PREDATORY EFFECT AND SELECTIVITY OF PREY OF NOTONECTA PERUVIANA (HEMIPTERA: NOTONECTIDAE) ON THE LARVAL CONTROL OF MOSQUITOES (DIPTERA: CULICIDAE)
DOI:
https://doi.org/10.4257/oeco.2022.2601.04Keywords:
Biocontrol, predators, predatory capacity, prey consumedAbstract
The larval stage of culicid mosquitoes are the main food resource of notonectides in aquatic systems. Prey alternation and abundance can significantly affect predator-prey interaction and functional response (FR). We evaluated the effect of predation and prey selectivity of Notonecta peruviana in fourth-stage larvae (F1) of Aedes aegypti and Culex quinquefasciatus at different densities and two test systems: one prey and the combination of both (ratio 1: 1). We used the FR protocol to measure predation and the Manly preference index () to evaluate the selectivity of prey, in a CRD experimental design. N. peruviana generated type II RF (“concave model”) of greater impact in larvae of Ae. aegypti (p ≤ 0.01). Predation capacity was similar in both of the prey, 17 ± 4 larvae / day in Cx. quinquefasciatus and 21 ± 4 in Ae. aegypti. The attack coefficient (a), turned out to be similar for both prey species in both test systems and the handling time (Th) was lower for Ae. aegypti than for Culex. Notonecta peruviana demonstrated selectivity for larvae of Ae. aegypti especially at the highest densities (≥ 0.5), attributed to the inefficient anti depredation response, active mobility and smaller size compared to those of Cx. quinquefasciatus. The FR demonstrated the success of N. peruviana in the larval control of culicid mosquitoes, prioritizing the type of prey; thus, promoting the need for its applicability in the field.
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References
Ayres, C. F. J. 2016. Identification of Zika virus vectors and implications for control. Lancet Infectious Diseases, 16(3), 278–279. DOI: 10.1016/S1473-3099(16)00073-6
Benelli, G., Jeffries, C. L., & Walker, T. 2016. Biological Control of Mosquito Vectors: Past, Present, and Future. Insects, 7(4), 52. DOI: 10.3390/insects7040052
Blaustein, L., Kotler, B., & Ward, D. 2008. Direct and indirect effects of a predatory backswimmer (Notonecta maculata) on community structure of desert temporary pools. Ecological Entomology, 20(4), 311–318. DOI: 10.1111/j.1365-2311.1995.tb00462.x
Brackenbury, J. 2000. Locomotory modes in the larva and pupa of Chironomus plumosus (Diptera, Chironomidae). Journal of Insect Physiology, 46(12), 1517–1527. DOI: 10.1016/S0022-1910(00)00079-2
Buxton, M., Cuthbert, R., Dalu, T., Nyamukondiwa, C., & Wasserman, R. 2020a. Complementary impacts of heterospecific predators facilitate improved biological control of mosquito larvae. Biological Control, 144, 104216. DOI: 10.1016/j.biocontrol.2020.104216
Buxton, M., Cuthbert, R. N., Dalu, T., Nyamukondiwa, C., & Wasserman, R. J. 2020b. Predator density modifies mosquito regulation in increasingly complex environments. Pest Management Science, 76(6), 2079–2086. DOI: 10.1002/ps.5746
Cabezas, C., Fiestas, V., García-Mendoza, M., Palomino, M., Mamani, E., & Donaires, F. 2015. Dengue en el Perú: a un cuarto de siglo de su reemergencia. Revista Peruana de Medicina Experimental y Salud. Pública, 32(1), 146–156. DOI: 10.17843/rpmesp.2015.321.1587
Chandrasegaran, K., Singh, A., Laha, M., & Quader, S. 2017. Playing it safe? Behavioural responses of mosquito larvae encountering a fish predator. Ethology Ecology & Evolution, 30(1), 1–18. DOI: 10.1080/03949370.2017.1313785
Chesson, J., 1989. The effect of alternative prey on the functional response of Notonecta hoffmani. Ecology 70(5), 1227–1235. DOI: 10.2307/1938180
Consoli, R. A. G. B., & de Oliveira, R. L. 1994. Principais mosquitos de importância sanitária no Brasil. Rio de Janeiro: Editora FIOCRUZ: p. 228.
