Sección control

Alternative food sources to predatory mites (Acari) in a Jatropha curcas (Euphorbiaceae) crop

Fuentes alternativas de alimentación de ácaros depredadores (Acari) en cultivos de Jatropha curcas (Euphorbiaceae)

RENATA VIEIRA MARQUES^1,2, RENATO ALMEIDA SARMENTO^1,3, VINÍCIUS ALVES FERREIRA^4,5, MADELAINE VENZON ⁶, FELIPE LEMOS ^4,7, MARÇAL PEDRO-NETO ^1,8, EDUARDO ANDREA LEMUS ERASMO ^1,9 and ANGELO PALLINI ^4,10

¹ Program in Plant Science, Federal University of Tocantins (UFT), PO BOX 66, Gurupi, TO, Brazil.
² Master researcher, Graduate. renatamarques@uft.edu.br.
³ Ph. D. Graduate. rsarmento@mail.uft.edu.br. Corresponding author.
⁴ Department of Entomology, Federal University of Viçosa, (UFV) CEP 36570-000,Viçosa, MG, Brazil.
⁵ M. Sc. ferreirava@hotmail.com.
⁶ Ph. D. Agriculture and Livestock Research Enterprise of Minas Gerais (EPAMIG), Vila Gianetti 46, CEP 36570-000 Viçosa, MG, Brazil, venzon@epamig.ufv.br.
⁷ Doctorate researcher, M. Sc. felipelemosufv@gmail.com.
⁸ Ph. D. Graduate. pedronetom@yahoo.com.br.
⁹ Ph. D. Graduate. erasmolemus@uol.com.br. 10 Ph. D. pallini@ufv.edu.br

Received: 18-aug.-2013 • Accepted: 12-feb.-2014

Abstract: In Brazil, smallholders produce the physic nut Jatropha curcas in association with crops such as pumpkin and corn, besides weeds. We evaluated the suitability of pumpkin and corn pollens, as well as pollen from a weed species (Peltaea riedelii), present in physic nut crop, as alternative food to predatory mites Euseius concordis and Iphiseiodes zuluagai. These species are natural enemies of Polyphagotarsonemus latus and Tetranychus bastosi, two important mite pests on J. curcas plants. The survival and oviposition rate of E. concordis and I. zuluagai were evaluated for five days on leaf discs supplied with pollen of pumpkin, corn or P. riedelii. Castor bean pollen (Ricinus communis) was provided to the predators as a control of suitable food. No significant difference on the oviposition rate of both I. zuluagai and E. concordis was observed when they fed with pollen from the three plants. However, the source of pollen affected the survival of the predatory mites. Pumpkin pollen was the worst food for both predatory mites while corn and P. riedelii was a better food. These results indicate the non-suitability of pumpkin pollen as alternative food to I. zuluagai and E. concordis. Corn and P. riedelli are sources of supplementary food to the predatory mites and can sustain predator populations when prey is scarce.

Key words: Iphiseiodes zuluagai. Euseius concordis. Polyphagotarsonemus latus. Tetranychus bastosi. Physic nut.

Resumen: En Brazil los pequeños agricultores producen el piñón Jatropha curcas L. asociado con plantaciones de zapallo, maíz, y muchas veces con malezas. Evaluamos la adecuación del polen de zapallo y maíz, así como de la maleza (Peltaea riedelli), frecuente en los cultivos del piñon, como fuente de alimento alternativo para los ácaros E. concordis y I. zuluagai. Estas especies son los enemigos naturales de Polyphagotarsonemus latus y Tetranychus bastosi, dos principales ácaros plagas de plantas de jatropha. La tasa de sobrevivencia y desove de los ácaros E. concordis y I. zuluagai fue evaluada por un período de cinco días en discos de hojas provistas con polen de zapallo, maíz o de P. riedelii. Polen de la planta Ricinus communis fue previsto para los depredadores, como control de alimentación adecuada. No hubo diferencia estadística en la tasa del desove de ambos I. zuluagai y E. concordis cuando alimentados con el polen de las especies evaluadas. No obstante, la fuente de polen afecta la sobrevivencia de los ácaros depredadores. El polen de zapallo fue el peor alimento para ambos ácaros depredadores, contrario al del maíz y la maleza P. riedelii, que fueron los mejores. Los resultados indican que el polen de zapallo es inadecuado como alimento alternativo para I. zuluagai y E. concordis. El maíz y la maleza P. riedelli representan una fuente alimenticia suplementaria para los ácaros depredadores y puede ser importante para sustentar poblaciones de depredadores, por lo menos algunos días, cuando la presa está ausente o escasa.

