Biological Control 60 (2012) 39–45

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Biological Control

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Variability in response of four populations of largoensis (: ) to indica (Acari: ) and Tetranychus gloveri (Acari: Tetranychidae) eggs and larvae ⇑ Daniel Carrillo a, , Martha E. de Coss b, Marjorie A. Hoy c, Jorge E. Peña a a University of Florida, Department of Entomology and Nematology, Tropical Research and Education Center, Homestead, FL 33031, USA b Universidad Autónoma de Chiapas, Terán Tuxtla Gutiérrez, Chiapas, CP 29050, Mexico c University of Florida, Department of Entomology and Nematology, Gainesville, FL 32611, USA highlights graphical abstract

" with different previous exposure to Raoiella indica were tested. " Predators consumed high numbers of R. indica eggs regardless of previous exposure. " Experienced predators consumed more R. indica larvae than naïve predators. " Plasticity in response could be associated to genetic selection, learning, or both. " Implications for biological control of the invasive species R. indica are discussed. article info abstract

Article history: Raoiella indica (Acari: Tenuipalpidae) is a phytophagous that recently invaded the Neotropical Received 24 May 2011 region. A predatory mite Amblyseius largoensis (Acari: Phytoseiidae) has been found associated with R. Accepted 2 September 2011 indica in Florida. This study evaluated A. largoensis by determining its likelihood of consuming eggs Available online 10 September 2011 and larvae of R. indica and Tetranychus gloveri (Acari: Tetranychidae) under no-choice and choice condi- tions. To detect variations in the response of A. largoensis to R. indica, four populations of predators were Keywords: examined: (1) predators reared exclusively on R. indica in the laboratory for 2 years, (2) predators reared Invasive species on T. gloveri in the laboratory for 2 months but reared on R. indica for 2 years previously, (3) predators Raoiella indica collected from a field infested with R. indica, and (4) predators collected from a field that had never been Amblyseius largoensis Learning infested with R. indica. Results of this study suggest that A. largoensis is likely to accept and consume high Selection numbers of R. indica eggs regardless of their previous feeding experience. In contrast, all populations con- sumed relatively fewer R. indica larvae than the other prey tested. Predators previously exposed to R. indica were more likely to consume R. indica larvae. By contrast, predators not previously exposed to R. indica showed the lowest likelihood of choosing to feed on this prey item. Plasticity in the response of A. largoensis to R. indica larvae could be associated to selection, learning, or a combination of both. The possible implications of the observed differences in terms of biological control of R. indica are discussed. Ó 2011 Elsevier Inc. All rights reserved.

⇑ Corresponding author. Fax: +1 305 2467003. E-mail address: dancar@ufl.edu (D. Carrillo).

1049-9644/$ - see front matter Ó 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2011.09.002 40 D. Carrillo et al. / Biological Control 60 (2012) 39–45