Cuthbert, R. N., Dalu, T., Wasserman, R. J., Callaghan, A., Weyl, O. L. F., & Dick, J. T. A. 2019. Using functional responses to quantify notonectid predatory impacts across increasingly complex environments. Acta Oecologica, 95, 116–119. DOI: 10.1016/j.actao.2018.11.004
Dalal, A., Cuthbert, R., Dick, J., & Gupta, S. 2019a. Prey preferences of notonectids towards larval mosquitoes across prey ontogeny and search area. Pest Management Science, 76 (2):609-616. DOI: 10.1002/ps.5556
Dalal, A., Cuthbert, R. N., Dick, J. T., & Gupta, S. 2019b. Water depth-dependent notonectid predatory impacts across larval mosquito ontogeny. Pest Management Science, 75(10), 2610–2617. DOI: 10.1002/ps.5368
Dick, J., Gallagher, K., Avlijas, S., Clarke, H., Lewis, S., Leung, S., Minchin, D., Caffrey, J., Alexander, M., Maguire, C., Harrod, C., Reid, N., Haddaway, N., Farnsworth, K., Penk, M., & Ricciardi, A. 2013. Ecological impacts of an invasive predator explained and predicted by comparative functional responses. Biological Invasions, 15, 837–846. DOI: 10.1007/s10530-012-0332-8
Domínguez, E., & Fernández, H. R. (Eds.). 2009. Macroinvertebrados bentónicos sudamericanos: sistemática y biología. Tucumán: Fundación Miguel Lillo: p. 654.
Espinoza, M., Cabezas, C., & Ruiz, J. 2005. Un Acercamiento al conocimiento de la fiebre Amarilla en el Perú. Revista Peruana de Medicina Experimental y Salud. Pública, 22(4), 308–315.
Fay, R., & Eliason, D. 1966. A preferred oviposition site as a surveillance method for Aedes aegypti. Mosquito News, 26(4), 531–535.
Fernández-Arhex, V., & Corley, J.C. 2004. La respuesta funcional: una revisión y guía experimental. Ecología Austral, 14(1), 83–93.
Fischer, S., Pereyra, D., & Fernández, L. 2012. Predation ability and non-consumptive effects of Notonecta sellata (Heteroptera: Notonectidae) on immature stages of Culex pipiens (Diptera: Culicidae). Journal of Vector Ecology, 37(1), 245–251. DOI: 10.1111/j.1948-7134.2012.00223.x
Fischer, S., Zanotti, G., Castro, A., Quiroga, L., & Vargas, D. 2013. Effect of habitat complexity on the predation of Buenoa fuscipennis (Heteroptera: Notonectidae) on mosquito immature stages and alternative prey. Journal of Vector Ecology, 38(2), 215–223. DOI: 10.1111/j.1948-7134.2013.12033.x
Fonseca, D. M., Wilkerson, R. C., Smith, J. L., & Fleischer, R. C. 2006. Pathways of expansion and multiple introductions illustrated by large genetic differentiation among worldwide populations of the southern house mosquito. American Journal of Tropical Medicine and Hygiene, 74(2), 284–289. DOI: 10.4269/ajtmh.2006.74.284
Gaffigan, T. V., Wilkerson, C. R., Pecor, J. E., Stoffer, J. A., & Anderson, T. 2020. Systematic Catalog of Culicidae. Walter Reed Biosystematics Unit. (Retrieved on January 25th, 2022, from https://www.wrbu.si.edu/resources/catalog).
