Exp Appl Acarol (2009) 47:235247 DOI 10.

1007/s10493-008-9211-5

Effects of starvation on reproduction of the predacious mite Neoseiulus californicus (Acari: Phytoseiidae)
Shingo Toyoshima Peter Michalik Giovanni Talarico Anja E. Klann Gerd Alberti

Received: 28 April 2008 / Accepted: 20 October 2008 / Published online: 6 November 2008 Springer Science+Business Media B.V. 2008

Abstract Effects of starvation on gravid females of Neoseiulus californicus were investigated at 20C and 85% RH. When females that had been reared with abundant prey were swapped, just after laying their rst egg, to conditions without any prey and water, they laid 1.8 eggs and survived for 4.3 days. In the body of well-fed females, an egg with eggshell and/or two oocytes were observed in the ventral and dorsal regions, respectively. The larger oocyte had two roundish nuclei and abundant yolk granules, and was enveloped with a vitelline membrane. These two nuclei were not fused but were just close to each other. The smaller oocyte had a nucleus, but had not yet formed yolk granules and vitelline membrane. Females after 12 h starvation had an egg in the ventral region and an oocyte in the dorsal region of the body. After more than 24 h starvation females maintained an oocyte in the dorsal region of the body, but had no egg in the ventral region. The oocyte was lled with abundant yolk granules and contained two irregular nuclei when females were starved for 24 h, but when starved for more than 36 h it contained one irregular nucleus. These ndings suggest that (1) gravid females maintained an oocyte in the dorsal region after laying two eggs during starvation, (2) the oocyte was not absorbed during starvation, (3) the oocyte advanced vitellogenesis and the fusion of two nuclei, and (4) the vitellogenic oocyte was not enveloped with an eggshell and had not started embryogenesis. Keywords Sex ratio Neoseiulus californicus Starvation Survival Oogenesis

S. Toyoshima (&) National Institute of Fruit Tree Science, Morioka 020-0123, Japan e-mail: toyosin@affrc.go.jp P. Michalik G. Talarico A. E. Klann G. Alberti Zoological Institute and Museum, Ernst-Moritz-Arndt-University Greifswald, Johann-Sebastian-Bach-Strasse 12/12, 17489 Greifswald, Germany

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Introduction Neoseiulus californicus (McGregor) is an important natural enemy to control spider mites on various crops in the world (e.g., Hoddle et al. 1999; Greco et al. 2005; Gerson and Weintraub, 2007). In Japan, indigenous populations of N. californicus control spider mites on pear and citrus trees (Katayama et al. 2006; Kawashima et al. 2006), and a commercially available strain of N. californicus is used for the control of spider mites on strawberry in the greenhouses (Miyata and Masuda 2006). Since the species does not occur indigenously in apple orchards (Toyoshima 2003), attempts to control two-spotted spider mites on apple trees with the commercial N. californicus have been conducted. In the attempts, continuous and abundant release of the commercial agent was successful in controlling the mites (S. Toyoshima, unpublished), but control failed when the predators were released at an economically acceptable rate (Toyoshima and Osakabe 2005). The present study was performed to explore possible reasons for the failure to establish effective populations. Perhaps the condition of the mites prior to their release in the orchards plays a key role. In particular, the nutritional state of the mites may be of importance. Thus, in this study, the effect of starvation on oogenesis, survival and oviposition of N. californicus was investigated, to estimate the survival strategy of N. californicus under no- or low-prey conditions. The commercial N. californicus undergoes an extensive journey without prey from the provider in Europe to Japan. Strong starvation may affect foraging behavior of phytoseiid mites although the food deprivation elicits ambulatory dispersal of N. californicus (Auger et al. 1999; Palevsky et al. 1999). The prey source during the journey is only own eggs and immature stages in the delivery bottle. Some phytoseiid species consume phytoseiid eggs and immatures to prolong their life span and to sustain egg production (Schausberger 2003). N. californicus also consumed own eggs and immatures, but preferred heterospecic to conspecic predation (Palevsky et al. 1999; Schausberger and Croft 1999). Since N. californicus females survived signicantly longer (22.4 day, after the rst egg was laid) than the other species when food was short (Williams et al. 2004), females may resorb eggs in their body to survive prey scarcity. In various insect species, oosorption (resorption of oocytes) is known as an effective mechanism to save and use resources in the eggs (Bell and Bohm 1975). Evidence for oosorption has not been found in other phytoseiid species (Croft et al. 1995), but oosorption in N. californicus was not investigated. If N. californicus females would resorb eggs in their body when prey is scarce or absent, they likely would survive longer without food than unable phytoseiid species. Thus, we investigated whether oosorption occurs under scarce-food conditions in N. californicus. Di Palma and Alberti (2001) have explored the detailed structure of the female genital system in phytoseiid mites. They distinguished four stages of oocyte development in relation to cell growth and yolk deposition (vitellogenesis) in mated females. Several oocytes belonging to stages 1 and 2 were located within the ovary. A large stage-3 oocyte that had just started vitellogenesis was located dorsally in the ovary. A stage-4 oocyte had a good amount of yolk deposition and was located dorsally and posteriorly in the ovary, lateral to the stage-3 oocyte. We identied the stages of oocytes in starved females and compared them with those in the body of well-fed females. It is also possible that the commercial N. californicus does not establish a population on apple trees as a result of the low rate of increase just after severe food deprivation. After deprivation, fecundity and progeny survival of N. californicus were low, and progeny sex ratio was more male biased (Palevsky et al. 1999). Phytoseiid females conditionally adjust offspring sex ratio in response to the presence of conspecics or their cues (Nagelkerke and

