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The influence of humidity and water availability on the survival of Amblyseius idaeus andAmblyseius anonymus

Van Dinh, N.; Janssen, A.; Sabelis, M.W.

Published in:Experimental and Applied Acarology

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Citation for published version (APA):Van Dinh, N., Janssen, A., & Sabelis, M. W. (1988). The influence of humidity and water availability on thesurvival of Amblyseius idaeus and Amblyseius anonymus. Experimental and Applied Acarology, 4, 27-40.

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Experimental & Applied Acarology, 4 (1988) 27-40 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

27

Inf luence of Humidi ty and Water Avai labi l i ty on the Surv iva l of A m b l y s e i u s idaeus and A. a n o n y m u s ( Acar ina: Phytose i idae )

NGUYEN VAN DINH 1, M~W. SABELIS 2'~ and ARNE JANSSEN 2

1Department of Entomology, Agricultural University of Hanoi (Vietnam) 2Department of Population Biology, University of Leiden, Kaiserstraat 63, P.O. Box 9516, 2300 RA Leiden (The Netherlands)

(Accepted 9 March 1987)

ABSTRACT

Dinh, N.V., Sabelis, M.W. and Janssen, A., 1988. Influence of humidity and water availability on the survival of Amblyseius idaeus and A. anonymus (Acarina: Phytoseiidae). Exp. AppI. Acarol., 4: 27-40.

Amblyseius idaeus (Denmark & Muma) and A. anonymus Chant & Baker are morphologically very similar species of phytoseiids inhabiting areas in South America that have very different levels of humidity. Above 60% RH, nearly all eggs of both species hatch successfully, but below 60% RH the egg hatching rate of A. anonymus is very poor, whereas eggs of A. idaeus hatch at humidities as low as 30% RH. The mobile stages ofA. idaeus are better able to survive in absence of food and water than those of A. anonymus. Water availability promotes survival of both species, but its effect on A. idaeus exceeds that on A. anonymus. These differences in low-humidity tol- erance and survival ability are consistent with the climatic origin of these phytoseiid species; Amblyseius idaeus has been reported from very dry and humid areas, and A. anonymus from humid areas only.

In comparison with other phytoseiid species, the eggs ofA. idaeus have the highest tolerance to low humidities reported to date, and, among the phytoseiids that are shown to be capable of controlling Tetranychus spp., this tolerance appears to be exceptionally high. The impact of this result on the scope of biological control of Tetranychus spp. is discussed.

INTRODUCTION

Phytoseiid mites have been used successfully to control spider mites in ag- ricultural crops (Huffaker et al., 1970; McMurtry, 1982; Helle and Sabelis, 1985). Of the factors that determine their effectiveness, humidity appears to be of major importance (Tanigoshi, 1982; Sabelis, 1985). The egg stage is es- pecially sensitive to low humidity. As shown in Table 1, hatching success of

3To whom requests for reprints should be sent.

0168-8162/88/$03.50 �9 1988 Elsevier Science Publishers B.V.

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TABLE 1

Approximate levels of relative humidity (RH) 1 at which 15%, 50% and 85% of the eggs of different phytoseiid species hatch successfully

Species 2 RHI~ RHso RHs5 Reference

T. sessor 64 80 - - Sciarappa and Swift (1977) A. potentiUae 50 70 80 McMurtry et al. (1976)

(Netherlands) 50 60 75 Sabelis (1981) A. [allacis 45 60 75 Zhang and Kong (1985) A. limonicus 50 60 70 McMurtry and Scriven (1965) A. anonymus 50 55 70 Dinh et al, (1988) P. persimilis 3 50 70 95 Pralavorio and Almaguel-Rojas (1979)

50 - - 80 Begljarow (1967) 60 - - 75 Pruszynski (1977) 45 60 70 Sabelis (1981) 40 - - 80 Stenseth (1979)

