Introduction

Tetranychus evansi Baker and Pritchard and Tetranychus urticae Koch are important pests of Solanaceae in many countries (Jeppson et al. 1975). T. evansi has been reported from countries in the Americas, Africa, Europe and, more recently, Asia (Ferreira and Carmona 1995; Meyer 1996; Bolland et al. 1998; Bonato 1999; Ferragut and Escudero 1999; Kreiter et al. 2002; Knapp et al. 2003; Ho et al. 2004; Duverney et al. 2005; Migeon 2005). It shows a strong preference for solanaceous plants. T. urticae is a cosmopolitan species that attacks a wide range of hosts of different families (Bolland et al. 1998).

Several studies have demonstrated that T. urticae is an acceptable prey to a large number of predatory mites on many different plants (Kostiainen and Hoy 1996), although the suitability of this prey for predatory mites depends on the host plant. For example, a few phytoseiid species can be used to control T. urticae on solanaceous plants. T. evansi, has been shown to be an unfavorable prey to most predatory mites that have been tested against it (Moraes and Lima 1983; Moraes and McMurtry 1985, 1986; Escudero and Ferragut 2005; Rosa et al. 2005). An exception is a Brazilian strain of Phytoseiulus longipes Evans, which seems to be a good predator of that pest species (Furtado et al. 2006, 2007).

Another predator of the same genus, Phytoseiulus fragariae Denmark and Schicha, was recently found in association with T. evansi on Solanum americanum Mill. in Uruguaiana, State of Rio Grande do Sul, Brazil (Furtado et al. 2006). Until then, this predator was only known from Brazil in association with T. urticae, on Fragaria sp. and Bidens pilosa L. (Denmark and Schicha 1983; Takahashi and Chant 1993).

Phytoseiulus fragariae is the least studied of the mites in the genus Phytoseiulus. At 26°C, and using eggs of Tetranychus pacificus McGregor as prey, Takahashi and Chant (1992, 1994) reported it to have longer developmental time and lower reproductive capacity than reported for other species of this genus. However, Fraga (1996) reported that at 27°C and with eggs of T. urticae as prey, P. fragariae has a developmental rate comparable to that of Phytoseiulus macropilis (Banks) (Smith and Summers 1949; Prasad 1967) and Phytoseiulus persimilis Athias-Henriot (Laing 1968; Amano and Chant 1977). The fact that different stages of P. fragariae have been found associated with populations of T. evansi on solanaceous plants in Brazil could indicate that this biotype is a potential biocontrol agent of that pest. Considering that until now a single phytoseiid species has shown potential as a predator of T. evansi (Furtado et al. 2006, 2007), the determination of a second prospective predator would be extremely desirable.

The objective of this paper is to evaluate biological parameters of P. fragariae on T. evansi and T. urticae as prey, at five temperatures, with special reference to evaluate its potential as biocontrol agent against T. evansi on Solanaceae.

Materials and methods

This work was conducted in the Acarology Laboratory of “Departamento de Entomologia, Fitopatologia e Zoologia Agrícola, Escola Superior de Agricultura Luiz de Queiroz (ESALQ)—Universidade de São Paulo”, where voucher specimens of the species used in this study were deposited.

Tetranychus evansi and T. urticae were obtained from colonies that had been maintained in the laboratory for about 5 years before the beginning of the study, on plants of Lycopersicon esculentum var. Kadi GI Mill. and Canavalia ensiformis (L.) DC., respectively. P. fragariae was obtained from a laboratory colony initiated with about 40 specimens (different life stages) collected in Uruguaiana about 6 months before the beginning of the study. The colony of the predator was maintained using an adaptation of the method of McMurtry and Scriven (1965), at 25.5 ± 0.5°C, 88 ± 7% RH and 12:12 h light:dark, and fed T. urticae on leaflets of C. ensiformis.

The study was initiated with newly laid eggs of P. fragariae. To obtain them, groups of about 100 females of the predator were transferred from the stock colony to a leaflet of C. ensiformis infested with T. urticae. Four hours later, single eggs laid by the predator were transferred to the experimental units, repeating this process until 50 eggs per treatment were available. Each experimental unit consisted of a plastic Petri dish (2.6 cm in diameter × 1.0 cm high), whose bottom was covered with a disk of filter paper, onto which a leaf disk (2.0 cm in diameter) of S. americanum infested with all developmental stages of T. evansi or T. urticae was placed. The filter paper was moistened daily with distilled water. Predators were transferred to new units every third day. The upper opening of each unit was sealed with a transparent plastic film (Magipack®). For each prey species, development, adult survival and fecundity were investigated in climatic chambers at 10 ± 0.8, 15 ± 0.8, 20 ± 0.8, 25 ± 0.8 and 30 ± 0.8°C and 12:12 h light:dark. Relative humidity in the experimental units was not controlled, but should be close to saturation, as the units were kept closed and water was added daily to the filter paper disk in it to prevent dehydration of the leaf disk.