Palabras clave: Iphiseiodes zuluagai. Euseius concordis. Polyphagotarsonemus latus. Tetranychus bastosi. Jatropha.

Introduction

In diversified farming systems, the association of plant species can result in more efficient biological control of pests due to increased diversity and abundance of natural enemies (Andow 1991; Altieri 1999; Letourneau et al. 2011). For instance, the occurrence and abundance of predatory mites of the family Phytoseiidae can be enhanced by food sources and shelter found in natural vegetation fragments near the main crop (Addison et al. 2000; Zacarias and Moraes 2002; Demite and Feres 2005). Generalist predatory mites have a diverse dietary habit including pollen and nectar (Yamamoto and Gravena 1996; McMurtry and Croft 1997). Thus, some predatory mite species can benefit from plant derived food provided by crops and weeds (Moraes et al. 1993; van Rijn and Tanigoshi 1999a; van Rijn and Tanigoshi 1999b; Bellini et al. 2005).

In Brazil, physic nut (Jatropha curcas L.) is cultivated mainly by smallholders. The broad mite Polyphagotarsonemus latus Banks, 1904 (Acari: Tarsonemidae) and the spider mite Tetranychus bastosi Tuttle, Baker and Sales, 1977 (Acari: Tetranychidae) are the main damaging mite species of physic nut (Lopes 2009; Sarmento et al. 2011; Cruz et al. 2013). The broad mite is a polyphagous and cosmopolitan species, which attacks mainly the apex of the plants (Gerson 1992; Kavitha et al. 2007). Conversely, the spider mite T.ç bastosi is more frequently found on underside of fully-developed leaves of J. curcas in comparison with younger leaves (Sarmento et al. 2011; Pedro-Neto et al. 2013). Besides, tetranychid mites, such as T. bastosi produces a considerableamount of web, which may serve to protect their colonies from predators (Gerson 1985; Saito 1985; Sabelis and Bakker 1992; Venzon et al. 2009).

The predatory mites Iphiseiodes zuluagai Denmark & Muma, 1972 and Euseius concordis Chant, 1959 (Acari: Phytoseiidae) are the most common natural enemies of P. latus and T. bastosi on J. curcas plants in Tocantins, Brazil (Sarmento et al. 2011; Cruz et al. 2012). Both species are considered promising in controlling P. latus and T. bastosi on J. curcas plants (Sarmento et al. 2011). Jatropha curcas can be cultivated associated plant species and under the natural occurrence of weeds. Smallholders and rural settlers diversified their cultivating areas of J. curcas with pumpkin and corn, and weeds are not controlled. Plant diversification play an important role in the maintenance of a community of predatory mites on this crop though provision of alternative plant food such as pollen and nectar (Moraes et al. 1993; Zannou et al. 2005; Cruz et al. 2012).

We investigated the suitability of pollen from the cultivated plants pumpkin Curcubita pepo L. (Cucurbitaceae) and corn (Zea mays L.) (Poaceae) as well as from Peltaea riedelii (Gürke) Standl. (Malvaceae), a weed species commonly present in J. curcas plantations, for survival and reproduction of the generalist predators I. zuluagai and E. concordis.