A. pseudolongispinosus 50 - - 75 Xin et al. (1984) A. citri[olius 40 50 70 De Moraes and McMurtry (1981) A. potentiUae (Italy) 50 55 70 McMurtry et al. (1976) A. addoensis addoensis 50 - - 65 McMurtry (1980) A. addoensis rubicolus 20 50 60 McMurtry (1980) A. cirri 20 40 55 McMurtry (1980) P, longipes 30 - - 60 Badii and McMurtry (1984) A. hibisci 20 30 50 McMurtry and Scriven (1965) A. idaeus - - 30 40 Dinh et al. (1988)

1Temperatures are within the range 20-30 ~ C. 2See also Knisley and Swift's (1971) study ofAmblyseius umbraticus. 3See also Hamamura et al. (1978) for effects of humidity at low temperatures; at 10 ~ C, RHI~ = 60%, RHso = 80 % and RHs5 = 95 %. Additionally, see Ustchekov and Begljarow (1968).

most phytoseiids investigated so far is poor below 50% RH ( at 25 ~ C ), whereas experiments by Nickel (1960) and Hazan et al. (1973) showed that several Tetranychus species can thrive under conditions of low humidity and high tem- perature. Thus, the population growth rate of the predator is reduced or even blocked, whereas that of the prey is stimulated under these climatic conditions. Consequently, biological control may not be effective, as shown by Stenseth (1979) in a series of population experiments with Phytoseiulus persimilis Athias-Henriot and Tetranychus urticae Koch. Measurements of humidity in Dutch greenhouses showed that levels below 50% RH do occur for periods long enough to affect the egg hatching rate of P. persimilis (M.W. Sabelis, personal observation).

Clearly, there is a need to investigate within- and between-species differ- ences in low-humidity tolerance. The logical first step is to test populations of phytoseiid species that inhabit relatively dry geographic areas. There is evi- dence in support of the hypothesis that phytoseiids from dry areas are more

29

resistant to low humidities than are phytoseiids from humid areas (McMurtry and Scriven, 1965; McMurtry et al., 1976; McMurtry, 1980). For example, Am- blyseius hibisci (Chant) inhabits inland areas in California, where humidity is much lower than in the coastal areas, which is the habitat of another phyto- seiid, Amblyseius limonicus (Garman & McGregor). Compared to the latter species, the eggs of A. hibisci are more resistant to low humidity and, as can be seen in Table 1, they appear to be the most resistant of all phytoseiids inves~ tigated to date. Unfortunately, this predator is not effective in controlling Te- tranychus spp. (McMurtry and Scriven, 1965). Applying this second requirement, Phytoseiulus longipes Evans is the most promising biological con- trol candidate found to date, but its hatching success is still poor in the range of 30-45% RH. Hence, more species should be screened for low-humidity tol- erance and efficacy in controlling Tetranychus spp.

In this paper we report on the survival ability of two phytoseiids from South America: AmbIyseius idaeus (Denmark & Muma, 1973 ), which has been found in both humid and very dry areas in Brazil (De Moraes and McMurtry, 1983) and in Colombia (G.J. De Moraes, personal communication, 1985; N. Mesa, personal communication, 1986) and Amblyseius anonymus, Chant & Baker, 1965, which is morphologically very similar to A. idaeus but has only been found in the more humid parts (N. Mesa, CIAT, Colombia, personal commu- nication, 1986) of the same countries (De Moraes and Oliveira, 1982; De Mor- aes et al., 1982). The intrinsic rate of increase and the predation rate of both species are comparable to those of phytoseiids known to control Tetranychus spp. ( Dinh et al., 1988, this volume ). Thus, because of their distribution in dry and humid areas in South America, and because of their possible efficacy in controlling Tetranychus spp., it is worthwhile to test and compare the survival abilities of these two species at low humidity levels.

Another reason to study survival of A. idaeus and A. anonymus at low hu- midities is that both species are being considered for their ability to control Mononychellus tanajoa (Bondar) sensu lato, a pest of cassava in Africa be- lieved to have been imported via plant material some 15-20 years ago (Great- head et al., 1984; IITA, 1984). Because cassava is grown in areas that differ widely in mean level and range of humidity, and because the cassava green mite reaches pest levels most frequently in the dry season (Greathead et al., 1984; Yaninek and Animashaun, 1988; Yaninek et al., 1988), it is of major importance to determine the ability of phytoseiids to survive under these cli- matic conditions.

