Comparative biology and growth rate of the mites Mononychellus tanajoa and Euseius ho (Acari)on cassava
Biología comparada y tasa de crecimiento de los ácaros Mononychellus tanajoa y Euseius ho (Acari)en yuca
ADRIANO S. RÊGO1,2, ANILDE G. S. MACIEL1,3, ÉVILA C. COSTA1,4, ESTER A. SILVA5 and ADENIR V. TEODORO1,6
1 Graduate Programme in Agroecology, Maranhão State University (UEMA), PO Box 09, São Luís, MA, Brazil.
2,4 M. Sc.
3 Agronomist. 5 Dra. Department of Crop Science and Plant Health, Maranhão State University (UEMA), PO Box 09, São Luís, MA, Brazil.
6 Ph. D. Embrapa Coastal Tablelands, Av. Beira-Mar 3250, Jardins, PO Box 44, Aracaju, SE, Brazil, adenir.teodoro@embrapa.br, corresponding author.
Abstract: The cassava green mite, Mononychellus tanajoa, is an important pest of cassava, Manihot esculenta (Euphorbiaceae), in the northeastern state of Maranhão, Brazil. Predatory mites of the family Phytoseiidae are key natural enemies of pest mites and are found inhabiting cassava plants. We compared some biological aspects and the growth rate of M. tanajoa and the generalist phytoseiid Euseius ho - the most abundant predatory mite inhabiting cassava plants in the study region. All experiments were conducted in the laboratory on leaf discs of cassava leaves. The predatory mite was fed in all developmental stages with M. tanajoa. Euseius ho had lower periods of egg, larva, protonymph and deutonymph developmental periods, as well as the period from egg to adult compared to M. tanajoa. Furthermore, the predatory mite E. ho had a high instantaneous rate of increase (ri), yet lower than that observed for its prey, the cassava green mite M. tanajoa. The laboratory results suggest that the predatory mite E. ho may contribute to regulate populations of M. tanajoa in the field.
Key words: Biological control. Phytophagous mite. Predatory mite.
Resumen: El ácaro verde Mononychellus tanajoa es una plaga importante de la yuca Manihot esculenta (Euphorbiaceae) en el nordeste del estado de Maranhão, Brasil. Los ácaros depredadores de la familia Phytoseiidae, son enemigos naturales clave de los ácaros plaga y se encuentran en plantas de yuca. Se compararon algunos de los aspectos biológicos y la tasa de crecimiento de M. tanajoa y Euseius ho, el ácaro depredador, generalista fitoseideo, más abundante en las plantas de yuca en la región de estudio. Todos los experimentos se llevaron a cabo en laboratorio en discos de hojas de yuca. El ácaro depredador se alimentó en todas las etapas de desarrollo con M. tanajoa. Euseius ho tuvo menores períodos de huevo, larva, protoninfa y deutoninfa, así como de huevo a adulto comparado con M. tanajoa. Además, el ácaro depredador E. ho presentó una alta tasa instantánea de crecimiento (ri) aunque inferior a la observada a su presa, el ácaro verde de la yuca M. tanajoa. Los resultados de laboratorio indican que el ácaro depredador E. ho puede contribuir a regular las poblaciones de M. tanajoa en el campo.
Palabras clave: Control biológico. Ácaro fitófago. Ácaro depredador.
Introduction
The cassava Manihot esculenta Crantz, 1766 (Euphorbiaceae) is grown in several tropical and subtropical regions of the world and is considered a major staple food (Henry and Hershey 2002; Hillocks 2002; Suja et al. 2010). In the Northeastern state of Maranhão, Brazil, cassava is cultivated by smallholders using slash and burn agricultural practices. In this region, cassava is one of the main crops food-securing smallholders.
Cassava is attacked by a variety of pests, among them the cassava green mite Mononychellus tanajoa (Bondar, 1938) (Acari: Tetranychidae). This mite is considered a key pest responsible for high yield losses (Yaninek et al. 1989; Moraes and Flechtmann 2008). The cassava green mite attacks shoots and leaves of cassava reducing both photosynthetic rate and root dry matter (Moraes and Flechtmann 2008; Yaninek et al. 1989; Yaninek et al. 1990). Management strategies ranging from pesticides to biological control agents may help to keep populations of the cassava green mite under damaging levels (Yaninek and Hanna 2003; Delalibera Jr and Hajek 2004; Delalibera Jr et al. 2004; Hanna et al. 2005).