1. Introduction 2. Materials and methods

Raoiella indica Hirst (Acari: Tenuipalpidae) is a phytophagous 2.1. General experimental procedures pest native to tropical and subtropical areas of Asia that recently invaded the Neotropical region (Etienne and Flechtmann, 2006; Experiments were conducted at 26.5 ± 1 °C, 70 ± 5% RH under a Vásquez et al., 2008; Marsaro et al., 2009). This mite is a multivol- 12:12 L:D photoperiod. The experimental arenas consisted of rect- tine and gregarious species that can reach high population densi- angles (4 2.5 cm) cut from mature unblemished (Cocos ties and cause significant damage to a variety of plant species, nucifera L.) leaves. Leaf rectangles were placed with the abaxial especially palms (). Establishment of this invasive spe- surface facing up on cotton squares (6 6 2 cm) saturated with cies in the Neotropical region has given rise to concerns about its water in a plastic tray (hexagonal polystyrene weighing dishes potential impact on a number of economically and ecologically 12.7/8.9 cm, FisherbrandÒ Cat. No. 02-202-103). Paper strips important plants (Carrillo et al., in press). (KimwipeÒ, Kimberly–Clark Corporation, Roswell, GA) were placed Efforts were undertaken to identify and evaluate potential along the edges of the leaf squares to minimize mite escape. A biological control agents of R. indica in the Neotropical region small plastic square (0.5 0.5 cm) was placed on top of each arena (Peña et al., 2009; Carrillo et al., 2010). The predatory mite as a shelter for A. largoensis. Amblyseius largoensis Muma (Acari: Phytoseiidae) has been found associated with R. indica in several areas of recent invasion 2.2. Prey including Florida, , , Colombia, Cuba, and Mexico. Moreover, this predator has been found asso- The two prey species, R. indica and T. gloveri, were obtained from ciated with R. indica in (Taylor et al., in press), stock colonies reared on potted coconut palms kept in separate (Gallego et al., 2003), and Dominica (Hoy, personal greenhouses following the procedure previously described (Carrillo communication), Benin and Tanzania (Zannou et al., 2010). It et al., 2010). Eggs of both prey were obtained by placing 100 ovipos- would be important to know if all the predators identified as iting females on each arena and allowing them to deposit eggs for A. largoensis are equally efficient natural enemies of R. indica. 5 days. After this period the females were removed and the desired The geographically diverse distribution of this phytoseiid number of eggs adjusted by removing excess eggs with a fine brush. suggests that strains, biotypes, or cryptic species could exist In the case of T. gloveri, extensive webbing resulted from the (Noronha and Moraes, 2004; Bowman, 2010), and that crowded conditions of females on the ovipositing arenas. Such differences in predatory behaviors among the various popula- extensive webbing is not observed under ‘natural’ field conditions, tions of A. largoensis could affect their propensity to feed on R. so a layer of webbing was carefully removed to expose T. gloveri eggs indica, as has been found for other phytoseiid species. and allow more common conditions for A. largoensis to access its Previous studies suggested that R. indica can be considered an prey. Larvae of both prey species were transferred from the stock appropriate prey for Florida populations of A. largoensis in terms colonies onto the arenas according to the desired prey ratios. Arenas of its reproductive success and consumption rates (Carrillo et al., with two prey species had an additional moistened paper strip on 2010; Carrillo and Peña, in press). The predator also showed good the mid vein of the leaf to allow separate placement of prey, but developmental and reproductive parameters when feeding on Tetr- the strip was removed just before releasing the predators. anychus gloveri Banks (Acari: Tetranychidae) (Carrillo et al., 2010). However, all previous experiments were conducted offering prey 2.3. Predatory mites in a no-choice condition. In the present study, A. largoensis was of- fered the choice between eggs and larvae of R. indica and T. gloveri, Four populations of A. largoensis from Florida with different which represents a more realistic test for this predator that has to feeding histories (previous diet) were used. Two populations were choose among prey found on coconut leaves in Florida. laboratory colonies that had been fed different diets (following Knowledge of the mechanisms that underlie prey acceptance the procedures previously described, Carrillo et al., 2010). The first and choice in predatory mites has recently expanded. Studies on colony had been fed exclusively with R. indica for more than 2 years the predatory mites Hypoaspis aculeifer (Canestrini) (Acari: Laelap- and will be referred to as the R-colony. This colony was initiated in idae) and persimilis Athias-Henriot (Acari: Phytoseii- November 2008 with 150 predators obtained from a coconut palm dae) demonstrated that foraging traits and prey preferences plantation (Malayan dwarf variety, pesticide-free, 26°02.93 N, could be genetically determined and that genetic polymorphism 80°09.82 W) that had been infested with R. indica since 2007. Indi- may occur within local populations (Lesna and Sabelis, 1999, viduals collected from the same site