larval development of the predatory midge feitieila ... · the two-spotted spider mite (tssm)...
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LARVAL DEVELOPMENT OF THE PREDATORY MIDGE Feitieila acarisuga
VALLOT (DIPTERA: CECIDOMYIIDAE) IN RESPONSE TO LlMlTED AVAILABILITY
OF ITS PREY Tetranychus urticae KOCH (ACARI: TETRANYCHIDAE)
by
Heidi Nadene Sawyer
M c . , University of British Columbia, 1991 .
THESIS SUBMllTED IN PARTIAL FULFILLMENT OF
THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF PEST MANAGEMENT
in the Department
of
Biological Sciences
O H.N. Sawyer 1998
SIMON FRASER UNIVERSITY
January 1998
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ABSTRACT
In order to evaluate the predatory midge Feltiella acarisuga Vallot as a biological
control agent for the two-spotted spider mite Tetranychus uttïcae Koch (TSSM) in
greenhouses, information is needed on its performance under conditions of prey limitation.
To study the effects of chronic low prey density, larvae were provided with 4 different
feeding treatments of 60 (approximately the maximum daily consumption) 30, 15, or 5 TSSM
eggs per day. Larval survival was significantly affected by prey availability with no lawae
surviving to pupation when provided 5 eggs per day. Among the groups with surviving
larvae, reduction in prey availability caused significant decreases in the total mite-egg
consumption and the dry weight at pupation. Pupal weight was a linear function of the total
number of eggs eaten.
To study the effects of short-tenn deprivation, larvae were first provided with either 60
eggs per day (well-fed) or 15 eggs per day (poorly-fed). After two days of feeding, larvae
were kept without prey for 0,1,2,4 or 6 days and then re-fed at the previous rate. A
proportion of larvae resumed feeding and reached pupation after al1 deprivation periods, but
survival decreased with deprivation time among both well-fed and poorly-fed larvae to a
minimum of approximately 30%. Developmental t h e increased significantly with increasing
deprivation time and was also significantly longer in the poorly-fed larvae compared to well-
fed larvae.
Total lifetime egg consumption and pupal dry weight were both significantly reduced
by deprivation among well-fed larvae but not among poorly-fed larvae. Among the well-fed
larvae, pupal weight and egg consumption were significantly reduced by shorter deprivation
times of one and two days, but were unaffected by longer deprivation times of four and six
days. These results appeared to have been influenced by behavioral changes during
deprivation. Lawae were very active after one or two days deprivation but became sedentary
at four, five and six days without prey. Daily feeding capacity was also reduced after four or
six days deprivation. Despite differing periods of deprivation, al1 well-fed larvae consistently
consumed more eggs than poorly-fed larvae and achieved higher pupal weights.
ACKNOWLEDGMENTS
I am very grateful to my senior supervisor Dr. Bemie Roitberg for his direction and
support during this study. I would also like to thank Dr. Dave Gillespie and Dr. Ron
Ydenberg for valued advice and editing, Nature's Alternative lnsectary and Dr. Dave
Gillespie for providing the insects, Ed Basalyga for collaboration in the experirnent in
chapter 2, and Cynthia Feil and Sue Robertson for technical assistance. Thanks also
go to the mernbers of the Roitberg lab, MPM students, and my farnily and friends who
have helped and encouraged me. Financial assistance was provided by the Western
Greenhouse Growers Cooperative Association, Agriculture and Agri-Foods Canada,
an NSERC grant to Dr. B. Roitberg and by several Teaching Assistantships at Simon
Fraser University. Statistical advice was provided by Robert Balshaw and lan
Bercovitz of the Statistical Consulting Group, Simon Fraser University.
TABLE OF CONTENTS ..
APPROVAL .................................................................................................................. II
m..
ABSTRACT.. ......................................................................................................... ..r II ACKNOWLEDGMENTS.. .......................................................................................... ..iv
TABLE OF CONTENTS ............................................................................................... v
LIST OF TABLES ....................................................................................................... .vi *.
LIST OF FIGURES ..................................................................................................... VII
1. INTRODUCTION ..................................................................................................... 1
2. EFFECTS OF CHRONIC LOW MITE DENSITY ON PREY
CONSUMPTION, SURVIVAL AND DEVELOPMENT OF F. ACARlSUGA
A. Introduction ................................................................................................. 1 O
B. Materials and Methods
i) Plant, Mite, and Insect Colonies .......................... ..... ...................... 13
ii) Experimental Arenas for F. acarisuga larvae ................................... 14
iii) Experimental Procedures and Analyses .......................................... 15
C. Results.. ...................................................................................................... 17
D. Discussion ............................................................................................... 1 9
3. EFFECTS OF TEMPORARY DEPRIVATION ON PREY CONSUMPTION,
DEVELOPMENT, SURVIVAL, AND ACTIVITY OF F. ACARlSUGA LARVAE
A. Introduction. ............................................................................................... .25 B. Materials and Methods ................................................................................ 28
...................................................................................................... C. Results. .31
D. Discussion. .................................................................................................. 33
4. CONCLUSIONS ..................................................................................................... 41
REFERENCES .......................................................................................................... .64
LIST OF TABLES
Table 1. Cornparison of pupation in F. acarisuga l a ~ a e reared with four
different densities of T. urficae eggs. At the lowest density of 5 eggs per day,
approxirnately half the larvae went missing and were presumed to have escaped,
............................................ and none of the remaining lawae reached pupation 45
Table 2. The means and standard deviations of the daily number of eggs of T.