Regarding the biological control, predatory phytoseiid mites are key natural enemies of pest mites (McMurtry et al. 1970; McMurtry and Croft 1997; Sarmento et al. 2011).
Phytoseiid mites belonging to the genus Euseius are considered generalist predators as they feed on pollen, nectar as well as on pest mites of the families Tetranychidae, Tarsonemidae, Tenuipalpidae and Eriophyidae (McMurtry and Croft 1997). In Brazil, phytoseiid species like Euseius citrifolius Denmark and Muma, 1970 (Moraes and McMurtry 1981), E. concordis (Chant, 1959) (Moraes and Lima 1983) and E. alatus De Leon, 1966 (Melo et al. 2009) are widely studied in regard to their potential to control pest mites. The predatory mite Euseius ho (De Leon, 1965) occurs throughout Brazil and in other Latin American countries such as Argentina, Colombia, Peru, Ecuador, Mexico and Puerto Rico (Moraes et al. 2004). In the region where our study was conducted, E. ho is the most abundant predatory mite inhabiting cassava plants over the year (Unpublished data). Generalist predatory mites such as E. ho play a major role in reducing populations of pest mites as they are able to survive in periods where the target pest is scarce or absent (Tsitsilas et al. 2011). Here, we studied the importance of E. ho as a potential natural biological control agent of the cassava green mite by comparing some biological aspects and growth rates of both mites under laboratory conditions. We predicted that although being a generalist predator, E. ho may contribute to the natural biological control of the cassava green mite M. tanajoa.
]]> Materials and MethodsThe study was conducted in the laboratory of Arthropods of the Maranhão State University at 27±10 °C, 10h L: 14 h D photoperiod, and 60 ± 20% relative humidity.
Mite rearing. The cassava green mite M. tanajoa and the predadory mite E. ho were collected from unsprayed cassava fields located around the city of Miranda do Norte (3º36’44.70”S 44º34’07.51”W, 44 masl), Maranhão State, Brazil. The cassava green mite M. tanajoa was reared on 6-months-old potted cassava plants in a greenhouse. The predatory mite E. ho was reared on cassava leaf discs (5 cm diameter) floating on a Petri dish without lid (10 cm diameter x 1.5 cm height) filled with distilled water. Cotton threads underneath a glass slide (18 x 18 mm) were placed at the middle of each leaf disc to serve as shelter for predatory mites. The predatory mite E. ho was provided with all developmental stages of the cassava green mite (eggs, larvae, nymphs and adults).
Biological studies. Life cycle parameters were determined for both M. tanajoa and E. ho. The egg periods for M. tanajoa and E. ho were evaluated in cassava leaf discs of 3 and 5 cm diameter, respectively. Leaf discs were transferred to Petri dishes without lid (10 cm diameter x 1.5 cm high) filled with distilled water as described above. Gravid females of either M. tanajoa or E. ho were transferred to cassava leaf discs for a period of four hours in order to obtain newly laid eggs. Afterwards, eggs were observed twice a day (08:00 a.m. and 16:00 p.m.) to determine the duration of the egg period. All developmental stages of M. tanajoa were provided as prey for E. ho.
Recently emerged larvae of both M. tanajoa and E. ho were individually transferred to cassava leaf discs with a fine brush and the duration of each immature developmental stage was recorded twice a day (08:00 and 16:00). Mites of both species were sexed after reaching adulthood and the duration of the periods of preoviposition, oviposition, postoviposition, number of eggs/female and number of eggs/female/day for females were also daily recorded. A male of M. tanajoa or E. ho was introduced to each leaf disc containing a newly emerged female and replaced whenever it died.Population growth rate. The intrinsic growth rate (ri) was used to compare the population build up of both the cassava green mite M. tanajoa and the predatory mite E. ho. The ri was estimated based on reproduction and mortality data using the equation ri= ln (Nf/ N0)/ Δt, where Nf is the final number of living mites, N0 is the initial number of living mites and Δt is the interval (days) elapsed between the start and end of the bioassay (Stark et al. 1997; Walthall and Stark 1997a). The instantaneous rate of increase (ri) is a direct measure of populaton growth in a given time and is positively related to the intrinsic growth rate (rm) (Walthall and Stark 1997b). A positive ri value indicates population increase while a negative value indicates population decline (Walthall and Stark 1997b).