Golding, N., Nunn, M., & Purse, B. 2015. Identifying biotic interactions which drive the spatial distribution of a mosquito community. Parasites & Vectors, 8, 367. DOI: 10.1186/s13071-015-0915-1
Hassell, M. P., & Varley, G. C. 1969. New inductive population model for insect parasites and its bearing on biological control. Nature, 223(5211), 1133–1137. DOI: 10.1038/2231133a0
Heckman, C. W. 2011. Encyclopedia of South American aquatic insects: Hemiptera - Heteroptera: Illustrated keys to known families, genera, and species in South America. Dordrecht: Springer: p. 679.
Holling, C. S. 1959. Some characteristics of simple types of predation and parasitism. The Canadian Entomologist, 91(7), 385–398. DOI: 10.4039/Ent91385-7
Juliano, S. A. 2001. Nonlinear curve fitting: predation and functional response curves, in: Scheiner, S.M., Gurevitch, J. (Eds.), Design and Analysis of Ecological Experiments. pp. 178–196. Oxford: Oxford University Press.
Kauffman, E., Payne, A., Franke, M. A., Schmid, M. A., Harris, E., & Kramer, L. D. 2017. Rearing of Culex spp. and Aedes spp. Mosquitoes. Bio-protocol, 7(17), e2542. DOI: https://doi.org/gcgzq7
Lacma, J. F., Iannacone, J., & Alvariño, L. 2017. Variation of entomological indicators of Aedes aegypti and other Culicids (Diptera: Culicidae) in two municipal parks of the province of Lima, Peru. Neotropical Helminthology, 11(1), 95–114. DOI: 10.24039/rnh2017111696
Li, Y., Rall, B. C., & Kalinkat, G. 2018. Experimental duration and predator satiation levels systematically affect functional response parameters. Oikos, 127(4), 590–598. DOI: 10.1111/oik.04479
Lounibos, L. P. 2002. Invasions by insect vectors of human disease. Annual Review of Entomology, 47, 233–266. DOI: 10.1146/annurev.ento.47.091201.145206
Manly, B. F. J. 1974. A model for certain types of selection experiments. Biometrics, 30, 281–294. DOI: 10.2307/2529649
Mills, J. N., Gage, K. L., & Khan, A. S. 2010. Potential influence of climate change on vector-borne and zoonotic diseases: A review and proposed research plan. Environmental Health Perspectives, 118(11), 1507–1514. DOI: 10.1289/ehp.0901389
MINSA 2019 (Ministerio de Salud). Boletín Epidemiológico del Perú: Semana Epidemiológica 07-2019 (Volumen 28 - SE 7). Centro Nacional de Epidemiología, Prevención y Control de Enfermedades. Lima, Perú. (Retrieved on January 25th, 2022, from https://www.dge.gob.pe/portal/docs/vigilancia/boletines/2019/07.pdf).
Mogi, M. 2007. Insects and other invertebrate predators. Journal of the American Mosquito Control Association, 23(sp. 2), 93–109. DOI: 10.2987/8756-971X(2007)23[93:IAOIP]2.0.CO;2
Pervez, A. O. 2005. Functional responses of coccinellid predators: An illustration of a logistic approach. Journal of Insect Physiology, 5(5), 1–6. DOI: 10.1093/jis/5.1.5
Pritchard, D. W., Paterson, R. A., Bovy, H. C., & Barrios‐O’Neill, D. 2018. Frair: an R package for fitting and comparing consumer functional responses. Methods in Ecology and Evolution, 8(11), 1528–1534. DOI: 10.1111/2041-210X.12784
Quiroz-Martínez, H., & Rodríguez-Castro, A. 2007. Aquatic insects as predators of mosquito larvae. Journal of the American Mosquito Control Association, 23(Suppl.2), 110–117. DOI: 10.2987/8756-971X(2007)23[110:AIAPOM]2.0.CO;2
Quiroz-Martínez, H., Rodríguez-Castro, V. A., Solís-Rojas, C., & Maldonado-Blanco, M. G. 2005. Predatory capacity and prey selectivity of nymphs of the dragonfly Pantala hymenaea. Journal of the American Mosquito Control Association, 21(3), 328–330. DOI: 10.2987/8756-971X(2005)21[328:PCAPSO]2.0.CO;2
R Core Team. 2018. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2630 pp.