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Sabelis 1998) and to the prey consumption rate (Toyoshima and Amano 1998). Several species of phytoseiid mites usually produce offspring with female-biased sex ratio when prey is abundant (Sabelis 1985), and decrease the bias of sex ratio gradually into even another extreme under certain conditions (Friese and Gilstrap 1982; Dinh et al. 1988; Nagelkerke and Sabelis 1998; Momen 1996). Such sex allocation may be more economical due to a more efcient use of nutrition. Since the eggs that develop into males (male eggs) are smaller than eggs that develop into females (female eggs) in Phytoseiulus persimilis and Amblyseius womersleyi (Toyoshima and Amano 1998), N. californicus females thus may also conserve nutrition by laying more male eggs than female eggs. If N. californicus females would resorb eggs and manipulate the sex of subsequent eggs during starvation, they would survive well even when prey is scarce or absent but the establishment of a population would be delayed. Thus, sex ratios of eggs laid by starved females were also compared with those laid by well-fed females.

Materials and methods Phytoseiid mites for experiment We obtained the commercial product of N. californicus (Spical: Koppert Biological Systems, Berkel en Rodenrijs, The Netherlands) and transferred the adult females onto kidney bean leaets infested with the two-spotted spider mite Tetranychus urticae Koch. Neoseiulus californicus were reared in a room with a constant temperature of 22 1C. Photoperiod in the room was not controlled but around L15:D9 h during experiments. Temperature and photoperiod conditions were the same in rearing and experiments. Survival under no-prey condition Newly developed adult females were coupled individually with males, and reared on a leaet (3 9 3 cm) with an abundance of prey eggs. Under these conditions, the mated females laid the rst egg ca. 24 h after mating and thereafter eggs were laid one by one at a rate of ca. two eggs per day. Then, females were observed at 3-h intervals during daytime (6:0018:00), and females that had already laid an egg at 6:00 h were removed from the experiment. Within 3 h after laying the rst egg, the females were transferred individually into rearing cases, each consisting of two yellow micropipette tips, one pressed in the other, both plugged with a piece of wooden toothpickthe mite was then captured in the ca. 15 mm long space between the two tips. The rearing cases were placed in a plastic container (3 cm in diameter, 1.5 cm high) along with a wet sponge in order to maintain the relative humidity inside the container at 85 2%. The females were kept in the case without prey and water until they died; survival and oviposition were monitored twice a day. Any eggs in the case were removed when observed, and dead females were embedded in Hoyers medium (Krantz 1978) in order to conrm whether they held eggs in their bodies. The females were observed under a phasecontrast microscope (Olympus BX60). Regarding intraspecic consumption (cannibalism) by adult females, it had been conrmed beforehand that N. californicus females in this study did not consume own eggs within 24 h, even without prey.