The intrinsic growth rates for M. tanajoa and E. ho were estimated by recording the number of eggs laid, immature and adult mites at the end of the bioassay (seven days). Four adult females of either the cassava green mite or the predator were placed separately onto cassava leaf discs (3 or 5 cm diameter, respectively). All mites tested were in the beginning of their reproductive period, i.e., ca. 10-day-old females of M. tanajoa or ca. 4-day-old females of E. ho. Males of either M. tanajoa or E. ho taken from the stock cultures were introduced in each leaf disc and replaced by new ones whenever they died.Statistical analyses. Student’s t tests (Sokal and Rohlf 1995) were used to compare the periods of immature development, egg to adult, preoviposition, oviposition, postoviposition and the population growth rates of M. tanajoa and E. ho. All analyses were carried out using the software Statistica 7.0 (StatSoft Inc. 2004).
Results
Eggs of the predatory mite E. ho hatched within 1.5 ± 0.03 days (means ± SE, n = 82) whereas those of the cassava green mite M. tanajoa had a longer incubation period (4.7 ± 0.01 days) (means ± SE, n = 104) (df = 487, t = 85.79, P < 0.05, Fig. 1). Viability of eggs, measured as percentage of hatching, were similar for M. tanajoa (95.93%, n = 442) and E. ho (95.34%, n = 86). The duration of the larval period of E. ho (0.6 ± 0.03 days, n = 75) was shorter than that of M. tanajoa (1.0 ± 0.02 days, n = 101) (df = 174, t = 9.15, P < 0.05, Fig. 1). Similarly, the stage of protonymph of E. ho (0.7 ± 0.03 days, n = 57) developed faster than that of M. tanajoa (0.9 ± 0.02 days, n = 77) (df = 132, t = 5.59, P < 0.05, Fig. 1). The duration of the stage of deutonymph was faster for E. ho (0.7 ± 0.02 days, n = 40) in comparison to M. tanajoa (1.0 ± 0.02 days, n = 70) (df = 108, t = 5.95, P < 0.05, Fig. 1). As a result of short development, E. ho had a shorter egg-to-adult period (4.4 ± 0.08 days, n = 40) in comparison to M. tanajoa (10.3 ± 0.02 days, n = 67) (df = 105, t = 42.84, P < 0.05, Fig. 1). The periods of protochrysalid, deutochrysalid and teliochrysalid for M. tanajoa were 0.8 ± 0.02, 0.7 ± 0.01, 0.9 ± 0.02, respectively (Fig. 1).
Euseius ho and M. tanajoa had similar preoviposition (df = 76, t = 0.48, P > 0.05, Table 1) and postoviposition periods (df = 42, t = 0.48, P > 0.05, Table 1). The periods of preovipositon and postoviposition for E. ho were 1.2 ± 0.06 and 2.6 ± 0.10 days, respectively, and the same periods for M. tanajoa were 1.2 ± 0.05 and 2.5 ± 0.16 days, respectively (Table 1). The predatory mite E. ho had, however, a longer oviposition period (21.7 ± 0.22 days) than M. tanajoa (16.3 ± 0.28 days) (df = 42, t = 15.11, P < 0.05) (Table 1). Conversely, the number of eggs/ female and the number of eggs/ female/ day were higher for M. tanajoa than for E. ho (Table 1). Daily oviposition was higher for M. tanajoa (5.3 ± 0.19) in comparison to E. ho (2.1 ± 0.03) (df = 42, t = 16.30, P < 0.05). Consequently, M. tanajoa laid more eggs (84.4 ± 4.22) than E. ho (47.3 ± 0.85) during their ovipositional periods (df = 42, t = 8.61, P < 0.05) (Table 1). Mononychellus tanajoa also presented higher values of population growth (0.42 ± 0.01) than E. ho (0.35 ± 0.005) (df = 49, t = 3.96, P < 0.05, n = 22 for both species).