Reiter, P. 1983. A portable battery-powered trap for collecting gravid Culex mosquitoes. Mosquito News, 43(4), 496–498.
Reiter, P., Amador, M. A., & Colon, N. 1991. Enhancement of the CDC ovitrap with hay infusions for daily monitoring of Aedes aegypti populations. Journal of the American Mosquito Control Association, 7(1), 52–55.
Requena-Zuñiga, E., Mendoza-Uribe, L., & Guevara-Saravia, M. 2016. Nuevas áreas de distribución de Aedes aegypti en Perú. Revista Peruana de Medicina Experimental y Salud. Pública, 33(1), 171–172. DOI: 10.17843/rpmesp.2016.331.1804
Roberts, D. 2014. Mosquito larvae change their feeding behavior in response to kairomones from some predators. Journal of Medical Entomology, 51(2), 368–374. DOI: 10.1603/ME13129
Rodríguez-Castro, V. A., Quiroz-Martinez, H., Solis-Rojas, C., & Tejada, L. O. 2006. Mass rearing and egg release of Buenoa scimitra bare as biocontrol of larval Culex quinquefasciatus. Journal of the American Mosquito Control Association, 22(1), 123–125. DOI: 10.2987/8756-971X(2006)22[123:MRAERO]2.0.CO;2
Samy, A. M., Elaagip, A. H., Kenawy, M. A., Ayres, C. F. J., Peterson, A. T., & Soliman, D. E. 2016. Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile Virus and Lymphatic Filariasis. PLOS ONE 11(10), e0163863. DOI: 10.1371/journal.pone.0163863
Saul, W. C., Roy, H. E., Booy, O., Carnevali, L., Chen, H. J., Genovesi, P., Harrower, C. A., Hulme, P. E., Pagad, S., Pergl, J., & Jeschke, J. M. 2017. Assessing patterns in introduction pathways of alien species by linking major invasion data bases. Journal of Applied Ecology, 54(2), 657-669. DOI: 10.5061/dryad.m93f6
Shah, M. A., & Khan, A. A. 2013. Functional response - a function of predator and prey species. The Bioscan, 8(3), 751–758.
Sih, A. 1986. Antipredator responses and the perception of danger by mosquito larvae. Ecology, 67(2), 434–441. DOI: 10.2307/1938587
Stein, M., Rossi, G. C., & Almirón, W. R. 2016. Sección 3: Ecología. Cap. 4. Distribución geográfica de Culicidae de Argentina. In: Berón, C. M., Campos, R. E., Gleiser, R. M., Díaz-Nieto, L. M., Salomón, O. D., & Schweigmann, N. (Eds.), Investigaciones sobre mosquitos de Argentina. pp. 47–56. Mar del Plata: Universidad Nacional de Mar del Plata.
Weterings, R., Vetter, K. C., & Umponstira, C. 2014. Factors influencing the predation rates of Anisops breddini (Hemiptera: Notonectidae) feeding on mosquito larvae. Journal of Entomological and Acarological Research, 46(1), 107–111. DOI: 10.4081/jear.2014.4036
Woodward, G., & Warren, P. 2007. Body size and predatory interactions in freshwaters: Scaling from individuals to communities. In: Hildrew, A.G., Raffaelli, D.G., & Edmonds-Brown, R. (Eds.), Body Size: The Structure and Function of Aquatic Ecosystems. pp. 98–117. New York: Cambridge University Press. DOI: 10.1017/CBO9780511611223.007