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Eggs in the females during starvation Females were transferred into the rearing case within 3 h after laying the rst egg and were reared for 12, 24, 36, or 48 h without prey and water. They were observed twice a day to check their oviposition. Ten females with different oviposition history (0, 1 or 2 eggs laid) were collected in each starvation period and embedded separately into Hoyers medium. Sex ratios of eggs laid by females after starvation treatment Females were transferred into the rearing case within 3 h after laying the rst egg and were reared for 48 h without prey and water. Females that had laid two eggs in the case were transferred onto a bean leaet with abundant prey and reared until they had laid three eggs on the leaet. The six eggs laid by each female (one egg before starvation, two in the rearing case, three after starvation) were reared separately to check their sex. Since the reproductive activity of starved females was fully recovered only after laying the three eggs, the sequence of eggs laid could not be distinguished by the observation twice a day. To compare the sex ratios of eggs produced by starved females with those produced by well-fed females, eggs were also obtained from the latter females. These females were reared on the bean leaet with abundant prey until they had laid more than six eggs. To obtain the eggs in sequence, oviposition was checked four times a day. The effect of starvation on the sex ratios was analyzed in eggs in sequence with the nonparametric Fishers exact test (using JMP software, version 6.0.2, from SAS, Cary, NC, USA). Internal observation of females Females that had laid their rst egg were kept separately for 12, 24, 36, 48, 72, or 96 h in rearing cases without prey and water. Then females were dissected and prexed overnight in ice-cold glutaraldehyde (3.5% glutaraldehyde in 0.1 M phosphate buffer; pH 7.4). Further processes included postxation with 2% OsO4 for 2 h, rinsing in buffer, dehydration in graded ethanol, and embedding in Spurrs medium. Semi- and ultrathin sections were cut using a microtome (Ultracut UCT; Leica Microsystems) with glass knives and a diamond knife (Diatome), respectively. The semithin sections were stained with Richardsons stain and oocytes were observed under a light microscope (Olympus BX60). The ultrathin sections were stained with saturated uranylacetate (in 70% methanol) and lead citrate for 10 min each and were examined under a transmission electron microscope (JEM-1011; JEOL Ltd).

Results Survival under no-prey condition Just after laying the rst egg, females laid 1.8 0.1 eggs and survived for 4.3 0.7 days (mean SE; n = 30) in the rearing case without prey and water (Fig. 1). Females laid eggs within 24 h after the beginning of the starvation period, and no female laid more than three eggs. Starved females held no egg in their body when dead. Maximum period of survival was 16 days.

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Exp Appl Acarol (2009) 47:235247 Fig. 1 The survival curve of adult females of Neoseiulus californicus under no-prey condition

239

100 80

Survival rate (%)

60 40 20 0

10

12

14

16

18

days

Eggs in the females during starvation When females were mounted after 12 h starvation, 10 females that had not yet laid an egg did contain an egg in their body, seven females held an egg even if they had already laid an egg, and three females that had not yet laid an egg contained no egg in their body. When females were mounted after 24 h starvation or longer, no females contained an egg in their body, regardless of the number of eggs laid during starvation. Sex ratios of eggs laid by females after starvation treatment Females that had starved for 48 h (n = 38) laid an egg within 24 h, but not within 12 h, after transfer onto the bean leaet with abundant prey. All eggs that had been laid before, during and after starvation, were collected in sequence. Sex ratios (number of adult daughters/number of adult daughters plus sons) are shown in Fig. 2. Sex ratio of the rst eggs laid by the starving females was 11% (strong male-bias). Sex ratio of the second and third eggs, which were laid in the rearing cases, was 84 and 53%, respectively. Sex ratios of the fourth, fth, and sixth eggs, laid on the leaet after starvation, were 79, 55 and 58%, respectively. On the other hand, sex ratio of eggs laid by well-fed females (n = 40) was 8% (1st), 88% (2nd), 60% (3rd), 80% (4th), 73% (5th) and 83% (6th). Sex ratio of the 1st5th eggs laid by starvation-treatment females was not signicantly different from that of well-fed females (Fishers exact test, n = 1, P = 0.71, 0.75, 0.71, 1.0 and 0.16, respectively). Only the difference in sex ratio between the sixth eggs was signicant (P = 0.03). Internal observation of females just before the starvation treatment Females just before the starvation treatment held an egg and well-developed oocytes in their body (0 h of starvation in Table 1). Among the nine females, ve had a mature egg in the ventral region and a large vitellogenic oocyte (oocyte at the stage 4) in the dorsal region of the body. The egg in the ventral region was located in the uterus, and was usually surrounded by an eggshell (four of the ve females). The remaining four females held two oocytes (stages 3 and 4), both located in the dorsal region of the body (Fig. 3).

