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1 Acarologia A quarterly journal of acarology, since 1959 Publishing on all aspects of the Acari All information: acarologia@supagro.inra.fr Acarologia is proudly non-profit, with no page charges and free open access Please help us maintain this system by encouraging your institutes to subscribe to the print version of the journal and by sending us your high quality research on the Acari. Subscriptions: Year 2018 (Volume 58): Previous volumes ( ): 250 / year (4 issues) Acarologia, CBGP, CS 30016, MONTFERRIER-sur-LEZ Cedex, France The digitalization of Acarologia papers prior to 2000 was supported by Agropolis Fondation under the reference ID through the «Investissements d avenir» programme (Labex Agro: ANR-10-LABX ) Acarologia is under free license and distributed under the terms of the Creative Commons-BY-NC-ND which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
2 EFFECT OF PREY DEPRIVATION ON SURVIVAL AND REPRODUCTION OF NEOSEIULUS CALIFORNICUS (ACARI: PHYTOSEIIDAE) FEMALES BY N. M. GRECO, G. G. LILJESTHRÖM, C. V. CÉDOLA & M. F. ROGGIERO* (Accepted November 2005) NEOSEIULUS CALIFORNICUS STARVATION STRAWBERRY FECUNDITY ADULT SURVIVAL PHYTOSEIIDAE SUMMARY: Neoseiulus californicus (MCGREGOR) is a phytoseiid that can provide biological control of Tetranychus urticae Koch. The effectiveness of phytoseiids for biological control depends on different attributes including their ability to survive conditions of food shortage. Newly N. californicus copulated females were singly introduced into an arena for 10 days and were either provided with or deprived of food (all stages of T. urticae) during the first 48 or 96h. Food deprivation reduced adult survival (control: 100%, 48h: 83% and 96h: 62.5%) and the proportion of reproducing females, while the pre-reproductive period increased with increasing starvation. The number of offspring produced by females of age x that effectively laid eggs after the periods of starvation was not significantly different from the control in all cases they levelled at approximately 2.9 eggs per reproducing female. Expressing the mean number of eggs laid per female in physiological age (days after starvation), differences were observed in the second and third days denoting the effect of starvation in the fecundity recovery period. The net reproduction rate during the first 10 days of adulthood was 18.22, 8.91 and 1.95 female eggs/female/10 days, for the control, the 48 and the 96h starvation treatments, respectively. The overall effect of food deprivation was mainly due to a reduction in adult survivorship and in the proportion of reproducing females. The negative effect on the net reproductive rate during the first 10 days of adulthood could reduce the capacity of N. californicus to prevent population increases of T. urticae in the short-term. Notwithstanding, this effect would be mitigated because this predator is capable of feeding on alternate food sources such as pollen, different mites and insect eggs. INTRODUCTION Phytoseiid mite species are predators commonly used for the biological control of the two-spotted spider mite, Tetranychus urticae Koch (HUSSEY & SCOPES, 1985; WAITE, 1988; RAWORTH, 1990; ZALOM et al., 1990; COOP et al., 1997; STEINBERG et al., 1999; ZALOM, 2002). The effectiveness of phytoseiids for biological control depends on different attributes including their ability to survive conditions of food shortage (DE COURCY WILLIAMS et al., 2004). Neoseiulus californicus (McGregor) life style has been rated between a type II and III (CROFT et al., 1998). It can provide biological control of T. urticae over a wide range of climatic and management conditions (MCMURTRY & CROFT, 1997). It was observed * Centro de Estudios Parasitológicos y de Vectores (UNLP-CONICET), 2 No 584 (1900), La Plata, Argentina Acarologia, 2005 [2006], XLVI, 1-2 :
3 14 exhibiting a high spatial coincidence with T. urticae and a high ability to detect leaflets with prey (GRECO et al., 1999). Moreover, N. californicus has a higher capacity to stay in patches with low pest density than other phytoseiids (MA & LAING, 1973; CROFT et al., 1998; PRATT et al., 1999). Field studies showed that T. urticae populations usually decline to very low levels due to the preypredator interaction (NACHMAN, 1991; GARCIA MARI et al., 1991; SIH &GLEESON, 1995; NYROP et al., 1998; GRECO at al., 1999) as well as to selective acaricide applications which allow the persistence of the predator (CROFT et al., 1998). In those situations predators may stay in the field with few preys (GRECO et al., 1999) and wait for the prey return or feed on other sources while minimizing starvation (CROFT et al., 1998). However, it must be evaluated the capacity of N. californicus and other phytoseiids to cope with subsequent population increase of T. urticae. It is known that adult phytoseiids allocate the most food to egg production and prey consumption affects reproduction which reaches its maximum early in the oviposition period (SABELIS 1985a; SABELIS & JANS- SEN 1993). Oviposition is not chronological agedependent but physiological age-dependent and during periods of food shortage resources are allocated primarily to maintenance at the expense of reproduction (SABELIS, 1985a; MÉGÉVAND & TANIGOSHI, 1994). Phytoseiid females surviving a period of food deprivation are capable of reproducing after they have been supplied with spider mites (HAMA- MURA et al., 1978) and