and confirmed as A. largoensis 2002; Jai et al., 2002; Tixier et al., 2010). In addition, there is were added to the colony (10 females/rearing plate) every increasing evidence suggesting that learning plays an important 6 months. The second laboratory colony was initiated with 50 fe- role in prey recognition and acceptance in phytoseiid mites males obtained from the R-colony which were subjected to a diet (Rahmani et al., 2009; Schausberger et al., 2010). Until now all shift from R. indica to T. gloveri 2 months prior to testing, which information on predation by A. largoensis upon R. indica is limited would have allowed the predators to have undergone approxi- to a single population of predators that was collected from a coco- mately six generations on the new diet. This colony will be referred nut plantation in Florida in 2007 and used to initiate a laboratory to as the T-colony. The other two populations were collected from colony. Because prolonged laboratory rearing could affect the prey coconut palm plantations and maintained in the laboratory for preference of phytoseiid mites (Mwansat, 2001), it is important to 1 week prior to testing on arenas constructed with the same leaves determine whether other populations of A. largoensis could and prey that were present at the time they were collected. The first respond differently to R. indica. field population was obtained from the same coconut plantation This study was designed to determine whether the feeding his- where 2 years before A. largoensis was obtained to initiate the R- tory of Florida populations of A. largoensis could influence their colony and will be referred to as the experienced field population likelihood of utilizing the invasive R. indica as prey. To detect pos- because of its long-term previous exposure to R. indica, although sible behavioral plasticity in the response of A. largoensis to R. indi- we cannot exclude the possibility that this population fed on pollen ca this study evaluated four populations of A. largoensis that had and T. gloveri, as well. The second field population was collected different feeding histories (experience feeding on R. indica). from a pesticide-free coconut plantation (Malayan dwarf variety) D. Carrillo et al. / Biological Control 60 (2012) 39–45 41 that had never been infested with R. indica (25°35.49 N, normality of data. The likelihood of choosing one prey item over 80°04.03 W, Tropical Research and Education Center, University another (choice experiments) was quantified using the preference of Florida, Homestead) and will be referred to as the naïve field pop- index b proposed by Manly et al. (1972): ulation for its lack of previous exposure to R. indica. The naïve field 2 31 N0 population was approximately 80 km away from any A. largoensis ln 0 4 Nc 5 population that could have fed on R. indica and most likely, it had b ¼ þ 1 ln N fed on pollen, T. gloveri, Oligonychus aff. modestus and Oligonychus Nc sp. (Acari: Tetranychidae); Nipaecoccus nipae (Maskell) (Hemiptera: where N and N0 are the numbers of each prey-stage provided and N Pseudococcidae); Aonidiella orientalis (Newstead) (Hemiptera: c and N0 are the numbers of each prey consumed. The index assigns Diaspididae); and Aleurocanthus woglumi Ashby (Hemiptera: Aley- c preference values from 0 to 1, where 0.5 represents no preference. rodidae) (Peña et al., 2009; Carrillo et al., 2010). Mean b-values were considered significant when 95% confidence intervals based on the t-distribution did not overlap with b = 0.5. 2.4. No-choice tests Preference (b) values were normally distributed (Kolmogorov– Smirnov P > 0.05) and had homogeneous variances (Levene test No-choice tests were included to ensure that each population of P > 0.05) in the experiments involving choice between R. indica lar- predators could feed on R. indica and T. gloveri and to determine vae and T. gloveri eggs or larvae. Differences in the prey preference whether feeding experience and laboratory rearing could affect (b) among the four populations of A. largoensis were analyzed prey consumption. Predators from the four populations were of- through ANOVAs and means separated by Tukey’s test. Data of fered separately 50 eggs or 50 larvae of either R. indica or T. gloveri. the experiments involving choice tests between R. indica eggs and The number of prey offered was chosen based on a previous study T. gloveri eggs or larvae were not normally distributed, so Krus- in which A. largoensis showed a maximum prey consumption of 45 kal–Wallis tests were used in this case. R. indica eggs/day (Carrillo and Peña, in press). Our experiments did not involve a test with R. indica nymphs and adults as prey. How- 3. Results ever, previous studies indicated that female A. largoensis (i.e., the R- colony) had difficulty handling nymphs or adults and consumed Prey survival in the absolute controls was always greater than significantly more R. indica eggs or larvae than nymphs and adults 95%, which ensures that mortality in the choice and no-choice (Carrillo and Peña, in press). No choice experiments were repli- experiments was caused by predation by A. largoensis females. cated 10 times. In addition, 10 absolute controls consisting of are- nas with prey but without predators were included to ensure that mortality was caused by predation. 3.1. No-choice tests