During immature development, the experimental units were observed every 8 h, to determine the duration of each developmental stage and the corresponding survivorship. With those data, thermal requirements of each developmental stage and of the whole immature development were calculated, using the coefficient of variation method (Arnold 1959). A male obtained in this study or taken from the stock colony was introduced to each arena containing a recently emerged female. The couple was maintained together up to the end of the study; dead males were replaced by new males. When mites were in the adult stage, observations were carried out every 24 h, to determine the reproductive parameters (preoviposition, oviposition and postoviposition periods as well as daily oviposition) and longevity. The sex ratio of the studied generation was determined based on the eggs laid on the third and fourth day of oviposition. To do that, eggs were transferred individually with a fine brush to a unit similar to that used for the stock colony, which also contained leaflets infested with T. urticae; that unit was maintained under the same condition mentioned for the stock colony. Mites were sexed soon after reaching adulthood. Fertility life tables (Birch 1948; Southwood 1978) were constructed using the method proposed by Maia et al. (2000), which consists on a statistical package developed using the SAS system for Windows®, version 6.12, that uses jackknife to estimate parameters for fertility life tables. At each temperature, averages of each parameter on both prey were compared using Student’s T-test (P ≤ 0.05). Regression equations were calculated to relate the variation of each evaluated parameter with the variation in temperature.

Results and discussion

Immature development

A rather erratic pattern was observed for the variation of survivorship rates of the whole immature phase of the predator at the different temperatures when prey was T. evansi; a quadratic equation significantly described the relation between those parameters (R 2 = 73.7%). When prey was T. urticae, survivorship progressively increased with increasing temperatures; a quadratic response curve fitted the observed data (R 2 = 77.7%). At all temperatures, survivorship was lower on T. evansi than on T. urticae. When prey was T. evansi, mortality of the whole immature phase was very high at 10°C; it was low in the egg stage, but high in the larval stage and very high in the protonymphal stage; none of the predators that succeeded in completing the latter stage was able to complete the deutonymphal stage on this prey. Even on T. urticae, only about a third of the predators reached the adult stage at that temperature (Table 1).

Table 1 Durations (days ± SE) of the immature stages, survivorship, equations relating each parameter with temperature, lower threshold temperature of development (t 0) and thermal constant (K), for Phytoseiulus fragariae on Tetranychus evansi and Tetranychus urticae as prey at different temperatures
Full size table

Lower survivorship on T. evansi than on T. urticae was also observed by Escudero and Ferragut (2005) for Neoseiulus californicus (McGregor) and P. persimilis. However, Furtado et al. (2007) observed higher survivorship of P. longipes on T. evansi than on T. urticae.

On both prey species, progressively shorter durations of each immature stage and of the whole immature phase were observed with increasing temperatures (Table 1). In each case, a quadratic response curve fitted the observed data well (R 2 ≥ 86.9%). Duration of the whole immature phase of P. fragariae at 25°C was slightly longer than reported by Takahashi and Chant (1992) and Fraga (1996) at 27°C (5.0 days) and 26°C (4.4 days), respectively.

Significant differences were not observed concerning the duration of the larval stage on the different prey at each temperature. Because of poor survivorship of post-larval stages of P. fragariae at 10°C, no comparisons were carried out concerning the duration of subsequent preimaginal developmental stages at this temperature. At other temperatures, differences were always significant for the post-larval stages, except for the protonymphal stage at 25°C; in other cases, development was always faster when the prey was T. urticae. Congruently, the duration of the total immature developmental time was significantly shorter on T. urticae reared individuals at all tested temperatures. Escudero and Ferragut (2005) also observed shorter duration of the immature phase of P. persimilis on T. urticae than on T. evansi. However, Furtado et al. (2007) did not find a significant effect of these two prey species on the duration of the immature phase of P. longipes.

Also because of the low survivorship of post-larval stages of P. longipes at 10°C, only data at higher temperatures were used in the determination of thermal requirements of those stages and of the whole immature phase when prey was T. evansi. For the whole immature development of P. fragariae, calculated lower threshold temperature for development (t 0) was 8.4 and 8.0°C on T. evansi and T. urticae, respectively (Table 1). However, because of high mortality at the protonymphal stage at 10°C, the higher values of the threshold for that stage (t 0 = 10.3 on T. evansi and 8.7°C on T. urticae) should be considered as the actual limiting values. The calculated lower threshold temperature for the protonymphal stage on T. evansi was close to the value determined by Badii and McMurtry (1984) for P. longipes on T. pacificus (10.8°C) but lower than the value determined by Silva et al. (2005) for P. macropilis on T. urticae (12.7°C).

The slower rate of development of P. fragariae on T. evansi resulted in a slightly higher thermal requirement (103.9 degree-days) on that prey than on T. urticae (97.1 degree-days). On both prey, the requirement was considerably higher than that reported by Badii and McMurtry (1984) for P. longipes (75.9 degree-days) and by Silva et al. (2005) for P. macropilis (66.0 degree-days).

