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Experimental and Applied Acarology 34: 263–273, 2004. 2004 Kluwer Academic Publishers. Printed in the Netherlands.

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Prey stage preference and functional response of Euseius hibisci to Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) MOHAMMAD H. BADII1,*, EMILIO HERNAŃDEZ-ORTIZ2, ADRIANA E. FLORES1 and JEROŃIMO LANDEROS3 1

Autonomous University of Nuevo Leon, Ap. 391, San Nicolas, N.L., 66450, Mexico; 2Programa Moscamed SAGAR-CONASAG, Tapachula, Chiapas, Mexico; 3UAAAN, Saltillo, Coahuila, Mexico; *Author for correspondence (e-mails: [email protected]) Received 7 January 2003; accepted in revised form 6 July 2004

Key words: Alternative food, Euseius hibisci, Functional response, Predation, Strawberry, Tetranychus urticae Abstract. The aims of this study were: (a) determine the prey stage preference of female Euseius hibisci (Chant) (Phytoseiidae) at constant densities of different stages of Tetranychus urticae Koch (Tetranychidae), (b) assess the functional response of the predator females to the varying densities of eggs, larvae, or protonymphs of T. urticae, and (c) estimate the functional response of E. hibisci when pollen of Ligustrum ovalifolium was present as well. We conducted experiments on excised pieces of strawberry leaf arenas (Fragaria ananassa) under laboratory conditions of 25 ± 2 C, 60 ± 5% RH and 12 h photophase. Our results indicated that the predator consumed significantly more prey eggs than other prey stages. Consumption of prey deutonymphs and adults was so low that they were excluded from the non-choice functional response experiments. The functional response on all food items was of type II. The two parameters of the functional response were estimated for each prey type by means of the adjusted non-linear regression model. The highest estimated value a¢ (instantaneous rate of discovery) and the lowest value of Th (handling time, including digestion) were found for the predator feeding on prey eggs, and a¢ was lowest and Th highest when fed protonymphs. Using the jack-knife method, the values for the functional response parameters were estimated. The values of a¢ and Th produced by the model were similar among all prey types except for the eggs, which were different. Using pollen simultaneously with prey larvae decreased the consumption of the latter over the full range of prey densities The suitability of this predator for biological control of T. urticae on strawberry is discussed.

Introduction Two-spotted spider mite, Tetranychus urticae Koch, is the key mite pest species on strawberry plants in Mexico (Badii et al. 2002). Strawberry (Fragaria ananassa) is cultivated in the field on an area of 2700 ha, part of an agricultural region called Bajio, which covers sections of the three states Michoacan, Guanajuato and Jalisco, in central Mexico (SAGARPA 2001). The mean annual production of strawberry in the Bajio region is 100,000 metric tons (SAGARPA 2001). This mite reduces the strawberry yield by 10–15% in California (Oatman et al. 1985) and up to 50% in Florida (Wysoki 1985).

264 Chemical control is the main method of combating this mite pest. However, due to the excessive use of agrochemicals, pesticide resistance and environmental pollution have developed, which in turn have rendered this control method inefficient. An alternative and ecologically sound control measure against this mite is the utilization of predaceous mites as control agents. Phytoseiulus persimilis Athias-Henriot is the phytoseiid species most used worldwide for biological control of T. urticae (Sabelis 1985; McMurtry 1992; McMurtry and Croft 1997; Garcia-Mari and Gonzalez-Zamora 1999; Badii et al. 2000). Phytoseiulus persimilis does not occur in strawberry fields in Mexico and in fact, does not occur naturally in the country (Badii et al. 2002). Garcia (1990) recorded the following 11 species of Phytoseiidae on strawberries in Bajio: Euseius hibisci (Chant), Neoseiulus brevispinus (Kennett), N. comitatus (De Leon), N. fallacis (Garman), N. mumai (Denmark), Proprioseiopsis asetus (Chant), P. exopodalis (Kennett), P. rotundus (Muma), Typhlodromalus peregrinus Muma, Typhlodromus annectens De Leon and T. flumensis Chant. Among these species, E. hibisci is the most abundant predaceous mite in the strawberry-growing area of Zamora (Michoacan). It is commonly associated with T. urticae, both on strawberries and on castor bean (Ricinus communis) surrounding the strawberry plants. This predaceous mite also feeds on pollen and other insect pests such as various instars of whitefly (Bemisia argentifolii) (Badii et al. 2002), and hence it is a so-called type IV predator [following the classification by McMurtry and Croft (1997)]. Much research has focused on the effect of specialized phytoseiids on T. urticae populations, but some has involved the impact of non-specialist phytoseiid mites (McMurtry 1992; Fan and Petitt 1994; McMurtry and Croft 1997). The option to use E. hibisci in an augmentative manner against the twospotted spider mite motivated us to carry out the present investigation. We designed experiments to gain insight into the potential capability of this indigenous predator for control of T. urticae on strawberry, as part of an integrated pest management program. The aims of the investigation were: (a) to measure the consumption rate of E. hibisci on different stages of the prey offered at constant densities, (b) to estimate the functional response of this phytoseiid mite to the varying densities of eggs, larvae and protonymphs of T. urticae, and (c) to assess the functional response to larvae in the presence of the pollen of Ligustrum ovalifolium trees, which are used as wind breaker as well as ornamental plants around most row crops in Mexico and hence are easily available.