The four populations of A. largoensis consumed equivalent num- 2.5. Choice tests bers of R. indica eggs, with consumption ranging from 44 to 47 eggs per female/day regardless of their previous feeding experience, [H Prey preference of the four populations was addressed by (3,N = 40) = 3.90, P = 0.27] (Table 1). By contrast, the four popula- choice experiments offering 50 individuals of each prey item in tions consumed relatively fewer R. indica larvae (ranging from 9 the following combinations: R. indica eggs and T. gloveri eggs, to 23 larvae per female/day) compared with the other prey items R. indica eggs and T. gloveri larvae, R. indica larvae and T. gloveri offered and they differed in their predation rates (P < 0.001, Table eggs, and R. indica larvae and T. gloveri larvae. Prey type(s) were 1). The naïve field population, not previously exposed to R. indica, randomly assigned to either side of the arena to discard any effect consumed significantly fewer R. indica larvae than the other three of prey location on the choice by A. largoensis. Fifteen replicates per populations [H (3,N = 40) = 19.0, P < 0.0001]. With respect to utili- treatment (prey combination) were used, including the same zation of T. gloveri as prey, the four populations preyed on 39–44 number of absolute controls to ensure that prey mortality was T. gloveri eggs per female/day, showing no statistical differences caused by predation. among the predator populations [H (3,N = 40) = 2.96, P = 0.4]. Con- Predators used in all experiments were A. largoensis mated fe- sumption of T. gloveri larvae ranged from 36 to 46 larvae per fe- males in their oviposition peak (3–5 days after adult emergence). male/day. The R-colony, fed on R. indica for 2 years without To ensure females were mated and of the same age deutonymphs exposure to T. gloveri prey, consumed significantly fewer T. gloveri were isolated and males added to the rearing arenas. In addition, larvae than the other three populations [H (3,N = 40) = 7.5, P = 0.05]. only replicates in which the female remained within the test arena and produced at least one egg within 48 h were considered for 3.2. Choice tests analyses. Females were starved for 8 h before being transferred to the experimental arenas. The numbers of each R. indica or All four populations of A. largoensis consumed more R. indica T. gloveri stage consumed during a period of 24 h were recorded eggs than T. gloveri eggs or larvae (Fig. 1A and B). Consequently, by counting the number of shriveled corpses (larvae) and by preference indices (b) were significant (not overlapping with subtracting the number of eggs remaining from the number of eggs b = 0.5) and favoring R. indica eggs without significant differences provided. A period of 24 h was selected to ensure a behavioral basis among the four populations tested [H (3,N = 52) = 0.68, P = 0.871) in the response because longer term tests could be influenced by and H (3,N = 58) = 6.54 P = 0.08 for the R. indica eggs vs. T. gloveri post-ingestive processes that are not necessarily a reflection of eggs and R. indica eggs vs. T. gloveri larvae, respectively] (Fig. 2A the predator’s prey preference. and B). The likelihood that the four A. largoensis populations would con- 2.6. Data analysis sume R. indica larvae was lower and differed among them (Fig. 1C and D). Preference analysis showed that the R-colony, fed on R. Data were separately analyzed for each experiment using SAS indica for 2 years, was more likely to choose to prey on R. indica lar- 9.2 (SAS Institute Inc., 2010). Predation by the four populations vae than the other three populations tested, which showed signifi- of A. largoensis in the no-choice experiments was analyzed by cant preferences for T. gloveri eggs (F = 5.29; df = 3, 52; P < 0.003, Kruskal–Wallis tests due to variance heterogeneity and non- Fig. 2C). Finally, in the R. indica and T. gloveri larval-choice test, three 42 D. Carrillo et al. / Biological Control 60 (2012) 39–45