in N. idaeus the female to male ratio of the offspring at the adult stage (secondary sex ratio) was unchanged (MÈGÉVAND & TANI- GOSHI, 1995). With respect to N. californicus, when adults were deprived of food but provided with water, stored energy was allocated for survivorship but not for reproduction (DE COURCY WILLIAMS et al., 2004). Information exists on N. californicus about the effect of food deprivation on adult longevity (DE COURCY WILLIAMS et al., 2004), the effect on other demographic parameters was only analyzed for Neoseiulus idaeus (MÉGÉVAND & TANIGOSHI, 1995). The aim of this work was to determine the effect of short periods of N. californicus female starvation on survival and reproduction. We hypothesize that N. californicus females surviving a short period of food deprivation are capable of reproducing after they have been supplied with spider mites, but adult survivorship and reproduction will be affected. We expect that when the starvation period increases adult survival and fecundity will decrease, the pre-oviposition period will increase, and the offspring sex ratio will remain unchanged. MATERIAL AND METHODS Mites (T. urticae and N. californicus) were collected in strawberry crops from La Plata, Argentina, and reared for more of 10 generations on strawberry leaves at CEPAVE, under controlled conditions. Reproductive females of the phytoseiid were placed with prey on strawberry leaflets, which were placed upside down on water-saturated foam in a Petri dish. After two days the females were removed and the eggs laid were reared up. On the fifth day the individuals were continuously observed to identify tending (adult males with palps touching the deutonymph or waiting close by) and mating (venter-toventer position) (SCHULTEN, 1985). Once mating ended, the recently copulated females (n = 45) were introduced singly into an arena and were either provided with or deprived of food (a mixture of all stages of T. urticae) during 48 or 96h as three separate experimental treatments. For each treatment 15 replicates were performed, and after starvation food was provided without limitation. Leaves and food were replaced when necessary. The experimental unit consisted in a plastic container of 3.5cm diameter, surrounded by a water groove, with a strawberry leaf disc arena (1.8cm diameter) placed over wet cotton. Each unit was placed in a Petri cage of 5cm diameter and covered with plastic film. Experiment was conducted at 25 fi 2 C, % RH and photoperiod of 14: 10 (L: D). During 10 days the number of surviving females of age x, and the number of eggs laid during the interval x, x + 1, were registered, from which the l(x) and m(x) distributions were calculated. To estimate the secondary sex ratio, the eggs were isolated and reared until the adult stage when the proportion of females (PF) was determined. Females that disappeared or drowned during the experiment were excluded from the analysis.
4 We estimated the pre-reproductive period in two ways: 1) the number of days before the onset of reproduction by an average female (PR), and 2) a subset of the former: the number of days before the onset of reproduction by an average female, after starvation (PRAS). We recorded the proportion of reproducing females in each treatment, a subset of surviving females, and the differences among each treatment and the control for each day by the normal deviate Z test (ZAR, 1996). The number of offspring produced by those females of age x during the period x, x + 1, RF (x), was also estimated. Complementary, the number of eggs laid per female in physiological age (after starvation) during six consecutive days was compared among treatments and the control by twoway ANOVA. Differences among treatments in the secondary sex ratio (PF) were tested by chi-square test. To estimate the overall effect of food deprivation, we calculated the net reproduction rate (NRR) during the first 10 days of adulthood: NRR= Σ l (x) (PF) m (x). Estimates of the means and standard errors of the NRR on each treatment were calculated with a Jacknife procedure (MEYER et al., 1986; CASWELL, 1989). NRR was compared among treatments by ANOVA. Following a significant ANOVA, means were separated using the Tuckey test. 15 RESULTS In the 48 and 96h starvation treatments the percentage of adult survival at the end of the experiment (10 days of adulthood) was 83% and 62.5%, respectively, and lower than the control that attained 100% survivorship (FIG. 1). The decline in survival after the prey re-introduction suggests that irreversible damage occurred to some females when starved for 48 and 96h. The age specific fecundity was highest in the control than in the treatments during the first days, but tended to level off at the end of the experiment (FIG. 2). The pre-reproductive period, PR, increased with increasing starvation and in both treatments they were higher than the control (F = 96.73; d.f. = 2, 26; P < 0.001) (FIG. 3). With respect to PRAS, values Fig. 1. Survivorship during 10 days of N. californicus newly mated adult females fed continuously on T. urticae (control=large line) and starved for 48h (line) and 96h. (dotted line) FIG. 2. Age specific fecundity during 10 days of N. californicus adult females fed continuously on T. urticae (control=large line) and starved for 48h (line) and 96h. (dotted line). FIG. 3. Pre-reproductive period of N. californicus adult females fed continuously on T. urticae (control) and starved for 48h and 96h.