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Starved females

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Well-fed females

100

(A)

(B)

80

Female ratio (%)

60

40

20

1st

2nd

3rd

4th

5th

6th

The sequence of eggs

Fig. 2 The sex ratios of the rst six eggs produced by females reared for 48 h under no-prey condition (starved females; black bar) or by females reared permanently under abundant prey condition (well-fed females; white bar). Sex was determined when the eggs had grown into adults. Arrow A indicates when the starved females were transferred into rearing cases. Arrow B indicates when the starved females were transferred onto leaets with abundant prey. The period between A and B was 48 h, and the second and third eggs of starved females were laid during this period. The female ratios of the offspring of the sixth eggs laid by the well-fed females were signicantly different from those laid by the starved females (Fishers exact test, n = 1, P = 0.03)

Table 1 The number of females with eggs and/or oocytes in their body when starved Period of starvation (h) No. of eggsa Combination of egg and oocytesb E ? O4 0 12 24 36 48 72 96
a b

O4 ? O3 4 1 0 0 0 0 0 0 0 0 0 0

O4 0 1 3 6 8 2 6 3 7 4 5 5

O3 0 0 0 0 0 0 0 0 0 0 0 1

0 1 1 2 1 2 1 2 1 2 1 2

5 5 3 0 0 0 0 0 0 0 0 0

The number of eggs laid during starving treatment Developmental stages of oocytes

E, a matured egg in the uterus at the ventral region of the body; O4, oocyte at stage 4 in the dorsal region; O3, oocyte at stage 3 in the dorsal region. These oocytes were distinguished with a light microscope. Referred to the Fig. 3

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O3 O4

Fig. 3 Schematic illustration of the sagittal section of an adult female of Neoseiulus californicus xed within 3 h after laying of the rst egg. The females had one oocyte in the uterus located in the ventral region and one in the dorsal region, or two oocytes in the dorsal region. The detailed structure of the egg in the uterus could not be observed because it was enveloped by the eggshell that prevented the penetration of the xative. An oocyte developed up to stage 4 having two nuclei and abundant yolk granules. Another oocyte developed up to stage 3 with one nucleus but no yolk granules. Abbreviations: E, mature egg in the uterus; O3, stage-3 oocyte; O4, stage-4 oocyte