Table 1 Predation of R. indica and T. gloveri eggs and larvae by four local populations of A. largoensis with different feeding history (previous diet) under no-choice conditions. Mean number prey items consumed in 24 h Means ± S.D. Means within a column followed by the same letter are not significantly different (P < 0.05; Kruskal-Wallis test).

Amblyseius largoensis population Number of individuals consumed/day R. indica eggs R. indica larvae T. gloveri eggs T. gloveri larvae R-colony 47.2 ± 2.7 a 23.4 ± 6.7 a 39.4 ± 8.2 a 35.5 ± 11.1 b Experienced field 44.4 ± 4.2 a 24.3 ± 7.1 a 40.5 ± 3.9 a 41.7 ± 6.4 a T-colony 46.6 ± 3.5 a 21.7 ± 5.4 a 42.6 ± 5.8 a 46.3 ± 2.3 a Naïve field 45.5 ± 3.0 a 9.2 ± 4.8 b 43.7 ± 5.0 a 41.3 ± 9.6 a H (3,N = 40) 3.9 18.9 2.96 7.5 P value 0.3 <0.001 0.4 0.05

Fig. 1. Percentage of individuals of R. indica (black bars) and T. gloveri (grey bars) consumed by four populations of A. largoensis with different feeding history (previous diet) under choice conditions. (A) R. indica eggs vs. T. gloveri eggs, (B) R. indica eggs vs. T. gloveri larvae, (C) R. indica larvae vs. T. gloveri eggs, and (D) R. indica larvae vs. T. gloveri larvae. populations of A. largoensis showed no significant differences in posed to R. indica, showed a low consumption of R. indica larvae their consumption rates or preference among these prey items (Figs.1C and 2D) and a marked preference for T. gloveri larvae (Fig. 2D). However, the naïve field population, not previously ex- (F = 5.29; df = 3, 40; P = 0.004) (Fig. 2D). D. Carrillo et al. / Biological Control 60 (2012) 39–45 43

Fig. 2. Prey preference of four local populations of A. largoensis with different feeding history (previous diet) when preying on R. indica and T. gloveri eggs and larvae under choice conditions. (A) R. indica eggs vs. T. gloveri eggs, (B) R. indica eggs vs. T. gloveri larvae, (C) R. indica larvae vs. T. gloveri eggs, and (D) R. indica larvae vs. T. gloveri larvae. The preference index b assigns preference values from 0 to 1, where 0.5 represents no preference. Mean b-values we considered significant when 95% confidence intervals (error bars) based on the t-distribution did not overlap with b = 0.5. Differences in b-values among the four populations of A. largoensis are represented by letters were analyzed through ANOVAs or Kruskal–Wallis tests depending on normality of data.