Reproduction

Similarly to what was reported for immature development, on both prey species, progressively shorter durations of preoviposition, oviposition and postoviposition periods as well as adult female longevity were observed with increasing temperatures (Table 2). With one exception, the relation between the duration of these phases and temperature was linear (R 2 ≥ 87.5%); on T. evansi, the relation of the oviposition period to temperature levels corresponded to a quadratic function (R 2 = 91.3%). In relation to adult male longevity, significant response curves were quadratic on T. evansi and linear on T. urticae (R 2 = 91.1% and 88.9%, respectively).

Table 2 Durations (days ± SE) of the preoviposition, oviposition, postoviposition and longevity, fecundity (eggs/female ± SE) and sex ratio (% females) of Phytoseiulus fragariae on Tetranychus evansi and Tetranychus urticae as prey at different temperatures
Full size table

On both prey, slightly lower fecundity were progressively observed with increasing temperatures; in both cases, the relation between that parameter and temperature was linear (R 2 nearly 98%). For unknown reason, the variation of sex ratio was quite different on different prey along the range of temperatures considered in the study. On T. evansi, sex ratio increased from 15 to 20°C and decreased from 25 to 30°C (R 2 = 87.0% for a quadratic response). The trend was exactly the opposite on T. urticae (R 2 = 72.5% for a quadratic response) (Table 2).

The preoviposition period was significantly longer on T. evansi, except at 15°C. On the same prey, the oviposition period and female longevity were shorter, and total fecundity was lower than the respective values recorded for the T. urticae reared individuals at all temperatures. This suggests that T. urticae is a more suitable prey for P. fragariae than T. evansi. The total fecundity determined in the present study on T. urticae are slightly lower than those observed by Takahashi and Chant (1994) but much lower than observed by Fraga (1996), at comparable temperatures.

The postoviposition period was significantly longer for predators fed T. evansi at 30°C. An irregular pattern was observed when comparing adult male longevity, probably because of the low numbers of males at each temperature on either prey.

Moraes and McMurtry (1986) and Escudero and Ferragut (2005) also reported less favorable reproductive parameters for P. persimilis when prey was T. evansi than when it was T. urticae. Furtado et al. (2007) observed the opposite for P. longipes. In that case, although the oviposition period was similar on both prey, fecundity was higher when it was fed T. evansi.

On both prey, sex ratio of the progeny of the mites reared at the different temperatures was higher than 75% [females/(females + males)] at 20, 25 and 30°C, but only 57.5% on T. evansi at 15°C, suggesting a possible disturbance of the pseudo-arrhenotoky process of predators reared at relatively low temperature and fed an apparently unfavorable prey, resulting in the production of a proportionally higher number of sons (Sabelis and Nagelkerke 1988). Takahashi and Chant (1994) and Fraga (1996) reported sex ratios of about 80% for this predator. Escudero and Ferragut (2005) reported a sex ratio of nearly 50% for P. persimilis and N. californicus fed T. evansi and 73% when the same predators were fed T. urticae. Conversely, Furtado et al. (2007) reported sex ratio of nearly 90% for P. longipes fed either of those prey.

Fertility life table

Concurrently with what was reported for duration of each immature stage and each adult phase (preoviposition, oviposition and postoviposition), calculated generation time (T) was progressively shorter with increasing temperatures on both prey, the observed data fitting well quadratic response curves (R 2 = 95.4% on T. evansi and 97.3% on T. urticae) (Table 3). At 15 and 20°C, T values were significantly lower on T. evansi, but no differences were observed at 25 and 30°C. The values of net reproduction rate (R 0), intrinsic rate of increase (r m ) and finite rate of increase (λ) generally increased with increasing temperatures, except for R 0 on T. evansi, which increased up to 25°C but then decreased at 30°C (R 2 = 77.6–81.7% for R 0 and higher than 97% for the other two parameters). The positive values of those parameters indicated that the population of P. fragariae can increase on both prey. However, the values were significantly higher on T. urticae, indicating faster population increase of the predator. The low capacity for population growth of P. fragariae on T. evansi was due to the small production of offsprings, with low net reproduction values R 0 at all tested temperatures. The net reproduction rate determined at 25°C in this study was about half as high as reported by Fraga (1996), but comparable to that determined by Takahashi and Chant (1994). At 25°C, when prey was T. evansi, net reproduction rate was much lower for P. persimilis (Escudero and Ferragut 2005) but much higher for P. longipes (Furtado et al. 2007) than reported for P. fragariae in this study.

Table 3 Life table parameters (± confidence interval) of Phytoseiulus fragaria e on Tetranychus evansi and Tetranychus urticae as prey at different temperatures
Full size table

Although the results of this study showed a better performance of P. fragariae as a predator of T. evansi than the species studied by Moraes and McMurtry (1985) and Escudero and Ferragut (2005), it seems that it cannot be considered a good predator of that pest. The results of Furtado et al. (2007) are much more encouraging, and showed a much better performance of P. longipes on the same pest. Conversely, the results suggest that P. fragariae is a promising control agent of T. urticae. However complementary studies should be conducted to determine whether it could also be effective on solanaceous plants, had that prey developed for successive generations on such type of substrate.