5 16 (control: 0.47 fi 0.52 days, n =15; 48h of starvation: 0.90 fi 0.74 days, n = 10; and 96h of starvation: 1.75 fi 1.26 days,n=4)weredifferent (F = 5.22; d.f. = 2, 26; P = 0.012), but the 48h starvation treatment did not differ from control (P > 0.05). The proportion of reproducing females was significantly lower in the 96h than the 48h and the control during the first three days after starvation: Z (5 th day) = 3.48, Z (6 th day) = 3.48, Z (7 th day) = 2.26; P < 0.05, (FIG. 4). The number of eggs produced by females of age x that effectively laid eggs, RF (x), levelled up at approximately 2.9 eggs per reproducing female (FIG. 5). Expressing the mean number of eggs laid per female in physiological age, differences were observed in the second and third days (FIG. 6). These differences denote the effect of starvation in the fecundity recovery period. The hatching success of the progeny for all treatments ranged from 99.4 to 100 %. The secondary sex ratio (PF) did not differ among treatments (control = 0.71; 48h treatment = 0.60; and 96h treatment = 0.82) (X 2 = 4.42; d.f. = 2; P > 0.05). To estimate the overall effect of starvation on N. californicus, NRR, we used a common mean secondary sex ratio of 0.68 (overall mean). The NRR was (SE = 0.77; n = 15), 8.91 (SE = 1.99; n = 12) and 1.95 (SE = 1.38;n=8)female eggs/female/10 days, for the control, the 48 and the 96h starvation treatments, respectively. Differences between treatments were significant (F = 31.50; d.f. = 2, 32; P < 0.001). The higher the starvation period the lower the NRR: the 48h starvation represented 48.88% of the control, and the 96h of starvation represented only 10.73%. DISCUSSION FIG. 4. Proportion of reproducing N. californicus adult females fed continuously on T. urticae (control=large line) and starved for 48h (line) and 96h. (dotted line). FIG. 5. Number of eggs daily laid by N. californicus female fed continuously on T. urticae (control=large line) and starved for 48h (line) and 96h. (dotted line). FIG. 6. Number of eggs daily laid by N. californicus female fed continuously on T. urticae (control) and starved for 48h and 96h, in terms of physiological age after starvation. The capacities to recover from starvation and to reproduce again after finding a new prey patch are advantageous features and will have been favoured by natural selection (BLOMMERS & VAN ARENDONK, 1979). In our study we found that N. californicus females surviving a short period of food deprivation were capable of reproducing after they have been supplied with spider mites. Similar results were obtained by HAMAMURA et al. (1978), BLOMMERS & VAN AREN-
6 17 DONK (1979) and MÉGEVAND & TANIGOSHI (1995). Adult survivorship after 96h of food deprivation attained 62.5% and reproduction began once prey were reintroduced, which implies that stored energy would be allocated for survival but not for reproduction. In effect, DE COURCY WILLIAMS et al. (2004) found that mean longevity of adult females provided only with water was 17.9 days. On the other hand, starvation did not affect the number of offspring produced by reproducing females of N. californicus, RF (x). The number of eggs per female per day found in this study was similar to the values reported by MA & LAING (1973) and CASTA- GNOLI & SIMONI (1999). Similarly, MÉGEVAND & TANIGOSHI (1995) found that after periods of prey deprivation up to 72h N. idaeus recovered the oviposition rates to the same or higher level than those of the control. With respect to the