Although the effects on egg hatching are very important, low humidity will not have equally important effects on the survival of the mobile stages, as long as water can be obtained from prey or other food. When these food sources are scarce, low humidity may be associated with low water availability, so that adaptations to cope with the effects of these factors may be expected both in the mobile and the immobile stages of predatory mites. However, such an as-

30

sociation of factors and adaptations need not be present. Even in dry climates, water sources may be available through dewfall or plant guttation. As shown by Mori and Chant (1966), Blommers et al. (1977) and Sabelis (1981), access to drinking water markedly increases survival and overrides the importance of low humidity, for obvious reasons. Thus, when investigating the survival abil- ity in dry climates, both the effects of the water available to the mobile stages and the effect of low humidity on the immobile stages (eggs) should be investigated.

The experiments discussed in this paper were designed to answer the follow- ing questions: 1 ) What is the influence of low humidity on the survival of eggs, and the influ- ence of water shortage on the survival of nymphs and adults (males and fe- males) of A. idaeus and A. anonymus? 2) If there are interspecific differences, are they consistent with the climatic conditions and spatial distribution observed in the field? 3 ) How does evapotranspiration by the plant affect the microclimate near the leaves and, consequently, predator survival?

MATERIALS AND METHODS

Mite cultures

Samples of A. idaeus and A. anonymus were obtained from the Common- wealth Institute for Biological Control (CIBC), England, and from the Centro Internacional de Agricultura Tropical (CIAT), Colombia, and were reared on a diet of Tetranychus urticae Koch. The rearing units consisted of inverted plant pots placed in a layer of water on the bottom of a Perspex cage (1 X 1 X 0.7 m). Prey-infested bean leaves were placed on the plant pots three times per week. The approximate range of temperatures in the box was 18-22 ~ C and the relative humidity was 60-80%.

Climate control

The experiments on egg mortality were carried out in temperature- and hu- midity-controlled climate boxes. Temperature was maintained at 25~ and humidity at either 30, 40, 50, 60, 70, or 80% RH. The highest humidity level (95-100%) was achieved as follows. The cover glass of a Petri dish (18-cm dia) was turned upside-down and filled with water. After positioning a leaf with predator eggs on the water surface the dish was closed by what is normally the bottom part of the Petri dish. This lid was slightly tilted by placing a piece of plastic in the water layer at one side only, just below the rim. Care was taken not to lift the lid above water level. The slightly sloping position of the lid ensured that condensed water ran to the lower side instead of dropping down

31

onto the leaf, where it would have contacted the predator eggs. Eggs of phyto- seiids usually do not hatch after contact with water (M.W. Sabelis, personal observation).

Hatch ing success rate

Predator eggs were obtained from a sample of 20 females placed for 36 h in the climate cabinet on a few bean leaves with ample prey. After this oviposition period the females were removed, the eggs were counted, and leaves plus pre- dator eggs were transferred back into to the climate cabinet. Because the leaves

plast ic ine cover

Fig. 1. The plant system used in the experiments on egg hatching at different relative humidities. It consists of a Lima bean seedling in a small bottle sealed by plasticine around the stem of the plant (Sabelis, 1981).

32

are excised and damaged by the spider mites, they desiccate within a few h and will have little or no effect on the ambient humidity in the cabinet. Four days later the numbers of eggshells and desiccated eggs were counted to assess the fraction of eggs that hatched successfully. This experiment was carried out simultaneously with eggs ofA. idaeus and A. anonymus.

In an additional series of experiments, the influence of the plant's microcli- mate on A. anonymus was investigated by repeating the same experimental procedure, but using the plant system shown in Fig. 1 as a substrate in place of an excised bean leaf.