Material and methods We collected E. hibisci from castor bean (R. communis) surrounding strawberry fields, and the prey, T. urticae, from strawberry leaves in the study area. Both prey and predator species were maintained for several generations

265 on strawberry leaf arenas (Badii et al. 1999) placed underside up on water-saturated foam mats located in aluminum cake pans in the environmental chambers at 25 ± 2 C. 60 ± 5% RH and 12 h photophase. We surrounded leaf arenas with strips of tissue paper in order to minimize the escape of the individual mites. In the consumption tests, we offered a total of 250 prey items i.e. equal number (50) of newly emerged individual eggs, larvae, protonymphs, deutonymphs and adults of two-spotted spider mite to a 24 h starved three-dayold mated female predator on 2 · 2 cm2 excised strawberry leaf arenas (McMurtry and Scriven 1964). We then allowed each predator to feed on the prey items for a total of 24 h, at the end of which we estimated the number of prey individuals consumed per predator per day. Each leaf arena was replicated 60 times. Functional response experiments were also conducted on 2 · 2 cm2 excised strawberry leaf arenas. Small pieces of plastic cover slips with strands of cotton underneath were placed on the leaf arenas to simulate the underside of the leaves for the predator species (Badii and McMurtry 1988). A three-dayold mated female predator, that had been starved for 24 h immediately prior to the experiments, was exposed to densities of 1, 2, 4, 8, 16, or 32 newly emerged individuals of different prey items (egg, larva, and protonymph, constituting three treatments). Similar densities of larvae plus equal amounts by weight of L. ovalifolium pollen were used as a fourth treatment. Each density was replicated 15 times. The exposure time was 24 h after which we counted the spider mite individuals eaten. Prey items consumed were replaced at the end of 2, 4, 6, 8, 10, and 12 h, assuming that the highest intensity of prey consumption occurs during the first half of the total exposure period. The frequency of replacement was chosen because E. hibisci does not hunt its prey as intensively as other phytoseiid species, e.g. of the genus Phytoseiulus, and because the observed period between two attacks is more than 1 h. To estimate and analyze the functional response parameters, we employed the non-linear regression model (SAS Institute 1985; Juliano and Williams 1987). Whereas a variety of methods are at hand, the following points support the use of the non-linear estimation of Holling’s disc equation: (1) small prey depletion relative to the number of prey present, except at the lowest prey density, (2) closer match among the observed and the expected prey numbers attacked for all food items obtained by non-linear estimations, and (3) higher reliability of non-linear parameter estimation than those based on linearization (Juliano and Williams 1987). Means and variances of the instantaneous rate of discovery (a¢) and handling time (Th) were estimated based on the jack-knife method as follows (Quenouille 1956). It should be realized that predation by phytoseiid mites is generally not limited by handling time per se, but by digestion rate (e.g. Sabelis 1985). This implies that Th as used in this paper also includes prey digestion time. We calculated 15 partial values for each parameter with n 1 replicates. We then converted these partial values into pseudovalues using the following equations:

266 VPa0 i ¼ na0T ½ðn 1Þa0pi ; VPThi ¼ nThT ½ðn 1ÞThpi ; where VP a¢ [Th]i is the pseudovalue of a¢ [Th] for the ‘ith’ replicate; n the number of replicates; a¢ [Th]T is the total a¢[Th] estimated with n replicates; and a¢[Th]pi is the partial a¢[Th] estimated for ‘ith’ replicate, with n 1 replicates. Once we estimated the pseudovalues for a¢ and Th, we calculated the means and standard errors of these values. The mean of all pseudovalues is the best estimate of each predation parameter (a¢ and Th). A set of 15 pseudovalues constituted the replicates for a predation parameter. Finally, we analyzed the data by means of the Kruskal–Wallis (non-parametric ANOVA) test and the mean separation test of Newman–Keuls (p £ 0.05, Zar 1996) to calculate any possible differences between the means of each parameter among the food items. Results and discussion Consumption capacity of Euseius hibisci on Tetranychus urticae The mean consumption rates of E. hibisci females differed between the various prey stages, but not between deutonymphs and adults (Table 1). Prey consumption was inversely related to prey size: the predators consumed mostly eggs (4.1 items/day), followed by prey larvae (3.4) and protonymphs (2.3). Consumption of deutonymphs (0.033) or adults (0.016) was very rare – these numbers actually represent the consumption of just two deutonymphs and only one adult out of 50 initial individuals per 60 replicates. The predators removed only about 8, 7, 4.6, 0.7 and 0.3% of the total number of prey eggs, larvae, protonymphs, deutonymphs and adults, respectively (Table 1).

Functional response of Euseius hibisci on different food items Because the consumption tests (Table 1) revealed that E. hibisci consumed practically zero deutonymphs or adults, we excluded these prey stages from the functional response experiments, and only utilized the three remaining prey instars: eggs, larvae, and protonymphs. We also added a fourth treatment, prey larvae combined with pollen of L. ovalifolium, to assess the effect of pollen on the consumption of prey. The form of the functional response on all food items was a curvilinear rise (type II of Holling and typical of invertebrate predators) approaching a plateau at higher prey densities (Figure 1). The observed consumption per predator per day is given in Table 2. Statistical analysis indicated that there is a significant fit (X2 goodness of fit test, p £ 0.05) between the observed and expected numbers of prey killed per predator, for every prey stage tested.

267 Table 1. Euseius hibisci consumption of immature stages of Tetranychus urticae: mean consumption (numbers of items per day) and proportion consumed (Na/No; Na – prey number attacked per predator; No – initial prey number). Prey stages

Mean ± SE*

Na/No

Egg Larva Protonymph Deutonymph Adult

4.087 3.412 2.334 0.033 0.016

0.081 0.068 0.046 0.007 0.003

± ± ± ± ±

0.115a 0.134b 0.167c 0.181d 0.126d

*Mean values followed by a different letter are significantly different from each other (n = 60, Kruskal–Wallis and Newman–Keuls tests, p £ 0.05). SE – standard error.

Figure 1. Observed functional response of Euseius hibisci females to densities of eggs, larvae or protonymphs of Tetranychus urticae, or to T. urticae larvae plus Ligustrum ovalifolium pollen.

The lowest consumption is noted for the protonymphal stage. Comparing the plateaus of the functional response curves in these experiments, we find that E. hibisci consumed a little over seven prey eggs at the highest initial prey density of 32 (Figure 1, Table 2), At the same initial prey density (Table 2), the

268 Table 2. Observed mean consumption (±standard error; Nao – number of prey items per female Euseius hibisci per day), proportion killed (Na/No), and expected consumption based on an adjusted non-linear (NaeNL) model for each of four diets: Tetranychus urticae eggs, larvae, protonymphs and larvae + Ligustrum ovalifolium pollen (theoretical X20.05,5 = 11.07). No

Nao ± SE

Egg 1 0.600 ± 0.13 2 1.400 ± 0.19 4 2.667 ± 0.30 8 3.533 ± 0.36 16 5.933 ± 0.60 32 7.067 ± 0.62 Calculated X2 = 0.1080 Mean proportion consumed = 0.498 Larva 1 0.533 ± 0.13 2 0.867 ± 0.13 4 1.800 ± 0.20 8 2.200 ± 0.24 16 3.733 ± 0.51 32 5.067 ± 0.43 Calculated X2 = 0.1269 Mean proportion consumed = 0.346 Protonymph 1 0.467 ± 0.13 2 0.667 ± 0.13 4 1.533 ± 0.19 8 1.667 ± 0.21 16 2.533 ± 0.31 32 3.800 ± 0.49 Calculated X2 = 0.2773 Mean proportion consumed = 0.276 Larva + pollen 1 0.400 ± 0.13 2 0.933 ± 0.21 4 1.267 ± 0.18 8 1.933 ± 0.23 16 2.600 ± 0.27 32 3.467 ± 0.32 Calculated X2 = 0.0620 Mean proportion consumed = 0.266