secondary sex ratio of N. californicus, starvation periods of 84 and 96h did not affect the female to male ratio. Phytoseiid mites are capable of sex ratio control (VELTKAMP, 1968; FRIESE &GILSTRAP, 1982) notwithstanding, the sex determining mechanism is not known (SABELIS, 1985b). The sex ratio of progeny was not affected by prey deprivation episodes of the parental females of N. idaeus (MÉGEVAND & TANIGOSHI, 1995). CASTAGNOLI & SIMONI (1999) showed that in N. californicus the female to male ratio tended to increase with prey density. In our study, the secondary sex ratio of N. californicus was female biased, independently of the starvation period. In this case, once the period of food deprivations ceased, the phytoseiids were provided with a constant and abundant number of preys. The overall effect of starvation on N. californicus was mainly due to a reduction in adult survivorship and the proportion of reproducing females. The negative effect on the net reproductive rate during the first 10 days of adulthood could reduce the capacity of N. californicus to prevent population increase of T. urticae in the short-term. Notwithstanding, this effect would be mitigated because this predator is capable to feed on alternate food sources such as pollen, different mites and insect eggs (SWIRSKI et al., 1970; CASTAGNOLI et al., 2001). However, N. californicus could be able to persist within the agroecosystem even at rather unfavourable conditions and low prey densities because it may stay in a field with few prey (GRECO et al., 1999). Further, this predator has a higher capacity to stay in patches with low pest density than other phytoseiids (MA & LAING, 1973; PRATT et al., 1999). Phytoseiids that can survive on food sources other than T. urticae especially during periods of low prey density, have a better chance to establish and persist in the field. These are important traits in the frame of biological control by conservation of natural enemies. ACKNOWLEDGEMENTS We thank to Adrián MITIDIERI of INTA San Pedro for providing strawberry runner plants. REFERENCES BLOMMERS (L.) & VAN ARENDONK (R.C.M.), The profit of senescence in phytoseiid mites. Oecologia, 44: CASTAGNOLI (M.) & SIMONI (S.), Effect of longterm feeding history on functional and numerical response of Neoseiulus californicus (Acari: Phytoseiidae). Exp. Appl. Acarol., 23: CASTAGNOLI (M.), SIMONI (S.) & NACHMAN (G.), Short-term changes in consumption and oviposition rates of Neoseiulus californicus strains (Acari: Phytoseiidae) after a diet shift. Exp. Appl. Acarol., 25: CASWELL (H.), Statistical Inference. Pp , In H. Caswell, (ed), Matrix population models. 328 pp. Sinauer Associates, Inc. Publishers. Sunderland, Massachusetts COOP (L.), ROSETTA (R.) & CROFT (B.), Release calculator and guidelines for using Neoseiulus fallacis to control two-spotted spider mites in strawberry. Version 1.1. Designed for use at the Web site: CROFT (B. A.), MONETTI (L. N.) & PRATT (P. D.), Comparative life histories and predation types: Are Neoseiulus californicus and Neoseiulus fallacis (Acari: Phytoseiidae) similar Type II selective predators of spider mites? Environ. Entomol., 27: DE COURCY WILLIAMS (M. E.), KRAVA-GARDE (L.), FENLON (J.S.) & SUNDERLAND (K.D.), Phytoseiid mites in protected crops: the effect of humidity and food availability on egg hatch and adult life span of Iphiseius degenerans, Neoseiulus cucumeris, N. californicus and Phytoseiulus persimilis (Acarai: Phytoseiidae). Exp. Appl. Acarol., 32: 1-13.