Survival o[ the mobile stages

Predators were reared in groups up to the protonymphal stage or up to the adult stage (male or female). Two days after the final moult, each predator was transferred to its own separate 4 X 1-cm glass tube. The tubes were closed by cotton plugs which were either moistened daily by 3-5 droplets of water, or kept dry. Survival of the predators was recorded daily at 25 ~ C and 70% RH. Mites were visually classified as dead or alive, but, if doubt arose, predators were considered dead if they did not respond to contact with a fine brush. This experiment was carried out simultaneously for each stage of A. idaeus and A. anonymus.

In an additional series of experiments, females of A. anonymus were pre- vented from contacting the moistened cotton plug by placing a piece of fine mesh gauze in the tube 0.5 cm from the plug. These experiments were carried out to determine the effect of within-tube humidity on survival and to estimate its relative contribution to the results of the previous experiment, where both within-tube humidity and free-water availability may influence survival.

RESULTS

Hatching success rate on excised leaves

The results in Fig. 2 show clear differences in low-humidity tolerance be- tween A. idaeus and A. anonymus. When RH was below 60%, very few or even no eggs ofA. anonymus hatched. Most eggs were shrivelled after i day. On the 2nd and 3rd day a flat spot marked the remnants of the egg and on the 4th day only a trace of the egg remained. The remnants of the shrivelled eggs cannot be mistaken by the torn parts of the egg chorion remaining after hatching, which keep their oval shape for a time period exceeding the duration of the experiment. In contrast to A. anonymus the eggs of A. idaeus were rarely ob- served to desiccate at low humidities, except at 30% RH where egg mortality rose to approximately 30%.

Above 60% RH the hatching success rate of both phytoseiid species was close

100

8O

6 0

40

20

0

A. i d a e u s

16o

30 40 50 60 70 80 95-100

Relat ive humid i ty , %

33

oJ

==

I

100

80

6O

40

20

91 0 i

3O

A. anonymus

T

116

40 50 60 0

123 9 5

I i

I t

~ i

80 95-10-0

Relat ive humid i ty , %

Fig. 2. A histogram of the egg-hatching rate of two phytoseiid species on excised leaves at 25 ~ C and different levels of humidity. The number of eggs used per experiment is presented in the top of each bar in the histogram.

to 100%, even at 95-100% RH. Survival at high humidities would have been much lower if the eggs were not prevented from contacting free water which condensed on the side of the vials. Direct contact with water causes the egg to be covered by a film of water, thus reducing gaseous exchange with the sur- rounding air.

Hatching success rate on a p lan t

In Table 2, the hatching success rates of the eggs of A. a n o n y m u s on bean plants and on an excised (rapidly desiccating) leaf are given. Comparison shows that the plant 's evapotranspirat ion causes egg-hatching to be more successful at intermediate levels of humidity (50-60% R H ) , but that it has virtually no

34

TABLE 2

The hatching success rate of the eggs of Amblyseius anonymus on excised (rapidly desiccating) leaves and on the leaves of living plants (see Fig. 1 )

RH (%) Hatching success rate ( % )

Excisedleaf n Plant n

30 0 91 0 142 40 0 116 1.2 172 50 8.4 119 48.6* 243 60 72.0 93 92.0* 224

*Significantly different (from results on excised leaves) at the 5% level according to binomial test for comparison of proportions.

l o o . . . . . . _ A. idaeus 25OC

80 \ \

\ x \ \ - 6 0

m 40

x \ \ \ 20

0 i N, ~ 1 L i ~ i ~ I I i I i lira ~ i I xq I

0 2 4 6 8 10 12 14 16 18 20

Time, day

I00~___ 80

} 6o

~ 4o

2 O

0 F i 0 2 4

A. anony.mus 25OC

A F

6 8 10 k , i L k . L ,

12 14 16 18 20

Time, day

Fig. 3. Survival curves of the nymphs ( N ) , adult males (AM) and adult females (AF) of two phytoseiid species at 25 ~ in absence (solid lines) and in presence (dashed lines) of a free water source. See also Table 3.