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Discussion
Although considered a generalist predator, E. ho fed and completed its life cycle on the cassava green mite M. tanajoa. Prey preference often matches reproductive success in phytoseiid mites (Dicke et al. 1990; Gnanvossou et al. 2003). The predatory mite E. ho had a lower egg-to-adult period in comparison to the cassava green mite M. tanajoa (Fig. 1). Indeed, all immature stages of E. ho (egg, larva, protonymph and deutonymph) developed faster than those of M. tanajoa (Fig. 1). Even though being a generalist predator, E. ho proved to be a potential natural enemy of M. tanajoa and could be used in conservation biological control programmes. Bruce-Oliver et al. (1996), evaluated the effects of several food resources on the development, fecundity and longevity of Euseius fustis (Pritchard and Baker, 1962), which is a generalist predatory mite associated to cassava in Africa. Euseius fustis sucessfully completed its life cycle when fed on M. tanajoa, Oligonychus gossypii (Zacher, 1921), maize (Zea mays L., 1753) pollen, castor bean (Ricinus communis L., 1753) pollen and cassava pollen. Euseius fustis fed on castor bean pollen or maize pollen had higher fecundity and longevity compared to M. tanajoa as prey indicating that the Euseius species may also benefit from alternative.
A suitable natural biological control agent of pest mites should have a fast development time and a high oviposition rate when feeding on its prey. Our results show that E. ho had a high reproductive potential when fed on the cassava green mite alone indicating that this predatory mite species is adapted to this type of prey and a potential biological control agent of M. tanajoa. The longer oviposition period (21.7 ± 0.22 days) combined with the shorter developmental time (4.4 ± 0.08 days) of E. ho in comparison to its prey are important parameters for a biological control agent.
The predatory mite E. ho had a high instantaneous rate of increase (ri), yet lower than that observed for its prey, the cassava green mite M. tanajoa. Euseius ho and M. tanajoa were confined in small leaf discs during experiments, which may have favoured prey location and predation resulting in high growth rate of the predatory mite. Predatory mite species are also favoured by tetranychid species which spin low amounts of web (McMurtry and Croft 1997; Vantornhout et al. 2004). It may also help to explain the high growth rate of E. ho feeding on M. tanajoa as the latter does not produce much web. The biological control of tetranychid mites under field conditions depend on several factors which may influence the survival and persistence of predatory mites such as the host plant, climate-related variables and the interaction with other (Kennedy and Storer 2000; Pratt et al. 2002; Zundel et al. 2009). Pest populations may be managed through preservation and enhancement of resident natural enemies using conservation biological control (Letourneau and Altieri 1999; Landis et al. 2000). However, it is essencial to know the biology of the pest and its natural enemies in order to have success in this type of biological control (Landis et al. 2000). As a generalist predatory mite, E. ho may be favoured by cassava intercropped with pollen-producing plants such as maize, pumpkin (Cucurbita moschata Duchesne) and weeds. Indeed, in the region where the study took place, smallholders usually intercrop cassava with maize, pumpkin besides allowing weeds to grown freely. The ability of generalist predatory mites to use pollen or alternative prey as food source to develop, reproduce and survive is key for their establishment and persistence in cassava plantations.
In conclusion, our laboratory results show that the predatory mite E. ho is a potential biological control agent of the cassava green mite M. tanajoa. However, complementary field studies are necessary to assess the real potential of E. ho in regulating populations of the cassava green mite M. tanajoa.
Acknowledgements
Funding was provided by PNPD/CAPES (PNPD0132080), CNPq (474994/2009-0) and FAPEMA (APP-00991/09). We also thank Renato A. Sarmento for helpful comments on a previous version of this manuscript.