Materials and methods

The experiments were carried out at the laboratory of Entomology of the Federal University of Tocantins (UFT), Gurupi, Tocantins (11°48'29"S 48°56'39"W, 280 m), Brazil. Stock cultures of both I. zuluagai and E. concordis were started with mites collected on J. curcas plants cultivated at experimental field. Stock colonies were established on arenas with 6-cm diameter of flexible plastic discs floating inside a plastic box filled with distilled water. The rearing of predatory mites was maintained with castor bean pollen (Ricinus communis L.), which was collected from plants of natural occurrence and added on a daily-basis as food (Reis and Alves 1997). Predatory mites were maintained inside a climate chamber (28 °C, 65-70% R.H. and 12h L/12h D photoperiod). The pollens of pumpkin, corn and P. riedelii used in the experiments were collected from plants cultivated in association with J. curcas. Each pollen species was separately kept in vials (Eppendorf^TM) with capacity of 10 mL and stored in refrigerator (6 ± 2 °C). The stock of each pollen species was monthly renewed.

The oviposition and survival rates of E. concordis and I. zuluagai were evaluated when the mites were fed either on pollen of pumpkin, corn, P. riedelii and R. communis (control). Pollen were offered to the predators on leaf discs (Ø = 3 cm) made from healthy plants without pesticide residues. Pumpkin and corn pollen were offered to the predators on leaf discs made from pumpkin and corn plants respectively. Due to the reduced size of the leaves of P. riedelii plants, we offered its pollen to the predatory mites using leaf discs made from plants of J. curcas. Pollen of R. communis was offered to the predators on plastic discs as a control because it is a suitable food for both predators (Moraes & Lima 1983; Reis and Alves 1997). The discs were kept in batches of five over a piece of foam covered with wet cotton wool and placed inside plastic trays (30 x 22 x 7 cm) containing water to prevent mites from escaping. Trays were kept inside a climate chamber at the same conditions described above. Two-dayold mated females of each predator species were starved in the presence of water for 2 hours before tested. Each treatment was started with 15 predatory mite females with the exception of castor bean pollen treatment, whichv was started with 12 predatory females. Subsequently, one female of each predatory mite species (I. zuluagai or E. concordis) was released on each disc according to the pollen diet ad libitum. Leaf discs and pollen were daily replaced. Eggs of each predatory mite were quantified and discarded daily during five days.

As the species of predatory mites tested here usually lays on average less than one egg per day per female, the data onç oviposition rate presents many zero which contributed to a strongly non-normal distribution data due to zero inflation. Based on this we decided to analyze the oviposition rates of predatory mites using the more conservative non-parametric Kruskal-Wallis test with multiple comparisons. This analysis was performed with the package "agricolae" (Mendiburu 2012). To analyze the effect of different foods on survival of the predators, data were subject to a Kaplan-Meier survival analysis using the package "survival" (Therneau 2013). The contrasts among the treatments levels were accessed by pairwise planned comparisons with Log-rank tests. All tests were performed using the software R2.11 (Crawley 2007, RDevelopment-Core-Team 2012).

Results

There was no effect of the pollen species on oviposition rates of I. zuluagai (Table1, Kruskal-Wallis test's, Chi² = 5.43; P = 0.14; d.f. = 3). However the oviposition of E. concordis was significantly different among the pollen species tested (Table 2, Kruskal-Wallis test's, X² = 9.05; P = 0.03; d.f. = 3). The higher oviposition rate of E. concordis was observed on pollen of R. communis, which was significantly different from all treatments (all P < 0.05).

However, there was an effect of pollen diets on survival of I. zuluagai (Fig. 1, log-rank test, X² = 30.20; P < 0.01; d.f. = 3) and of E. concordis (Fig. 2, log-rank test, X² = 34.10; P < 0.01; d.f. = 3). The survival of I. zuluagai was significantly higher when mites fed on R. communis pollen (log-rank test, all P < 0.05). The lowest survival was observed when I. zuluagai was fed on pollen of pumpkin and P. riedelii, which does not differed statistically (log-rank test, X² = 1.40; P < 0.24; d.f. = 1).

