pelotas: EMBRAPA Clima Temperado, pp. 75–97.Google Scholar
Botelho, PSM, Parra, JRP, Chagas Neto, JF and Oliveira, CPB (1999) Associação do parasitóide de ovos Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae) e do parasitóide larval Cotesia flavipes (Cam.) (Hymenoptera: Braconidae) no controle de Diatraea saccharalis (Fabr.) (Lepidoptera: Crambidae) em cana-de-açúcar. Anais da Sociedade Entomológica do Brasil 28, 491–496.CrossRefGoogle Scholar
Box, HE (1953) List of Sugar-Cane Insects. A Synonymic Catalogue of the Sugar-Cane Insects and Mites of the World, and of Their Insect Parasites and Predators, Arranged Systematically. London: CIE.Google Scholar
Brinkman, MLJ, da Cunha, MP, Heijnen, S, Wicke, B, Guilhoto, JJM, Walter, A, Faaij, APC and van der Hilst, F (2018) Interregional assessment of socio-economic effects of sugarcane ethanol production in Brazil. Renewable and Sustainable Energy Reviews 88, 347–362.CrossRefGoogle Scholar
Carver, M, Inkerman, PA and Ashbolt, NJ (1987) Anagyrus (Hymenoptera: Encyrtidae) and other associated with (Cockerell) (Homoptera: Pseudococcidae) in Australia. Australian Journal of Entomology 26, 367–368.CrossRefGoogle Scholar
Cerri, CC (2007) Sequestro de Carbono (Carbon Sequestration). Presentation at II Encontro de Tendências em Biocombustíveis, na Área Internacional, Petrobrás, Rio de Janeiro.Google Scholar
Chong, JH and Oetting, RD (2006) Influence of temperature, nourishment, and storage period on the longevity and fecundity of the mealybug parasitoid, Anagyrus sp. nov. nr. sinope Noyes and Menezes (Hymenoptera: Encyrtidae). Environmental Entomology 35, 1198–1207.CrossRefGoogle Scholar
Cloutier, C, Lévesque, CA, Eaves, DM and Mackauer, M (1991) Maternal adjustment of sex ratio in response to host size in the aphid parasitoid Ephedrus californicus. Canadian Journal of Zoology 69, 1489–1495.CrossRefGoogle Scholar
CONAB (2020) Acompanhamento da safra brasileira de cana-de-açúcar. p. 10. Brasília, Brasil.Google Scholar
Cooper, DJ and Zhang, QY (1992) Virus-like particles in the pink sugarcane mealybug, Saccharicoccus sacchari. Journal of Invertebrate Pathology 60, 206–207.CrossRefGoogle Scholar
Cruz, M, Peronti, AL, Martinelli, N, Costa, V, Ignácio, G and Almeida, L (2019) Complex of natural enemies associated with scale insects (Hemiptera: Coccomorpha) on sugarcane in Brazil. Journal of Agricultural Science 11, 160–175.CrossRefGoogle Scholar
Cuny, MAC, Traine, J, Bustos-Segura, C and Benrey, B (2019) Host density and parasitoid presence interact and shape the outcome of a tritrophic interaction on seeds of wild lima bean. Scientific Reports 9, 1–9.CrossRefGoogle ScholarPubMed
Davies, AP, Ceballo, FA and Walter, GH (2004) Is the potential of Coccidoxenoides perminutus, a mealybug parasitoid, limited by climatic or nutritional factors? Biological Control 31, 181–188.CrossRefGoogle Scholar
Fernández, F and Sharkey, MJ (2006) Introducción a los Hymenoptera de la región Neotropical. Bogotá: Sociedad Colombiana de Entomología y Universidad Nacional de Colombia.Google Scholar
Franke, IH, Fegan, M, Hayward, C, Leonard, G, Stackebrandt, E and Sly, LI (1999) Description of Gluconacetobacter sacchari sp. nov., a new species of acetic acid bacterium isolated from the leaf sheath of sugar cane and from the pink sugar-cane mealy bug. International Journal of Systematic Bacteriology 49, 1681–1693.Google ScholarPubMed
Gallo, D, Nakano, O, Silveira Neto, S, Carvalho, RPL, Batista, GC, Berti Filho, E, Parra, JRP, Zucchi, RA, Alves, SB, Vendramin, JD, Marchini, LC, Lopes, JRS and Omoto, C (2002) Entomologia Agrícola. Piracicaba: FEALQ.Google Scholar
García Morales, M, Denno, BD, Miller, DR, Miller, GL, Ben-Dov, Y and Hardy, NB (2016) Scalenet: a literature-based model of scale insect biology and systematics. Available at http://scalenet.info/catalogue/Saccharicoccus%20sacchari/ (Accessed 13 March 2020).Google Scholar