It was difcult to observe the detailed structure and embryogenesis in the egg if surrounded with eggshell, because the shell prevented penetration of the xative into the egg. Without shell, however, a single nucleus was seen in the center of the egg (Fig. 4a). There was no evidence for the start of embryogenesis within eggs that lacked the shell. A single nucleus was detected in the oocyte at stage 3 (not shown in Fig. 4a). Two roundish nuclei were observed in the large vitellogenic oocyte (stage 4) (Fig. 4b). These two nuclei were close to each other but not fused (Fig. 4c). The vitellogenic oocyte was forming a vitelline membrane (Fig. 4d). Also stages 1 and 2 oocytes were detected in the ovary (Fig. 4e). Internal observation of females with starvation treatment Females were collected separately based on duration of starvation and number of eggs laid during starvation (Table 1). When females laid no egg during 12 h starvation, they held an oocyte (stage 4) in the dorsal region (n = 1), 2 oocytes (stages 3 and 4) in the dorsal region (n = 1), or 1 oocyte (stage 4) in the dorsal region along with a mature egg in the ventral region (n = 5). When females laid an egg during 12 h starvation, they held an oocyte (stage 4) in the dorsal region (n = 3) or an oocyte (stage 4) in the dorsal region along with a mature egg in the ventral region (n = 3). Regardless of the duration of starvation and the number of eggs laid during the starvation period, the females with more than 24 h starvation held a large vitellogenic oocyte (stage 4) in the dorsal region, but no mature egg in the uterus (Table 1; Figs. 5a, 6a). Two nuclei were observed in the oocyte at stage 4 in the female with 24 h starvation (Fig. 5b, c). On the other hand, a single nucleus was observed in the stage-4 oocyte in almost all females with more than 24 h starvation (Fig. 6b, c). In any case, the shape of the nucleus was not round but irregular, as compared to the nucleus in the oocytes of well-fed females. Stage-2 oocytes in the ovary had an irregular shaped nucleus (Figs. 5e, 6e) as that in the lyrate organ (Fig. 5d). The vitelline membrane of the oocyte was formed even in females with 96 h starvation (Fig. 6d), just as in well-fed females (Fig. 4d).

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Fig. 4 Internal structures of an adult female that had not been starved. The females were xed within 3 h after laying the rst egg. a Sagittal section of an adult female with a mature egg in the uterus. Arrow head shows a nucleus of the egg. Light microscopy. Scale bar = 50 lm. b Stage-4 oocyte with two nuclei. Transmission electron microscopy (TEM). Scale bar = 10 lm. c Detailed structure of the adjacent two nuclei shown in (b). The two nuclei have not yet fused. TEM. Scale bar = 1 lm. d The boundary between the stage-4 oocyte and the adjacent tissues. The vitelline membrane is being formed (arrowheads). TEM. Scale bar = 2 lm. e The center of the ovary adjacent to the lyrate organ. Arrowheads show nuclei in the oocytes at stage 2. TEM. Scale bar = 10 lm. Abbreviations: E, mature egg; G, genital opening; L, lyrate organ; N1, N2, nuclei; No, nucleolus; O2, stage-2 oocyte; O4, stage-4 oocyte; Yl, lipid-yolk granule; Yp, protein-yolk granule

Discussion In this study, N. californicus females did not stock nutrients in their body, but invested them in egg production, even under no-prey condition. They laid 1.8 eggs without food in

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Fig. 5 Internal structures of an adult female reared for 24 h under no-prey condition. a Sagittal section of the adult female with an oocyte in the dorsal region. Light microscopy. Scale bar = 50 lm. b Stage-4 oocyte showing two nuclei. Transmission electron microscopy (TEM). Scale bar = 5 lm. c The detailed structure of the adjacent two nuclei in (b). The two nuclei are very close to each other but remain separate. TEM. Scale bar = 1 lm. d A part of the lyrate organ. TEM. Scale bar = 2 lm. e The center of the ovary. TEM. Scale bar = 5 lm. Abbreviations: G, genital opening; L, lyrate organ; M, mitochondria; N, N1, N2 nuclei; No, nucleolus; NLS, nucleus-like-structure; O2, stage-2 oocyte; O4, stage-4 oocyte; U, uterus; Yl, lipid-yolk granule; Yp, protein-yolk granule

the rearing cases. Egg production without food is common in phytoseiid mites (Croft and Croft 1996), and eggs were sometimes consumed by ovipositing females when food was absent (Schausberger 2003). In the case of N. californicus, females can prolong their life

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Fig. 6 Internal structures of an adult female reared for 96 h under no-prey condition. a Sagittal section of the adult female with an oocyte in the dorsal region. Light microscopy. Scale bar = 50 lm. b Stage-4 oocyte with a nucleus. TEM. Scale bar = 10 lm. c The detailed structure of the nucleus in (b). TEM. Scale bar = 2 lm. d The boundary between the stage-4 oocyte and the lyrate organ. Formation of the vitelline membrane was maintained (arrowheads). TEM. Scale bar = 2 lm. e Stage-2 oocyte in the ovary. TEM. Scale bar = 5 lm. Abbreviation: G, genital opening; L, lyrate organ; N, nucleus; No, nucleolus; O2, stage-2 oocyte; O4, stage-4 oocyte; Yl, lipid-yolk granule; Yp, protein-yolk granule

span when feeding on conspecic eggs and larvae (Walzer and Schausberger 1999a), but normally avoid cannibalism (Walzer and Schausberger 1999b). In our study, females did not consume eggs laid in a rearing case, because the eggs were removed within 3 h after oviposition. As a result, they did not encounter any food and survived only 4.3 days. In