For E. concordis, the highest survival was obtained when the predator fed on R. communis pollen (log-rank test, all P < 0.05). No significant difference on survival of this predatory mite was observed when it fed on corn or on P. riedelii pollen (log-rank test, X² = 0.00; P = 0.99; d.f. = 1). However P. riedelii provided a longer survival to E. concordis when compared with pumpkin pollen (log-rank test, X² = 4.10; P = 0.04; d.f. = 1). The lowest survival was observed when predatory mites were fed with pollen of pumpkin and corn, which does not differed statistically from each other (Fig. 2, log-rank test, X² = 2.60; P = 0.11; d.f. = 1).

Discussion

The pollen affected survival of the predatory mites I. zuluagai and E. concordis. However, none was as suitable as R. communis pollen. Pollen of pumpkin was not suitable as food to the predators at all. It resulted in death of 100% of individuals of I. zuluagai and E. concordis in three days. Likewise, the pollens of corn and of P. riedelii suit to keep E. concordis alive only for five days. Instead P. riedelii pollen was able to promote a slight long survival on I. zuluagai, but this was lower than the survival on R. cummunis pollen. However, the between the pollen for both predatory mites.

Pollen is an important resource for generalist predatory mites such as I. zuluagai and E. concordis (McMurtry and Croft 1997). It is a source of nitrogen for many insects and mites. Pollen protein content ranges from 2.5% to 61% and this concentration may influence plant-animal interactions (Roulston et al. 2000; Venzon et al. 2006). Apart from the nutritional value of macro-nutrients found in pollen, vitamins, mineral nutrients and sterols are important for digestion and other metabolic processes (Stanley and Linskens 1974; Waldbauer and Friedman 1991). Thus, differences in the digestibility and assimilation of nutrients from different pollen species are expected to have influence on fecundity and survival of predators.

Pollen can be an alternative or supplementary food for predatory mites. The term alternative food is generally applied when the predator is able to survive and reproduce on this diet (Overmeer 1985). Otherwise, the food is considered only a supplementary source. Thus, the alternative food should also be able to keep the predator alive in the absence of essential food. The pollen of corn and P. riedelii were most promising as a supplementary food source as they were not capable of maintaining I. zuluagai and E. concordis alive for long periods.

The I. zuluagai oviposition rates obtained were lower than those found in the literature when the predator fed castor bean pollen (Reis et al. 1998). This pollen species is considered an important food to rear predatory mites, giving high oviposition rates and survival over 40 days (Reis and Haddad 1997; Reis et al. 1998). Regarding survival, all alternative pollen species tested were responsible for a sharp decline in survival of the predators I. zuluagai and E. concordis. However, corn pollen resulted in better survival of I. zuluagai compared to the other tested pollens, and it is therefore the most promising pollen species. Yamamoto and Gravena (1996) added honey solution at 10% to castor bean pollen diet for I. zuluagai and reported that the mean number of eggs deposited per day was twice as high as that found by Reis et al. (1998). This suggests that nectar may be an additional food source to the diet of this predator. Possibly, in field conditions predatory mites may complement their diet exploring extrafloral nectar or plant exudates (van Rijn and Tanigoshi 1999a; Gnanvossou et al. 2005).

Although the oviposition rate of I. zuluagai when fed on corn pollen is lower than when it fed with T. bastosi or P. latus, pollen corn may improve predatory mite performance when offered with prey items or sustain predator population when prey is absent (Sarmento et al. 2011). The same pattern was observed for E. concordis. Oviposition rate was 0.29 ± 0.11 eggs/day when predator fed of corn pollen and it was 0.90 ± 0.24 and 0.68 ± 0.25 eggs/day when it fed on T. bastosi or P. latus, respectively (Sarmento et al. 2011). It was also lower when this predatory mite was fed with pollen of Typha angustifolia L. (Ferla and Moraes 2003). Furthermore, corn pollen is able to maintain E. concordis ovipositing for three days in the absence of prey.

