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The influence of humidity and water availability on the survival of Amblyseius idaeus
and Amblyseius anonymus
Van Dinh, N.; Janssen, A.R.M.; Sabelis, M.W.
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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 the
survival of Amblyseius idaeus and Amblyseius anonymus. Experimental and Applied Acarology, 4, 27-40.
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Experimental & Applied Acarology, 4 (1988) 27-40
27
Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands
I n f l u e n c e of H u m i d i t y and Water A v a i l a b i l i t y on
the S u r v i v a l of A m b l y s e i u s i d a e u s and A.
a n o n y m u s ( Acarina: P h y t o s e i i d a e )
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 availabilitypromotes survival of both species,
but its effect on A. idaeus exceeds that on A. anonymus. These differences in low-humidity tolerance 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 agricultural 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 especially 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.
28
TABLE 1
Approximate levels of relative humidity (RH) 1at which 15%, 50% and 85% of the eggs of different
phytoseiid species hatch successfully
Species2
RHI~
RHso
RHs5 Reference
T. sessor
A. potentiUae
(Netherlands)
A. [allacis
A. limonicus
A. anonymus
P. persimilis 3
64
50
50
45
50
50
50
50
60
45
40
50
40
50
50
20
20
30
20
--
80
70
60
60
60
55
70
--60
--50
55
-50
40
-30
30
-80
75
75
70
70
95
80
75
70
80
75
70
70
65
60
55
60
50
40
A. pseudolongispinosus
A. citri[olius
A. potentiUae (Italy)
A. addoensis addoensis
A. addoensis rubicolus
A. cirri
P, longipes
A. hibisci
A. idaeus
Sciarappa and Swift (1977)
McMurtry et al. (1976)
Sabelis (1981)
Zhang and Kong (1985)
McMurtry and Scriven (1965)
Dinh et al, (1988)
Pralavorio and Almaguel-Rojas (1979)
Begljarow (1967)
Pruszynski (1977)
Sabelis (1981)
Stenseth (1979)
Xin et al. (1984)
De Moraes and McMurtry (1981)
McMurtry et al. (1976)
McMurtry (1980)
McMurtry (1980)
McMurtry (1980)
Badii and McMurtry (1984)
McMurtry and Scriven (1965)
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 temperature. 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 differences in low-humidity tolerance. The logical first step is to test populations of
phytoseiid species that inhabit relatively dry geographic areas. There is evidence 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, Amblyseius hibisci (Chant) inhabits inland areas in California, where humidity is
much lower than in the coastal areas, which is the habitat of another phytoseiid, 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 Tetranychus spp. (McMurtry and Scriven, 1965). Applying this second
requirement, Phytoseiulus longipes Evans is the most promising biological control 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 tolerance 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 communication, 1986) of the same countries (De Moraes and Oliveira, 1982; De Moraes 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 humidities is that both species are being considered for their ability to control
Mononychellus tanajoa (Bondar) sensu lato, a pest of cassava in Africa believed to have been imported via plant material some 15-20 years ago (Greathead 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 climatic 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 ability 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 following questions:
1 ) What is the influence of low humidity on the survival of eggs, and the influence of water shortage on the survival of nymphs and adults (males and females) 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?
MATERIALSAND METHODS
Mite cultures
Samples of A. idaeus and A. anonymus were obtained from the Commonwealth 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 humidity-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 phytoseiids usually do not hatch after contact with water (M.W. Sabelis, personal
observation).
H a t c h i n g 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 predator eggs were transferred back into to the climate cabinet. Because the leaves
plasticine 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 microclimate 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 prevented 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 between 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 observed 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
33
A.
idaeus
100
16o
8O
60
40
20
0
30
40
50
60
70
80
95-100
Relative h u m i d i t y , %
A. anonymus
100
123
95
80
T
oJ
6O
I
==
i
40
I
I
20
t
0
91
i
3O
116
40
50
60
0
~
i
80
95-10-0
Relative h u m i d i t y , %
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 surrounding air.
H a t c h i n g success rate on a p l a n t
In Table 2, the hatching success rates of the eggs of A. a n o n y m u s on bean
plants a n d on an excised (rapidly desiccating) leaf are given. Comparison shows
that the plant's evapotranspiration 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 )
R H (%)
Hatching success rate ( % )
30
40
50
60
Excisedleaf
n
Plant
n
0
0
8.4
72.0
91
116
119
93
0
1.2
48.6*
92.0*
142
172
243
224
*Significantly different (from results on excised leaves) at the 5% level according to binomial test
for comparison of proportions.
l o o
. . . . .
.
25OC
A. idaeus
_
\\
80
\x\\
-
60
m 40
x\\\
20
0
i
0
N, ~ 1
2
L
4
i
~
6
i
~
I
8
I
i
10
I
i
12
lira
14
~
i
16
I
18
xq
I
20
Time, day
I00~___
25OC
A. anony.mus
80
}
6o
~ 4o
2O
AF
0
0
2
F i
4
k
6
8
10
12
,
i
L
14
16
k.
L
,
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
TABLE 3
Survival t i m e s of different stages of two p h y t o s e i i d species at 25~
w i t h o u t ( - ) access to free w a t e r (Access)
Species
Stage
Amblyseius idaeus
nymph
male
female
A. anonymus
nymph
male
female
Access
+
+
(70% R H ) w i t h ( + )
or
Survival t i m e (days)
2
s
n
0.4
1.1
4.0
7.6
0.6
0.5
1.7
5.2
0.5
0.6
1.7
4.4
0.6
0.6
0.8
1.9
29
37
40
3O
31
42
35
35
M e a n (2) a n d s t a n d a r d d e v i a t i o n (s) were e s t i m a t e d graphically using G a u s s i a n p r o b a b i l i t y paper; n = n u m b e r o f replicates.
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. anony m u s 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 prevented 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).
DISCUSSION
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 temperatures 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 temperatures), 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 elucidate 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 indeed 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 possible to extrapolate from these studies to the temperatures used in our experiments, our attempts showed that the predictions were too sensitive to small
errors and to the assumptions underlying the interpolation method. More comparative studies at standard temperatures are needed before definite conclusions can be drawn.
It is probably true that the interspecific differences in low-humidity tolerance of the eggs observed in this study are consistent with the known distribution 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 available, 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 h a 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) exploration 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 atmospheric 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 excised 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 humidity 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.
T h a t 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 shipment of both Arnblyseius idaeus and A. anonymus, and the Netherlands Uni-
38
versities F o u n d a t i o n F o r 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 r o v i d i n g
t h e f i n a n c i a l s u p p o r t t h a t e n a b l e d t h e first a u t h o r to s t a y for 6 m o n t h s a t t h e
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. G i l b e r t o de M o r a e s
( EMBRAPA; B r a z i l ) , S t e v e Y a n i n e k ( IITA, N i g e r i a ) a n d N o r a M e s a ( CIAT, Colombia) contributed significantly by providing information and by their comm e n t s on t h e m a n u s c r i p t . T h e t e c h n i c a l a s s i s t a n c e of K e e s H o f k e r was m u c h
a p p r e c i a t e d . T h e figures were d r a w n b y M a r t i n B r i t t i j n .
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der Sovjetunion. Nachrichtenbl. Pflanzenschutzdienstes, 21 (47): 197-200.
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