4. Discussion T. gloveri over larvae of R. indica. Apart from the phytoseiidae, other predatory mites have shown preference for the egg stage of prey. Our experiments showed that populations of A. largoensis did For example, Poecilochirus carabi G. & R. Canestrini (: not differ in the extent to which they fed on R. indica eggs, but rather Parasitidae) females are oophagous on Nicrophorus vespilloides in the extent to which they fed on R. indica larvae. R. indica eggs Herbst (Coleoptera: Silphidae) (Beninger, 1993) and Macrocheles were consumed in high numbers under no-choice conditions, and peregrinus (Krantz) (Acari: Macrochelidae) showed a strong prefer- chosen over T. gloveri eggs and larvae by the four populations of ence for eggs of various dipteran species (Roth et al., 1988). In addi- A. largoensis in the choice tests, regardless of their previous feeding tion, the predatory insect Delphastus catalinae (Horn) (Coleoptera: experience. Naïve predators, not previously exposed to R. indica, Coccinellidae) showed a strong preference for Bemisia argentifolii responded to R. indica eggs similarly as the laboratory colony fed Bellows and Perring (Homoptera: Aleyrodidae) eggs (Legaspi exclusively on R. indica for 2 years, suggesting that the four popula- et al., 2006). tions of A. largoensis rapidly associated R. indica eggs with a reward A. largoensis displayed ability to rapidly recognize and prey on R. and started to consume and prefer this prey item. Thus, the cues indica eggs. By contrast, results of our study suggest that predators used by A. largoensis to recognize and associate R. indica eggs with need to habituate to R. indica before starting to utilize R. indica a reward must be well defined and easily assimilated by the pred- larvae as prey. The four A. largoensis populations differed in their ator. Previous studies showed that oviposition rates of A. largoensis likelihood of preying upon R. indica larvae. The laboratory R-colony females (i.e., the R-colony) fed on a diet of R. indica eggs showed the highest likelihood preying on R. indica larvae in the (2.36 ± 0.1153 eggs/day, Carrillo and Peña, in press) were higher choice experiments, which could have resulted from selection than oviposition rates when the predator was provided a diet of due to it having access only to R. indica for over 2 years (ca. 50 gen- mixed R. indica stages (1.63 ± 0.27 eggs/day, Carrillo et al., 2010), erations). Interestingly, this selection was not eliminated by suggesting that a diet of R. indica eggs is more rewarding in terms 2 months of rearing exclusively on T. gloveri in the T-colony, of the predator’s reproductive success than a mixed diet. A similar suggesting that the changes in feeding behavior of A. largoensis condition was observed with occidentalis (Nesbitt) could have a genetic basis. In general, the three populations that (Acari: Phytoseiidae), which showed better reproductive parame- had a ‘long term’ exposure to R. indica (i.e., R-colony, T-colony, ters when fed on Tetranychus pacificus McGregor (Acari: Tetranychi- and the experienced field population) had a higher likelihood of dae) eggs compared to a diet of mixed immature stages preying on R. indica larvae than the naïve field population with (Bruce-Oliver and Hoy, 1990). Blackwood et al. (2001) tested no previous exposure to R. indica, suggesting that its lack of several species of phytoseiid mites for preferences between eggs experience in preying on R. indica might have affected its ability and larvae of Koch (Acari: Tetranychidae) and to consume this prey. suggested that specialized predators had a preference Overall, results of our studies suggest that multiple mechanisms for eggs whereas generalist predators had no prey-stage preference. can be involved in the response of A. largoensis to R. indica. It is pos- Our results suggest that A. largoensis, despite being a generalist sible that these mechanisms do not act independently but are con- predator (McMurtry and Croft, 1997), showed a marked preference ditionally expressed depending on the conditions that the predator for eggs of R. indica over eggs and larvae of T. gloveri. In addition, faces (Sabelis and Lesna, 2010). For instance, it is likely that popu- three out of four populations of A. largoensis preferred eggs of lations of A. largoensis are subject to relatively long periods of expo- 44 D. Carrillo et al. / Biological Control 60 (2012) 39–45 sure to R. indica which has become by far the dominant should be explored. Moreover, research towards identifying chem- on in areas of recent invasion. These circumstances could ical control practices that can preserve these natural enemies for favor selection processes and the likelihood of A. largoensis preying their use in integrated management plans targeting R. indica on R. indica active stages may increase. Experienced predators could should be conducted. learn to optimize their foraging activities and also increase the like- lihood of preying on R. indica larvae. However, when food quality declines and predators are forced to disperse, dispersal might bring Acknowledgments A. largoensis to a location where another food type is dominant. Thus, predators must retain the ability to switch prey (Sabelis and We are thankful with Dr. Cal Welbourn (FSCA-DPI) for the iden- Lesna, 2010). Our results suggest that A. largoensis can switch to no- tification of mites, Dr. Na-Lampang Sikavas (UF-TREC) for help with vel prey after a period of starvation despite possible conditioning of the statistical analyses, and Dr. Josep Jacas (UJI Spain) for helpful prey preferences due to genetic