The survival rate of E. concordis was similar when they fed on corn pollen or P. riedelii pollen. However I. zuluagai exhibited a higher survival when fed with P. riedelii pollen in comparison with corn pollen. In addition, the survival of the predators on pollen of P. riedelii was higher than on pollen of pumpkin to both predators tested. Although the pollen of this plant species might not be ideal for development of these predators, P. riedelii may contribute to the maintenance of predators in the field for a few days in prey shortage. Additionally, the presence of the forage vegetation interspersed in crops is important to provide environments for refuge for beneficial organisms (Altieri 1999; Duso et al. 2004). Peltaea riedelii belongs to the Malvaceae family, has a wide distribution in Brazil and spontaneously occurs in several agroecosystems (Barth 1975). This plant could fit in this system as a spontaneous plant, which, together with J. curcas and corn, is able to provide food resources for maintenance of the predators I. zuluagai and E. concordis. Moreover, this plant may play a role in the dispersal of predatory mites, since these, besides dispersal with the wind and with the relationship with other forest species (Helle and Sabelis 1985), can also be dispersed by meta-population dynamics (Zemek and Nachman 1998). Thus, weeds as P. riedelii and intercrops such as corn may have an important role in providing alternative food and facilitating dispersion.

When fed on pollen of pumpkin, oviposition and survival of the predators E. concordis and I. zuluagai were lower than that of the other species of pollen. It may be related to the size of the pollen grain. In the laboratory it was observed that the pollen of pumpkin is considerably larger than those of corn and P. riedelii, which can impede handling and ingestion by predators. In addition, pollen grains usually have a tough outer wall (i.e. exine) thathas protection function (Overmeer 1985). Alternatively, pumpkin pollen may notbe nutritional suited to the predator due to its chemical composition. Thus, either a physical or a chemical barrier refrain predatory mite utilization of pumpkin pollen.

The presence of plant resources (e.g. pollen and nectar) in the field is responsible for maintenance of predatory mite populations when prey is scarce or absent (Aguilar-Fenollosa et al. 2011). Furthermore, it has been shown for other systems that biological control of phytophagous mites may be improved in the presence of plant derived food (Smith and Papacek 1991; McMurtry 1992; Liang and Huang 1994; González-Fernández et al. 2009).

Field studies are necessary to determine how the predators can access these pollens and to elucidate mechanisms on how the dispersion of these species occurs. Moreover, it is necessary to evaluate the net effect of such crop diversification in the control of pest mites of J. curcas.

Conclusion

Pollen of corn and of P. riedelii has the potential to be used as food source to supplement the diet of the predators I. zuluagai and E. concordis in a J. curcas crop system.

Acknowledgements

This research was supported by The National Council of Scientific and Technological Development (CNPq) and Coordination of Improvement of Higher Education Personnel CAPES-Brazil (projects 475408/2008-0; 620028/2008-4 and PROCAD-NF 187/2010). MV and AP have a scholarship from CNPq (PQ) and MV has a grant from Minas Gerais State Foundation for Research Aid (FAPEMIG) (PPM V).

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Suggested citation:

MARQUES, R.V.; SARMENTO, R. A.; FERREIRA, V. A.; VENZON, M.; LEMOS, F.; PEDRO-NETO, M.; ERASMO, E. A. L.; PALLINI. A. 2014. Alternative food sources to predatory mites (Acari) in a Jatropha curcas (Euphorbiaceae) crop. Revista Colombiana de Entomología 40 (1): 74-79. Enero-julio 2014. ISSN 0120-0488.