Géneau, CE, Wäckers, FL, Luka, H, Daniel, C and Balmer, O (2012) Selective flowers to enhance biological control of cabbage pests by parasitoids. Basic and Applied Ecology 13, 85–93.CrossRefGoogle Scholar
Gibson, GAP, Huber, IT and Woolley, JB (1997) Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa, Ontario, Canada: NRC Research Press.Google Scholar
Girón, KP, Lastra, LAB, Gómez, LAL and Mesa, NCC (2005) Observations on the biology and natural enemies of Saccahricoccus sacchari y Pulvinaria poselongata, two homopterans associated with the crazy ant in sugar cane. Revista Colombiana de Entomología 31, 29–35.Google Scholar
Godfray, HCJ and Shimada, M (1999) Parasitoids as model organisms for ecologists. Population Ecology 41, 3–10.CrossRefGoogle Scholar
Goldemberg, J, Coelho, ST and Guardabassi, P (2008) The sustainability of ethanol production from sugarcane. Energy Policy 36, 2086–2097.CrossRefGoogle Scholar
Guzo, D and Stoltz, DB (1987) Observations on cellular immunity and parasitism in the tussock moth. Journal of Insect Physiology 33, 19–31.CrossRefGoogle Scholar
Hance, T, van Baaren, J, Vernon, P and Boivin, G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annual Review of Entomology 52, 107–126.CrossRefGoogle Scholar
Heimpel, GE and Jervis, MA (2005) Does floral nectar improve biological control by parasitoids. In Wackers, FL, Van Rijn, PCJ and Bruin, J (eds), Plant-provided Food for Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge: Cambridge University Press, pp. 267–304.CrossRefGoogle Scholar
Inkerman, P.A., Ashbol, N.J., Carver, M. and Williams, D. J. (1986) Observations on the pink sugarcane mealybug, Saccharicoccus sacchari (Cockerell) in Australia (Homoptera: Pseudococcidae). pp. 612–618 in Proceedings of the 19th Congress International Society of Sugar Cane Technologists, 1986 Indonesia, International Society of Sugar Cane Technologists.Google Scholar
Islam, KS and Copland, MJW (1997) Host preference and progeny sex ratio in a solitary koinobiont mealybug endoparasitoid, Anagyrus pseudococci (Girault), in response to its host stage. Biocontrol Science and Technology 7, 449–456.CrossRefGoogle Scholar
Islam, KS and Copland, MJW (2000) Influence of egg load and oviposition time interval on the host discrimination and offspring survival of Anagyrus pseudococci (Hymenoptera: Encyrtidae), a solitary endoparasitoid of citrus mealybug, Planococcus citri (Hemiptera: Pseudococcidae). Bulletin of Entomological Research 90, 69–75.CrossRefGoogle Scholar
Jervis, MA and Copland, MJW (1996) The life cycle. In Jervis, MA and Kidd, NAC (eds), Insect Natural Enemies, Practical Approaches to Their Study and Evaluation. London: Chapman & Hall, pp. 63–160.CrossRefGoogle Scholar
Jervis, MA, Kidd, NAC, Fitton, MG, Huddleston, T and Dawah, HA (1993) Flower-visiting by hymenopteran parasitoids. Journal of Natural History 27, 67–105.CrossRefGoogle Scholar
King, BH (1989) Host-size-dependent sex ratios among parasitoid wasps: does host growth matter? Oecologia 78, 420–426.CrossRefGoogle ScholarPubMed
Lockhart, BEL, Autrey, LJC and Comstock, JC (1992) Partial purification and serology of sugarcane mild mosaic virus, a mealybug-transmitted closterolike virus. Phytopathology 82, 691–695.CrossRefGoogle Scholar
Maga, D, Thonemann, N, Hiebel, M, Sebastião, D, Lopes, TF, Fonseca, C and Gírio, F (2019) Comparative life cycle assessment of first- and second-generation ethanol from sugarcane in Brazil. International Journal of Life Cycle Assessment 24, 266–280.CrossRefGoogle Scholar
Marcari, MA, Souza Rolim, G and Oliveira Aparecido, LE (2015) Agrometeorological models for forecasting yield and quality of sugarcane. Australian Journal of Crop Science 9, 1049.Google Scholar