Na/No

NaeNL

0.60 0.70 0.66 0.44 0.37 0.22

0.751 1.396 2.447 3.925 5.621 7.171

0.53 0.43 0.45 0.28 0.23 0.16

0.433 0.819 1.478 2.470 3.719 4.976

0.47 0.33 0.38 0.21 0.16 0.11

0.328 0.616 1.099 1.807 2.666 3.496

0.40 0.47 0.32 0.24 0.16 0.11

0.400 0.734 1.259 1.959 2.712 3.357

consumption of protonymphs and of larvae + pollen was approximately half that of the eggs, whereas the consumption of prey larvae was 30% lower than that of eggs. The analysis of the proportion of each prey item consumed by the predators (Table 2) revealed that the proportions declined as an increasing function of the initial prey densities. Furthermore, the average proportions of prey consumed by the predator across all initial densities were 0.27, 0.28, 0.35 and 0.50

269 on larvae + pollen, protonymphs, larvae and eggs, respectively (Table 2). In other words, the female predator removed approximately half of the prey eggs, a little over a third of the larvae and almost 28% of the protonymphs of the two-spotted spider mite. The addition of pollen as supplemental food reduced the consumption of prey larvae by the predator by about 32%. The mean and standard error values of the instantaneous rate of discovery (a¢) and handling time (Th, including digestion time) are given in Table 3. These values are estimated based on the jack-knife method (Quenouille 1956). The non-linear regression model produced statistically higher values of a¢ for the egg stage in comparison with the other food items. The 95% confidence intervals (CI) for a¢ on the egg stage are wider compared to those of the other food items, whereas, there is no overlap between the CI-values for a¢ on the egg in comparison with those on protonymph, as well as larva plus pollen (Table 3). The CI-values for larvae overlap those of the rest of the food items. In general terms, these results indicate that E. hibisci has a higher attack rate on the eggs in comparison with other food items and an equal attack rate on the larvae, protonymphs and larvae + pollen. The values of a¢ had an inverse relationship with the size of the prey stage (Table 3). This might be explained by: (1) prey items with little or no mobility are easier to handle and to subdue, or (2) an innate tendency for this predator species to prey on smaller prey items. The model generated significantly lower values of Th for prey eggs than for the other diets (Table 3). There is overlap between the CI-values among protonymphs and larvae + pollen, protonymphs and larvae, but not among larvae + pollen and those of eggs and larvae (Table 3). Based on Table 3, the egg and larval stages could be clustered into one category (relatively easy to handle), and protonymph and larvae + pollen into another (relatively hard to

Table 3. Mean estimated values of a non-linear regression model (±SE), and confidence intervals, of the instantaneous rate of discovery (a¢) and handling time (Th, including digestion time) for each of four diets of Euseius hibisci: Tetranychus urticae eggs, larvae, protonymphs and larvae + Ligustrum ovalifolium pollen. Diet

Non-linear regression*

Instantaneous rate of discovery (a¢) Egg 0.813 ± 0.114a Larva 0.460 ± 0.077b Protonymph 0.351 ± 0.131b Larva + Pollen 0.441 ± 0.082b Handling time (Th) Egg 0.101 ± 0.015a Larva 0.133 ± 0.024b Protonymph 0.197 ± 0.060c Larva + Pollen 0.227 ± 0.031c

Confidence interval

0.5695–1.0441 0.3141–0.6166 0.1637–0.5670 0.3256–0.5681 0.0792–0.1221 0.0952–0.1693 0.1056–0.2726 0.1871–0.2655

*Mean values in each column followed by different letters are significantly different from each other (Neuman–Keuls, p £ 0.05).