Literature cited
BRUCE-OLIVER, S. J.; HOY, M. A.; YANINEK, J. S. 1996. Effect of some food sources associated with cassava in Africa on the development, fecundity and longevity of Euseius fustis (Pritchard and Baker) (Acari: Phytoseiidae). Experimental and Applied Acarology 20 (2): 73-85. [ Links ]
DELALIBERA Jr., I.; HAJEK, A. E. 2004. Pathogenicity and specificity of Neozygites tanajoae and Neozygites floridana (Zygomycetes: Entomophthorales) isolates pathogenic to the cassava green mite. Biological Control 30 (3): 608-616. [ Links ]
DELALIBERA Jr., I.; HAJEK, A. E.; HUMBER, R. A. 2004. Neozygites tanajoae sp. nov., a pathogen of the cassava green mite. Mycologia 96 (5): 1002-1009. [ Links ]
DICKE, M.; SABELIS, M. W.; JONG, M.; DE ALERS, M. P. T. 1990. Do phytoseiid mites select the best prey species in terms of reproductive success? Experimental and Applied Acarology8 (3): 161-173. [ Links ]
GNANVOSSOU, D.; YANINEK, J. S.; HANNA, R.; DICKE, M. 2003. Effects of prey mite species on life history of the phytoseiid predators Typhlodromalus manihoti and Typhlodromalus aripo. Experimental and Applied Acarology 30 (4): 265-278. [ Links ]
HANNA, R.; ONZO, A.; LINGEMAN, R.; SABELIS, M..; YANINEK, J. S. 2005. Seasonal cycles and persistence of an acarine predator-prey system on cassava in Africa. Population Ecology 47 (2): 107-117Links ]Verdana","sans-serif"'>.
HENRY, G.; HERSHEY, C. 2002. Cassava in South America and the Caribbean. pp. 17-40. In: Hillocks, R. J.; Tresh, J. M.; Bellotti, A. C. (Eds.). Cassava: Biology, Production and Utilization. CABI International, Wallingford, UK, 332 p. [ Links ]
Hillocks, R. J. 2002. Cassava in Africa. pp. 40-54. In: Hillocks, R. J.; Tresh, J. M.; Bellotti, A. C. (Eds.). Cassava: Biology, Production and Utilization. CABI International, Wallingford, UK, 332 p. [ Links ]
KENNEDY, G. G.; STORER, N. P. 2000. Life systems of polyphagous arthropod pests in temporally unstable cropping systems. Annual Review of Entomology 45 (1): 467-493. [ Links ]
LANDIS, D. A.; WRATTEN, S. D.; GURR, G. M. 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology 45 (1): 175-201. [ Links ]
LETOURNEAU, D. K.; ALTIERI, M. A. 1999. Environmental management to enhamce biological control in agroecosystems. pp. 319-354. In: Bellows, T. S.; Fisher, T. W. (Eds.). Handbook of Biological Control. Academic Press, San Diego, USA, 1046 p. [ Links ]
McMURTRY, J. A.; HUFFAKER, C. B.; VAN DE VRIE, M. 1970. Ecology of tetranychid mites and their natural enemies: A review I. Tetranychidae enemies: their biological characters and the impact of spray practices. Hilgardia 40 (1): 331-390. [ Links ]
McMURTRY, J. A.; CROFT, B. A. 1997. Life styles of phytoseiid mites and their roles in biological control. Annual Review of Entomology 42 (1): 291-321. [ Links ]
MELO, J. W. S.; DOMINGOS, C. A.; GONDIM JUNIOR, M. G. C.; DE MORAES, G. J. 2009. Pode Euseius alatus DeLeon (Acari: Phytoseiidae) predar Aceria guerreronis Keifer (Acari: Eriophyidae) em coqueiro? Neotropical Entomology38 (1): 139-143. [ Links ]
MORAES, G. J.; MCMURTRY, J. A. 1981. Biology of Amblyseius citrifolius (Denmark and Muma) (Acarina: Phytoseiidae). Hilgardia 49 (1): 1-29. [ Links ]
MORAES, G. J.; LIMA, H. C. 1983. Biology of Euseius concordis (Chant) (Acarina: Phytoseiidae) a predator of the tomato russet mite. Acarologia 24 (3): 251-255. [ Links ]
MORAES, G. J.; MCMURTRY, J. A.; DENMARK, H. A.; CAMPOS, C. B. 2004. A revised catalog of the mite family Phytoseiidae. Zootaxa (434). Magnolia Press, Auckland, New Zealand, 494 p. [ Links ]