Matioli, CS (1998) Irrigação suplementar de cana-de-açúcar: modelo de análise de decisão para o Estado de São Paulo (Sugarcane suplementar irrigation: a decision analysis model to São Paulo state). Piracicaba, SP, Tese (Doutorado)-Escola Superior de Agricultura ‘Luiz de Queiroz’, Universidade de São Paulo.Google Scholar
Mozaddedul, HN and Copland, MJW (2002) Study on fecundity, reproductive rate, intrinsic rate of increase and effects diets on adult longevity, of a long-tailed mealy bug, Pseudococcus longispinus (Torgioni-Tozzetti) parasitoid, Leptomastix nr. Pakistan Journal of Biological Sciences 5, 923–930.CrossRefGoogle Scholar
Müller, CB, Adriaanse, ICT, Belshaw, R and Godfray, HCJ (1999) The structure of an aphid–parasitoid community. Journal of Animal Ecology 68, 346–370.CrossRefGoogle Scholar
Nava, DE, Pinto, AS and Silva, SDA (2009) Controle biológico da broca da cana-de-açúcar. Pelotas: EMBRAPA Clima Temperado, p. 28.Google Scholar
Noyes, JS (2000) Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 1. The subfamily Tetracneminae, parasitoids of mealybugs (Homoptera: Pseudococcidae). Gainesville: The American Entomological Institute.Google Scholar
Parra, JRP, Botelho, PSM, Corrêa-Ferreira, BS and Bento, JMS (2002) Controle biológico: terminologia. São Paulo: Manole.Google Scholar
Parra, JRP, Botelho, PSM and Pinto, AS (2014) Biological control of pests as a key component for sustainable sugarcane production. In Cortez, LAB (ed.), Sugarcane Bioethanol – R&D for Productivity and Sustainability. São Paulo: Edgard Blücher, pp. 441–450.Google Scholar
Rae, DJ (1993) A method for discrimination between instars of Saccharicoccus sacchari (Cockerell) (Hemiptera: Pseudococcidae). Australian Journal of Entomology 32, 249–252.CrossRefGoogle Scholar
Rae, DJ and De'Ath, G (1991) Influence of constant temperature on development, survival and fecundity of sugarcane mealybug, Saccharicoccus sacchari (Cockerell) (Hemiptera: Pseudococcidae). Australian Journal of Zoology 39, 459–472.CrossRefGoogle Scholar
Rajendra, A (1974) The biology and control of Saccharicoccus sacchari Ckll. (Hom: Pseudococcidae) the pink mealy bug of sugar cane in Sri Lanka. Ceylon Journal of Science, Biological Sciences 11, 23–28.Google Scholar
Romo, CM and Tylianakis, JM (2013) Elevated temperature and drought interact to reduce parasitoid effectiveness in suppressing hosts. PLoS ONE 8, e58136.CrossRefGoogle ScholarPubMed
Sagarra, LA, Vincent, C and Stewart, RK (2000) Fecundity and survival of Anagyrus kamali (Hymenoptera: Encyrtidae) under different feeding and storage temperature conditions. European Journal of Entomology 97, 177–182.CrossRefGoogle Scholar
Sagarra, LA, Vincent, C and Stewart, RK (2001) Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bulletin of Entomological Research 91, 363–367.CrossRefGoogle Scholar
Sagarra, LA, Vincent, C and Stewart, RK (2002) Impact of mating on Anagyrus kamali Moursi (Hym., Encyrtidae) lifetime fecundity, reproductive longevity, progeny emergence and sex ratio. Journal of Applied Entomology 126, 400–404.CrossRefGoogle Scholar
Salama, HS and Rizk, AM (1969) Composition of the honey dew in the mealy bug, Saccharicoccus sacchari. Journal of Insect Physiology 15, 1873–1875.CrossRefGoogle Scholar
Sangle, PM, Satpute, SB, Khan, FS and Rode, NS (2015) Impact of climate change on insects. Trends in Biosciences 8, 3579–3582.Google Scholar
Shukla, SK, Solomon, S, Sharma, L, Jaiswal, VP, Pathak, AD and Singh, P (2019) Green technologies for improving cane sugar productivity and sustaining soil fertility in sugarcane-based cropping system. Sugar Tech 21, 186–196.CrossRefGoogle Scholar
Silva, VP, Garcia, M and Botton, M (2017) Biology of Blepyrus clavicornis (Compere) (Hymenoptera: Encyrtidae), a parasitoid of Pseudococcus Viburni (Signoret) (Hemiptera: Pseudococcidae). Revista Brasileira de Entomologia 61, 257–261.CrossRefGoogle Scholar
