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EFFECT OF PREY DEPRIVATION ON SURVIVAL AND REPRODUCTION
OF NEOSEIULUS CALIFORNICUS (ACARI: PHYTOSEIIDAE) FEMALES
 N. M. GRECO, G. G. LILJESTHRÖM,
C. V. CÉDOLA & M. F. ROGGIERO *
(Accepted November 2005)
NEOSEIULUS
CALIFORNICUS
STARVATION
STRAWBERRY
FECUNDITY
ADULT SURVIVAL
PHYTOSEIIDAE
S: Neoseiulus californicus (MG) 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.
I
Phytoseiid mite species are predators commonly
used for the biological control of the two-spotted
spider mite, Tetranychus urticae Koch (H &
S, 1985; W, 1988; R, 1990; Z
et al., 1990; C et al., 1997; S et al., 1999;
Z, 2002). The effectiveness of phytoseiids for
biological control depends on different attributes
including their ability to survive conditions of food
shortage (D C W et al., 2004).
Neoseiulus californicus (McGregor) life style has
been rated between a type II and III (C et al.,
1998). It can provide biological control of T. urticae
over a wide range of climatic and management conditions (MM & C, 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 : 13-18.
— 14 —
exhibiting a high spatial coincidence with T. urticae
and a high ability to detect leaflets with prey (G
et al., 1999). Moreover, N. californicus has a higher
capacity to stay in patches with low pest density than
other phytoseiids (M & L, 1973; C et al.,
1998; P et al., 1999).
Field studies showed that T. urticae populations
usually decline to very low levels due to the preypredator interaction (N, 1991; G M
et al., 1991; S & G, 1995; N et al., 1998;
G at al., 1999) as well as to selective acaricide
applications which allow the persistence of the predator (C et al., 1998). In those situations predators may stay in the field with few preys (G et al.,
1999) and wait for the prey return or feed on other
sources while minimizing starvation (C 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 (S 1985a; S & J 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 (S, 1985a; M & T,
1994). Phytoseiid females surviving a period of food
deprivation are capable of reproducing after they
have been supplied with spider mites (HAMAMURA et al., 1978) and in N. idaeus the female to
male ratio of the offspring at the adult stage (secondary sex ratio) was unchanged (M & T, 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 (D C W et al., 2004).
Information exists on N. californicus about the
effect of food deprivation on adult longevity (D
C W et al., 2004), the effect on other
demographic parameters was only analyzed for Neoseiulus idaeus (M & T, 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 depri-
vation 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.
M  M
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) (S, 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, 60-70 % 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.
— 15 —
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 (Z, 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 (M et al., 1986;
C, 1989). NRR was compared among treatments by ANOVA. Following a significant ANOVA,
means were separated using the Tuckey test.
R
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 (F. 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
(F. 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) (F. 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)
F. 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) .
F. 3. Pre-reproductive period of N. californicus adult females fed
continuously on T. urticae (control) and starved for 48h and 96h.
— 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) were different (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 (5th day)
= 3.48, Z (6th day) = 3.48, Z (7th day) = 2.26; P < 0.05,
(F. 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
(F. 5). Expressing the mean number of eggs laid per
female in physiological age, differences were observed
in the second and third days (F. 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)
(X2 = 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
18.22 (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%.
D
F. 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).
F. 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).
F. 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 (B & V A,
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
H et al. (1978), B & V A-
— 17 —
 (1979) and M & T (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, D C W 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 M & L (1973) and C & S (1999). Similarly, M &
T (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 (V, 1968; F
& G, 1982) notwithstanding, the sex determining mechanism is not known (S, 1985b). The
sex ratio of progeny was not affected by prey deprivation episodes of the parental females of N. idaeus
(M & T, 1995). C &
S (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 (S et al., 1970;
C et al., 2001). However, N. californicus
could be able to persist within the agroecosystem even
at rather unfavourable conditions and low prey den-
sities because it may stay in a field with few prey
(G et al., 1999). Further, this predator has a
higher capacity to stay in patches with low pest density than other phytoseiids (M & L, 1973;
P 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.
A
We thank to Adrián M of INTA San Pedro
for providing strawberry runner plants.
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