35

T A B L E 3

Survival t imes of d i f fe rent s tages of two phy tose i id species a t 25~ (70% R H ) wi th ( + ) or w i thou t ( - ) access to free water (Access)

Species Stage Access Survival t ime (days)

2 s n

Amblyseius idaeus n y m p h - 0.4 0.5 29 male - 1.1 0.6 37 female - 4.0 1.7 40

+ 7.6 4.4 3O A. anonymus n y m p h - 0.6 0.6 31

male - 0.5 0.6 42 female - 1.7 0.8 35

+ 5.2 1.9 35

M e a n (2) and s t a n d a r d dev ia t ion (s) were e s t ima ted graphical ly using Gauss ian probabi l i ty pa- per; n = n u m b e r of repl icates.

effect at lower humidities, where all eggs shrivelled irrespective of whether the substrate was a plant or an excised leaf.

Survival of the mobile stages

The most important conclusions emerging from the results presented in Fig. 3 and Table 3 are: (1) mean survival time of females exceeds that of males and nymphs; (2) mean survival time of A. idaeus females exceeds that of A. anon- ymus females; and (3) access to drinking water promotes survival of adult females. All these conclusions were supported by t-test for comparison of means at the 0.001 level.

The presence of a source of drinking water may explain the 3rd result, but it cannot be concluded directly. By moistening the cotton plug, free water is made available to the predator, but within-tube humidity may be increased as well. The latter factor, however, cannot have influenced the results because additional experiments showed that, when females of A. anonymus were pre- vented from contacting the moistened plug, mean survival time was 2 days ( n = 20), which is comparable with their mean survival time in tubes with dry cotton plugs (1.7 days).

D I S C U S S I O N

In the literature survey presented in Table 1, phytoseiid species are ranked according to the approximate critical humidity threshold at which 50% of the eggs fail to hatch. The ranking may not be too precise because the threshold humidities were crudely estimated by interpolation between available data

36

points, and because these data stem from experiments carried out at temper- atures ranging from 20 to 30 ~ C. De Moraes and McMurtry (1981) have argued that the differential effect of temperature on the egg-hatching rate is basically an effect of exposure time during the egg stage. They found support for this hypothesis by the relatively small effects of temperature on the relationship between the egg-hatching rate and the product of the water vapour pressure and the egg incubation period (the latter of which is strongly dependent on temperature). However, as these authors rightly pointed out, this product is rather sensitive to the imprecision of the measurement of the egg incubation time. As development was only inspected at 1-day intervals in most reports (which is long relative to the egg incubation period, especially at high temper- atures), the interesting correction method proposed by De Moraes and McMurtry (1981) is of little use here.

There is, however, little doubt that the low-humidity tolerance of the eggs of A. idaeus is exceptionally high compared to that of all other phytoseiids investigated to date (Table 1 ). This warrants a more detailed study to eluci- date the morphological and/or physiological properties that enable the eggs of A. idaeus to complete embryonic development under dry conditions.

It is tempting to suggest that the survival ability of the mobile stages of A. idaeus is also exceptionally high when compared to A. anonymus. This is in- deed what was found. However, scrutiny of the available data in the literature (Mori and Chant, 1966; Blommers et al., 1977; Sabelis, 1981) shows that the temperatures at which experiments were carried out are different and that the effect of temperature on survival is very significant. Though it may seem pos- sible to extrapolate from these studies to the temperatures used in our exper- iments, our attempts showed that the predictions were too sensitive to small errors and to the assumptions underlying the interpolation method. More com- parative studies at standard temperatures are needed before definite conclu- sions can be drawn.