Slansky, F Jr (1978) Utilization of energy and nitrogen by larvae of the imported cabbageworm, Pieris rapae, as affected by parasitism by Apanteles glomeratus. Environmental Entomology 7, 179–185.CrossRefGoogle Scholar
Souza, IL, Marucci, RC, Silveira, LCP, de Paulo, NCP and Lee, JC (2018) Effects of marigold on the behavior, survival and nutrient reserves of Aphidius platensis. BioControl 63, 543–553.CrossRefGoogle Scholar
Stapel, JO, Cortesero, AM, De Moraes, CM, Tumlinson, JH and Lewis, WJ (1997) Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environmental Entomology 26, 617–623.CrossRefGoogle Scholar
Tabadkani, SM, Ashouri, A, Rahimi-Alangi, V and Fathi-Moghaddam, M (2012) When to estimate sex ratio in natural populations of insects? A study on sex ratio variations of gall midges within a generation. Entomological Science 16, 54–59.CrossRefGoogle Scholar
Takano, S and Takasu, K (2019) Food deprivation increases reproductive effort in a parasitoid wasp. Biological Control 133, 75–80.CrossRefGoogle Scholar
Timberlake, PH (1932) Three new parasitic Hymenoptera from the Indo-Malayan region. Proceedings of the Hawaiian Entomological Society 8, 153–162.Google Scholar
Torres, JB, Zanuncio, JC, Cecon, PR and Gasperazzo, WL (1996) Parasitismo de ovos de Podisus nigrispinus (Dallas) em áreas de liberação. Anais da Sociedade Entomológica do Brasil 25, 465–473.CrossRefGoogle Scholar
Torres, JB, Musolin, DL and Zanuncio, JC (2002) Thermal requirements and parasitism capacity of Trissolcus brochymenae (Ashmead) (Hymenoptera: Scelionidae) under constant and fluctuating temperatures, and assessment of development in field conditions. Biocontrol Science and Technology 12, 583–593.CrossRefGoogle Scholar
Trail, DRS (1980) Behavioral interactions between parasites and hosts: host suicide and the evolution of complex life cycles. The American Naturalist 116, 77–91.Google Scholar
Van Lenteren, JC (2000) A greenhouse without pesticides: fact or fantasy? Crop Protection 19, 375–384.CrossRefGoogle Scholar
Van Lenteren, JC and Bueno, VHP (2003) Augmentative biological control of arthropods in Latin America. BioControl 48, 123–139.CrossRefGoogle Scholar
Wäckers, FL (2001) A comparison of nectar- and honeydew sugars with respect to their utilization by the hymenopteran parasitoid Cotesia glomerata. Journal of Insect Physiology 47, 1077–1084.CrossRefGoogle ScholarPubMed
Wang, XG, Serrato, MA, Son, Y, Walton, VM, Hogg, BN and Daane, KM (2018) Thermal performance of two indigenous pupal parasitoids attacking the invasive Drosophila suzukii (Diptera: Drosophilidae). Environmental Entomology 47, 764–772.CrossRefGoogle Scholar
Willcocks, FC (1925) The Insects and Related Pests of Egypt. Cairo: Sultanic Agricultural Society.Google Scholar
Wyckhuys, KAG, Hughes, AC, Buamas, C, Johnson, AC, Vasseur, L, Reymondin, L, Deguine, JP and Sheil, D (2019) Biological control of an agricultural pest protects tropical forests. Communications Biology 2, 1–8.CrossRefGoogle ScholarPubMed
Yadav, T, Baloda, AS and Jakhar, B (2019) Impact of climate changes on insect pest and integrated pest management: a review. Journal of Entomology and Zoology Studies 7, 1150–1156.Google Scholar
Yang, J and Sadof, CS (1995) Variegation in Coleus blumei and the life history of citrus mealybug (Homoptera: Pseudococcidae). Environmental Entomology 24, 1650–1655.CrossRefGoogle Scholar
Zhang, YB, Zhang, GF, Liu, WX and Wan, FH (2019) Variable temperatures across different stages have novel effects on behavioral response and population viability in a host-feeding parasitoid. Scientific Reports 9, 1–10.Google Scholar
Zu, GH, Zhang, X, Li, CD and Zhang, YZ (2018) A new species of Anagyrus (Hymenoptera, Encyrtidae) from Malaysia, parasitoid of Lanceacoccus sp. (Hemiptera, Pseudococcidae). Journal of Hymenoptera Research 65, 141–148.CrossRefGoogle Scholar