7 FRIESE, (D.D.)& GILSTRAP (F.E.), Influence of prey availability on reproduction and prey consumption of Phytoseiulus persimilis, Amblyseius californicus and Metaseiulus occidentalis (Acarina: Phytoseiidae). Int. J. Acarol., 8: GARCIA MARI, (F.), MASIELLO, (L.), SAQUES (J.), RIBES (A.), SORO (T.)&LABORDA (R.), Control biológico de araña roja en cultivos valencianos de fresón. Agrícola Vergel. Marzo: GRECO (N.), SÁNCHEZ (N.) & LILJESTHÖM (G.), Spatial distribution and coincidence of Tetranychus urticae (Acari: Tetranychidae) and the predator Neoseiulus californicus (Acari: Phytoseiidae) on strawberry. Exp. Appl. Acarol., 23 (7), HAMAMURA (T.), SHINKAJI (N.)&ASHIHARA (W.), Studies on the low temperature storages of Phytoseiulus persimilis Athias-Henriot (Acarina: Phytoseiidae). Bull. Fruit-Tree Res. Stn., Ser. E (Akitsu), 2: HUSSEY (N. W.)& SCOPES (N), Greenhouse Vegetables (Britain). Pp , In W. Helle, & M. W. Sabelis(eds), Spider Mites Their Biology, Natural Enemies and Control, Vol. 1B: Elsevier, Amsterdam. MA (W.-L.)&LAING (J. E.), Biology, potential for increase and prey consumption of Amblyseius chilenensis (Dosse) (Acarina: Phytoseiidae). Entomophaga, 18: MCMURTRY (J. A.) & CROFT (B. A.), Life-styles of phytoseiid mites and their roles in biological control. Annu. Rev. Entomol., 42: MÉGEVAND & TANIGOSHI (L. K.), Effects of prey deprivation on life table attributes of Neoseiulus idaeus Denmark and Muma (Acari: Phytoseiidae). Biological Control, 5: MEYER (J. S.), INGERSOLL (C. G.), MCDONALD (L. L.) & BOYCE (M. S.), Estimating uncertainty in population growth rates, jacknife vs. bootstrap techniques. Ecology, 67: NACHMAN (G.), An acarine predator-prey metapopulation system inhabiting greenhouse cucumbers. Biol. J. Linn. Soc., 42: NYROP (J.), ENGLISH-LOEB (G.) & RODA (A), Conservation biological control of spider mites in perennial cropping systems. Pp , In: P. BARBOSA, (ed), Conservation biological control. Academic Press, San Diego. PRATT (P. D.), SCHAUSBERGER (P.) & CROFT (B. A.), Prey-food types of Neoseiulus fallacis (Acari: Phytoseiidae) and literature versus experimentally derived preyfood estimates for five phytoseiid species. Exp. Appl. Acarol., 23: RAWORTH (D. A.), Predators associated with the twospotted spider mite, Tetranychus urticae, on strawberry at Abbottsford, BC, and development of nonchemical mite control. J. Ent. Soc. Brit. Columbia, 87: SABELIS (M. W.), 1985 a. Reproduction. Pp , In W. HELLE, & M. W. SABELIS (eds), Spider Mites Their Biology, Natural Enemies and Control, Vol. 1B: Elsevier, Amsterdam. SABELIS (M. W.), 1985 b. Sex allocation. Pp , In W. HELLE, & M. W. SABELIS (eds), Spider Mites Their Biology, Natural Enemies and Control, Vol. 1B: Elsevier, Amsterdam. SABELIS (M. W.) & JANSSEN (A.), Evolution of life-history patterns in the Phytoseiidae. Pp In M. A. HOUCK (ed), Mites: ecological and evolutionary analyses of life-history patterns. Chapman & Hall, New York, pp SCHULTEN (G. G. M.), Mating - Pp , In W. HELLE, & M. W. SABELIS (eds), Spider Mites Their Biology, Natural Enemies and Control, Vol. 1B: Elsevier, Amsterdam. SIH (A.) & GLEESON (S. K.), A limits-oriented approach to evolutionary ecology. Trends Ecol. Evol., 10 (9): STEINBERG (S.), HADASSA (C.) & KAMINSKI (J.), Product control of Phytoseiulus persimilis (Athias- Henriot): current practice of a commercial producer. Pp , In VAN LENTEREN J. C. (ed) Integrated Control in Glasshouses, IOBC/WPRS Bulletin 22 (1): SWIRSKI (E.), AMITAI (S.)& DORZIA (N.), Laboratory studies on the feeding habits, post-embryonic survival and oviposition of the predaceous mites Amblyseius chilenensis Dosse and A. hibisci Chant (Acarina: Phytoseiidae) on various kinds of food substances. Entomophaga, 15: VELTKAMP (J. V.), Effect oif prey density on the sex ratio in the progeny of Typhlodromus longipilus Nesbitt (Phytoseiidae). Neth. J. Zool., 19: WAITE (G. K.), Integrated control of Tetranychus urticae in strawberries in southeast Queens-land. Exp. Appl. Acarol., 5: ZALOM (F. G.), PICKEL (C.) & WELCH (N. C.), Recent trends in strawberry arthropod management for coastal areas of the western United States. In BOSTA- NIAN, N. J., WILSON, L. T. anddennehy, T. J. (eds.) Monitoring and integrated management of arthropod pests of small fruit crops. Hampshire, England: Intercept, pp ZALOM (F. G.), UC IPM Pest Management guidelines: strawberry. Insects and mites. En: P.A. PHILIPS, UC IPM Program, UC Cooperative Extension Ventura Co. N.C. Toscano, Entomology, UC Riverside UC ANR, Publication PMG/selectnewpest.strawberry.html ZAR (J. H.), Biostatistical analysis. Prentice Hall, New Jersey.
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