selection or experience. In conclu- reviews of the original manuscript. We thank K. Santos, R. Duncan, sion, A. largoensis showed plasticity in its utilization of R. indica D. Long, A. Vargas, and J. Alegria, for their help. This research was larvae which could be related to selection, learning or a combina- partially funded by a TSTAR Grant to JEP. tion of both. Moreover, the environmental conditions that predators face can modulate the expression of these. Another factor that could affect the prey preference of References phytoseiid mites is the presence of feeding attractants and deter- rents (Hoy and Smilanick, 1981; Vet and Dicke, 1992). It has been Alberti, G., Crooker, A.R., 1985. Internal Anatomy. In: Helle, W., Sabelis, M.W. (Eds.), Spider Mites: Their Biology, Natural Enemies, and Control, vol. A. Elsevier, suggested that R. indica could produce repellent compounds be- Amsterdam, Netherlands, pp. 29–311. cause of the presence of droplets located at the tips of the dorsal Beninger, C.W., 1993. Egg predation by Poecilochirus carabi (Mesostigmata: body setae and at the tip of the egg’s pedicel (Zanotto and Parasitidae) and its effect on reproduction of Nicrophorus vespilloides (Coleoptera: Silphidae). Environmental Entomology 22 (4), 766–769. Rodrigues, 2010). The marked preference for R. indica eggs Blackwood, J.S., Schausberger, P., Croft, B.A., 2001. Prey-stage preference in observed in the present study and the high ‘profitability’ of this generalist and specialist phytoseiid mites (Acari: Phytoseiidae) when offered prey for A. largoensis (Carrillo et al., 2010) do not support the Tetranychus urticae (Acari: Tetranychidae) eggs and larvae. Environmental hypothesis of toxic or repellent compounds being present in the Entomology 30 (6), 1103–1111. Bowman, H.M., 2010. Molecular discrimination of phytoseiids associated with the pedicel droplets on R. indica eggs. However, it is possible that the red palm mite Raoiella indica (Acari: Tenuipalpidae) from Mauritius and South droplets found on other R. indica larvae (and other life stages) could Florida. MS Thesis, University of Florida, Gainesville. have a different composition and affect the ability of A. largoensis to Bruce-Oliver, S.J., Hoy, M.A., 1990. Effect of prey stage on life-table attributes of a genetically manipulated strain of Metaseiulus occidentalis (Acari: Phytoseiidae). feed on them. The possible existence of kairomones or allomones Experimental and Applied Acarology 9, 201–217. produced by R. indica should be investigated to better understand Carrillo, D., Peña, J.E., in press. Prey-stage preferences and functional numerical their role on the prey choice of this predator. In addition, mites can responses of Amblyseius largoensis (Acari: Phytoseiidae) to Raoiella indica (Acari: Tenuipalpidae). Experimental and Applied Acarology. doi:10.1007/s10493-011- have other defense mechanisms that could directly influence their 9488-7. attractiveness to predators. The hardness of the cuticle could serve Carrillo, D., Peña, J.E., Hoy, M.A., Frank, J.H., 2010. Development and reproduction of as a defense mechanism against predators (Alberti and Crooker, Amblyseius largoensis (Acari: Phytoseiidae) feeding on pollen, Raoiella indica (Acari: Tenuipalpidae), and other microarthropods inhabiting coconuts in 1985). Observations made during the experiments showed that Florida, USA. Experimental and Applied Acarology 52, 119–129. A. largoensis usually required a single attack to successfully pene- Carrillo, D., Amalin, D., Hosein, F., Roda, A., Duncan, R., Peña, J.E., in press. Host plant trate the chorion and imbibe all of the egg contents. In contrast, range of Raoiella indica Hirst (Acari: Tenuipalpidae) in areas of invasion of the new world. Experimental and Applied Acarology. doi:10.1007/s10493-011- A. largoensis females probed several times in order to penetrate 9487-8. the larval cuticle, had a longer handling time, and did not consume Carrillo, D., Navia, D., Ferragut, F., Peña, J.E., 2011. First report of Raoiella indica Hirst the larval prey entirely. Thus, preference of A. largoensis for (Acari: Tenuipalpidae) in Colombia. Florida Entomologist 94 (2), 370–371. R. indica eggs and the lack of preference for larvae could be related Etienne, J., Flechtmann, C.H.W., 2006. First record of Raoiella indica (Hirst, 1924) (Acari: Tenuipalpidae) in and , West Indies. to the energy spent and the nutritional reward obtained when International Journal of Acarology 32, 331–332. feeding on each of them. Gallego, C.E., Aterrado, E.D., Batomalaque, C.G., 2003. Biology of the false spider Findings of this study suggest that different populations of A. mite, Rarosiella cocosae Rimando, infesting coconut palms in Camiguin, northern Mindanao (Philippines). Philippines Entomology 17 (2), 187. largoensis may be responding to the invasion by R. indica either Hoy, M.A., Smilanick, J.M., 1981. Non-random prey location by the phytoseiid by learning or adapting to be better predators of this invasive pest. predator Metasieulus occidentalis: differential responses to several spidermite These findings may be important for future biological control pro- species. Entomologia Experimentalis et Applicata 29, 241–253. Jai, F., Margolies, D.C., Boyer, J.E., Charlton, R.E., 2002. Genetic variation in foraging grams targeting R. indica. Since R. indica gained importance as an traits among inbred lines of a predatory mite. Heredity 89, 371–379. invasive pest in the neotropics, surveys for natural enemies in sev- Legaspi, J.C., Simmons, A.M., Legaspi, B.C., 2006. 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