MORAES, G. J.; FLECHTMANN, C. H. W. 2008. Manual de Acarologia: acarologia básica e ácaros de plantas cultivadas no Brasil. Holos, Ribeirão Preto, Brazil, 308 p. [ Links ]
PRATT, P. D.; ROSETTA, R.; CROFT, B. A. 2002. Plant-related factors influence the effectiveness of Neoseiulus fallacis (Acari: Phytoseiidae), a biological control agent of spider mites on landscape ornamental plants. Journal of Economic Entomology95 (6): 1135-1141. [ Links ]
SARMENTO, R. A.; RODRIGUES, D. M.; FARAJI, F.; ERASMO, E. A. L.; LEMOS, F.; TEODORO, A. V.; KIKUCHI, W.; SANTOS, G. R.; PALLINI, A. 2011. Suitability of the predatory mites Iphiseiodes zuluagai and Euseius concordis in controlling Polyphagotarsonemus latus and Tetranychus bastosi on Jatropha curcas plants in Brazil. Experimental and Applied Acarology53 (3): 203-214. [ Links ]
STARK, J. D.; TANIGOSHI, L.; BOUNFOUR, M.; ANTONELLI, A. 1997. Reproductive potential: its influence on the susceptibility of a species to pesticides. Ecotoxicology and Environmental Safety 37 (3): 273-279. [ Links ]
SOKAL, R. R.; ROHLF, F. J. 1995. Biometry: the principles and practice of statistics in biological research. Freeman and Co, New York, 887 p. [ Links ]
SUJA, G.; JOHN, S. K.; SREEKUMAR, J.; SRINIVAS, T. 2010. Short-duration cassava genotypes for crop diversification in the humid tropics: growth dynamics, biomass, yield and quality. Journal of the Science of Food and Agriculture 90 (2): 188-198. [ Links ]
STATSOFT INC. 2004. Statistica for Windows (Software-system for data-analyses), Version 7.0. Tulsa, USA. [ Links ]
TSITSILAS, A.; HOFFMANN, A. A.; WEEKS, A. R.; UMINA, P. A. 2011. Impact of groundcover manipulations within windbreaks on mite pests and their natural enemies. Australian Journal of Entomology 50 (1): 37‑47. [ Links ]
VANTORNHOUT, I.; MINNAERT, H. L.; TIRRY, L.; DE CLERCQ, P. 2004. Effect of pollen, natural prey and factitious prey on the development of Iphiseius degenerans. BioControl 49 (6): 627-644. [ Links ]
WALTHALL, W. K.; STARK, J. D. 1997a. Comparison of acute mortality and population growth rate as endpoints of toxicological effect. Ecotoxicology and Environmental Safety 37 (1): 45-52. [ Links ]
WALTHALL, W. K.; STARK, J. D. 1997b. Comparison of two population-level ecotoxicological endpoints: the intrinsic (rm) and instantaneous (ri) rates of increase.Environmental Toxicology and Chemistry 16 (5): 1068-1073. [ Links ]
YANINEK, J. S.; DE MORAES, G. J.; MARKHAM, R. H. 1989. Handbook on the cassava green mite Mononychellus tanajoa in Africa. Ibadan: International Institute of Tropical Agriculture, Benin, 140 p. [ Links ]
YANINEK, J. S.; GUTIERREZ, A. P.; HERREN, H. R. 1990. Dynamics of Mononychellus tanajoa (Acari: Tetranychidae) in Africa: impact on dry matter production and allocation in cassava, Manihot esculenta. Environmental Entomology 19 (6): 1767-1772. [ Links ]
YANINEK, J. S.; HANNA, R. 2003. Cassava green mite in Africa: a unique example of successful classical biological control of a mite pest on a continental scale. pp. 61-75. In: Neuenschwander, P.; Borgemeister, C.; Langewald, J. (Eds.). Biological control in IPM systems in Africa. CABI International, Wallingford, UK, 414 p. [ Links ]
ZUNDEL C.; NAGEL, P.; HANNA, R.; KORNER, F.; SCHEIDEGGER, U. 2009. Environment and host-plant genotype effects on the seasonal dynamics of a predatory mite on cassava in sub-humid tropical Africa. Agricultural and Forest Entomology 11 (3): 321-331. [ Links ]
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