270 handle). Probably E. hibisci eats fewer larvae in presence of pollen, because it prefers pollen over spider mites, like all Euseius species (McMurtry and Croft 1997). Much work has been conducted on P. persimilis and many other phytoseiid species used for biological control of pest mites on strawberry. The prey consumption capacity of P. persimilis on T. urticae is substantially higher than that of any type IV (pollen feeder and generalist predator) phytoseiid mite species (McMurtry and Croft 1997). Phytoseiulus persimilis in particular has been used extensively against T. urticae, providing good biological control on strawberry under suitable environmental conditions (Wysoki 1985; Benuzzi et al. 1992; Easterbrook 1992; Decou 1994). In addition to specialist predators, other phytoseiid species with type II life style (selective predators, sensu McMurtry and Croft 1997), such as Neoseiulus californicus (McGregor), N. fallacis, Thyphlodromus occidentalis Nesbitt, and Typhlodromus pyri Scheuten, have also been used for biocontrol of two-spotted spider mite on strawberries (Wysoki 1985; Coop and Croft 1995; Zacharda and Hluchy 1997; Garcia-Marie and Gonzalez-Zamora 1999). Several authors have studied the functional responses of generalist predatory mites on T. urticae. For example, Neoseiulus barkeri Hughes displayed a functional response of type II on increasing densities of eggs, larvae and adults of two-spotted spider mite on pepper discs under the conditions of 25 C, and 70–80% RH (Fan and Petitt 1994). The number of prey eggs and larvae consumed by the predator are at least twice as much as the number of prey killed at similar initial prey densities by E. hibisci in our experiments (Table 2). The values of a¢ and Th found by Fan and Petitt (1994) in comparison to our data (Table 3), indicate higher attack rates and lower handling times for N. barkeri on each immature stage of the prey. Shih and Wang (2001) assessed the a¢ and Th values of Amblyseius ovalis (Evans) females on increasing densities of different stages of T. urticae, based on Holling’s disc equation. They used polyethylene substrate, at 25 C, 50% RH and 13L:11D. Their a¢ and Th values were respectively higher and lower than our corresponding values on similar prey stages. Phytoseiid mites with type IV life style (sensu McMurtry and Croft 1997) are generalists and pollen feeders and have a higher reproduction rate when feeding on pollen in comparison to mite prey. Several studies have indicated the relevance of these species as effective biocontrol agents of spider mites and thrips on some crops. For example, E. hibisci on avocado brown mite, Oligonychus punicae (Hirst) on avocado, and Euseius tularensis Congdon on citrus red mite, Panonychus citri (McGregor), and citrus thrips, Scirtothrips citri (Moulton) (Thysanoptera: Thripidae), on citrus (Tanigoshi and Nishio-Wong 1982; McMurtry 1985a, b; Tanigoshi et al. 1985; Congdon and McMurtry 1988). According to McMurtry and Scriven (1964), Tetranychus cinnabarinus (Boisdual), a species closely related to T. urticae, was a less favorable prey for E. hibisci compared to other tetranychid mite species such as P. citri, O. punicae, and Eotetranychus sexmaculatus (Riley). The reason for this was con-

271 sidered to be the hindrance and entanglement of this predator in the copious web network of T. cinnabarinus. McMurtry and Scriven (1964) also found a shorter developmental period and a higher reproduction rate of E. hibisci occurred on pollen (as compared to tetranychid mite) from various plant species. This effect was most pronounced with avocado pollen (Persea Americana), castor bean (R. communis), ice plant (Mesembryanthemum sp.), sweet corn (Zea mays), pepper (Capsicum frutescens), and oak (Quercus agrifolia). Euseius hibisci preferred ice plant pollen to Pacific spider mite, Tetranychus pacificus McGregor, and P. citri (Zhao and McMurtry 1990). In conclusion, although E. hibisci is not a specialized predator of T. urticae, it potentially aids in enhancing control of this mite and other pests on strawberry in Mexico. This predator was found to have moderate and partial impact on spider mite eggs and immatures. Our data come from simple laboratory trials where no or very little web was produced; in the field, however, spidermite web surrounds practically all prey stages. Type IV phytoseiid predators such as E. hibisci are not comfortable with web. Therefore, we must take great caution in directly translating our laboratory results into the field conditions. We consider E. hibisci as an auxiliary and potential biocontrol agent that could, in augmentative release programs, aid in achieving biological control of T. urticae on strawberry in Mexico, in combination with imported specialized and effective predatory mites such as P. persimilis. Perhaps this added benefit can emerge from the fact that E. hibisci is likely to remain longer on the plant than a specialized predator such as P. persimilis, and hence could at least partially counteract the resurgence and rapid recolonization of the plant by T. urticae populations. Needless to say, this hypothesis needs experimental testing.

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