It is probably true that the interspecific differences in low-humidity toler- ance of the eggs observed in this study are consistent with the known distri- bution of both species. The best evidence comes from comparing the tolerance of species that inhabit nearby geographic areas differing in the mean humidity level. Examples can be found in McMurtry and Scriven (1965), McMurtry et al. (1976), McMurtry (1980) and in this paper. De Moraes and McMurtry (1983) reported that A. idaeus was found under humid as well as under very dry conditions in Northeastern Brazil. Exact data on humidity are not avail- able, but according to De Moraes (personal communication, 1985 ) the rainfall in the driest areas where A. idaeus is commonly found does not exceed 500 mm/year. The distribution of A. anonymus, however, seems to be centered in more-humid areas, where rainfall is 800 mm/year or more. How these data on rainfall relate to the mean and variance in humidity and to the rainfall in areas where the phytoseiids listed in Table 1 occur is not known. A quantitative test

37

of the more precise null hypothesis t ha t the interspecific differences scale to the mean and variance of humidity in the habitat is, therefore, at present not feasible. Testing this hypothesis could be of importance in (foreign) explora- tion for new phytoseiid species as candidates for biological control.

Deviations from what is predicted by the above hypothesis may well be due to our lack of knowledge of the climatic conditions at the microhabitat level. Vegetation density and evaporation from soil and plant may be factors that have to be taken into account. Recently, Ferro and Southwick (1984) made calculations of the impact of atmospheric humidity on humidity within the leaf boundary layer, where the mites live. They showed that humidity in the unstirred air layer around the leaf is usually higher than the ambient atmos- pheric humidity. Stomatal opening and evapotranspiration of the leaf and the thickness of the unstirred boundary layer (which in turn are functions of many other factors ) contribute to the relatively higher humidity experienced by the mites on the leaf of an intact plant. This explains why the critical threshold of atmospheric humidity at which 50% of the eggs fail to hatch is lower when the substrate of the phytoseiid eggs is a living plant rather than a desiccated ex- cised leaf. Very similar results were found by Sabelis (1981), who studied egg hatching of Amblyseius potentillae (Garman) and P. persirnilis in the same experimental setup. The shift in the critical threshold humidity in this and the latter study was not spectacular, however, (from 60% RH to 50% RH) and, as shown by Sabelis (1981), the shift tends to become smaller and smaller with increasing temperature. Hence, it may be concluded that low atmospheric hu- midity associated with high temperature are significant selective factors in phytoseiid populations, i.e. little modified by plant-related factors. This may explain why macroclimatic data on, e.g., average rainfall seem to correlate well with humidity tolerance of phytoseiids inhabiting areas where temperatures frequently rise above 25 ~ C. However, caution should be exercised because the influence of vegetation structure on within-vegetation humidity remains to be assessed quantitatively.

That A. idaeus incurs low risks of egg mortality in dry environments may be of great significance for broadening the scope of biological spider-mite control. As this species is capable of eliminating T. urticae on Lima bean (N.V. Dinh and M.W. Sabelis, personal observation, 1985), and as it has an intrinsic rate of increase and predation rate similar to that of some phytoseiids that proved to be successful in controlling T. urticae (Dinh et al., 1988, this volume), it may be a promising agent for the control of this pest species. However, caution should be exercised, because other traits such as dispersal ability, searching behaviour, prey preferences, and survival on other food substances, have not yet been investigated in detail.

ACKNOWLEDGEMENTS

We thank Dr. A.C. Bellotti (CIAT) and Dr. N.W. Hussey (CIBC) for ship- ment of both Arnblyseius idaeus and A. anonymus, and the Netherlands Uni-

38

vers i t ies F o u n d a t i o n For I n t e r n a t i o n a l C o o p e r a t i o n (NUFFIC) for p rov id ing the f inanc ia l s uppo r t t h a t enab led the f i rs t a u t h o r to s tay for 6 m o n t h s a t the D e p a r t m e n t of P o p u l a t i o n Biology, U n i v e r s i t y of Leiden. Gi lber to de M o r a e s ( EMBRAPA; Braz i l ) , S teve Yan i nek ( IITA, Nige r i a ) a n d N o r a M e s a ( CIAT, Col- o m b i a ) c o n t r i b u t e d s igni f icant ly by p rov id ing i n f o r m a t i o n and by the i r com- m e n t s on the m a n u s c r i p t . T h e t echn ica l a s s i s t ance of Kees H o f k e r was m u c h apprec ia ted . T h e f igures were d r a w n by M a r t i n Br i t t i jn .

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