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previous studies, N. californicus females (after laying the rst egg) survived only 1.8 days when deprived of food and water (Williams et al. 2004), although they survived longer when deprived of food but supplied with water (Palevsky et al. 1999; Williams et al. 2004). The females in our study probably would have survived longer if water had been supplied in the rearing cases. In the body of 12-h starved females, an egg with eggshell was observed. This egg was laid during the following starvation period, and no egg with eggshell was observed in females with more than 24 h starvation. The stage-4 oocyte appeared from 24 h after the starvation treatment and was maintained for at least 96 h in the dorsal region of the body (Figs. 5, 6). It seems evident that females do not absorb the egg with shell and stage-4 oocyte to obtain nutrition for further survival. Neoseiulus californicus females may not need the oosorption because they can prolong their life span when water is supplied (Palevsky et al. 1999; Williams et al. 2004). They seem to prefer reproduction over survival even under scarce prey condition. Eggs can hatch if ovipositing females avoid cannibalism, and then larvae would survive and develop to adulthood if they encounter prey later on. Stage-2 oocytes with a single nucleus were observed in females with more than 24 h starvation, but no stage-3 oocyte was observed (Figs. 5e, 6e). In insects, oosorption includes cessation of oocyte production in the ovary and formation of a plug at the entrance of the oviduct (Bell and Bohm 1975). Neoseiulus californicus females may stop producing vitellogenic oocytes or may absorb oocytes at stage 3 that have just started to grow between 12 and 24 h of starvation. However, there is no evidence whether stage-3 oocytes were absorbed or stopped growing in the starved females. The effect of starvation on gravid females was limited to the oocyte in the ovary. Starvation treatment did not affect the sex of stage-4 oocytes in the starved females, that laid these oocytes as the 4th egg when females resumed feeding (Fig. 2). The vitellin membrane around the stage-4 oocyte (Figs. 4d, 6d) may protect the oocyte against stress caused by the starvation of the mothers. On the other hand, the sex of oocytes in the ovary was inuenced by the starvation treatment: some of the 6th eggs apparently changed their sex from female to male (Fig. 2). Since the offspring sex ratio of starved females of N. californicus recovered within 9 days after resuming prey consumption (Palevsky et al. 1999), the sex ratio of later eggs is expected to gradually get back to the female-biased sex ratio also under the experimental conditions in this study. The mode of reproduction in phytoseiid mites is known as pseudoarrhenotoky, where males arise from fertilized eggs that become haploid after inactivation or elimination of the paternal chromosomes (Nelson-Rees et al. 1980). It is difcult to imagine the sex-determining mechanism in this mode of reproduction as compared to that in an arrhenotokous mode (Bull 1983), despite the maintenance of the precise control of the sex ratio in phytoseiid mites in relation to prey density (Sabelis and Nagelkerke 1993). In the present study, we found that N. californicus females did not resorb developed oocytes in order to control the sex ratio of their brood when food is scarce. The oocyte was lled with abundant yolk granules, and held two irregular-shaped nuclei when females had been starved for 24 h. The oocyte advanced the fusion of the two nuclei but did not start embryogenesis. For further discussion, however, a comprehensive study of the oocytes in the ovary and in the dorsal region of the body is necessary in order to conrm whether the oocytes are inseminated in the ovary or at another position in the body.
Acknowledgments We thank Mrs. C. Putzar for her skilful technical assistance and Mr. Ard van der Maarel (Koppert Biological Systems) for his kindness to provide N. californicus. We also thank anonymous

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reviewers for their advisory comments to this manuscript. This study was nancially supported by a grantin-aid from the National Agriculture and Food Organization of Japan.

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