urticae eaten by larvae of F. acarisuga during the first four days of feeding at
three different densities of eggs ........................................................................... 46
LIST OF FIGURES
Figure 1. A diagram of experimental arenas used to enclose and observe larvae of
F. acarisuga. a) petri dish filled with agar b) hole cut out of agar c) plastic
coverslip ............................................................................................................... 47
Figure 2. Number of F.acarisuga larvae reaching pupation on each day after
eclosion, while feeding at three different prey densities. Larvae were reared in
agar cells with 60, 30, or 15 eggs of T. urticae per day. Symbols V indicate the
mean developmental times for each treatment ..................................................... 48
Figure 3. Mean number of T. urticae eggs consumed by F. acarisuga during the
entire larval period at three different prey densities. Error bars indicate 95%
confidence intervals .............................................................................................. 50
Figure 4. Mean pupal dry weights of F. acarisuga after feeding at three different
densities of T. urticae eggs. Error bars indicate 95% confidence intervals ......... 51
Figure 5. The relationship between the total number of T. urticae eggs consumed by
F. acarisuga larvae, and the dry weight of F. acarisuga at pupation. Data from
larvae fed at al1 three prey densities are included. The regression equation for
the line is Y = 0.21 x - 2.28 (t = 0.91) .................................................................. 52
Figure 6. The relationship between the developmental time of F. acarisuga and the
dry weight at pupation. Data from larvae provided with three different prey
densities are included. Larvae feeding at the highest density had greater
vii
variation in pupal weight, whereas those feeding at the lowest density had greater . .
variation in developmental time ............................................................................ 53
Figure 7. The mean proportion of larvae of F. acarisuga surviving to pupation after
increasing periods of deprivation. Before and after deprivation, larvae were
provided daily with two different levels of prey density. Error bars indicate the
...................................................................................... 95% confidence intervals 54
Figure 8. The effects of deprivation time and prey availability on the developmental
time and survival of F. acariçuga. Vertical bars indicate the number of larvae
pupating on each day after hatching. Horizontal bars indicate the total number of
larvae surviving to pupation (shaded squares) out of the total number of replicates
for each treatment group. Symbols V indicate the mean developmental times for
each treatment ...................................................................................................... 55
Figure 9. The relationship between deprivation time of F. acariçuga during larval
development, and the total number of days taken to reach pupation. Larvae were
placed in cells with eittier 60 (well-fed) or 15 ( poorly-fed) eggs of 7: urticae per
day before and after the deprivation period. The regression equations are Y =
1 2 7 x + 6.69, P = 0.68 (poorly-fed and Y = 1.31~ + 4.74, r2=0.75 (well-
fed). .................................................................................................................... ..57
Figure 10. The effects of feeding rate and increasing periods of larval starvation on
total mite egg consumption of F. acarisuga l a ~ a e . Error bars indicate 95%
confidence intervals .............................................................................................. 58
Figure 11. The effects of feeding rate and increasing periods of larval starvation on
dry weight of F. acarisuga pupae. Enor bars indicate 95% confidence
............................................................................................................... intervals -59
Figure 12. Mean number of eggs eaten by E acarisuga lawae on each day after
hatching. Larvae were reared in agar cells with 60 eggs of T. utficae per day and
starved for 0, 1, 2,4, or 6 days. There were significant differences in the number
of eggs eaten on the third day of feeding (marked with symbol m) among the five
treatment groups .................................................................................................. 60
Figure 13. The proportion of larvae of F. acatisuga moving when observed at 24-
hour intervals after food deprivation. Only those larvae that eventually recovered
to reach pupation were included. Prior to and after the deprivation period, either
60 (well-fed) or 30 ( poorly-fed) eggs of T. urticae per day were available to each
larva. .................................................................................................................... .62
Figure 14. The relationship between the developmental time of F. acansuga and the
dry weight at pupation. Larvae of F. acarisuga were placed in cells with either 60
(well-fed, filled symbols) or 30 (poorly-fed, unfilled symbols) eggs of T. urticae per
day, and after 2 days of feeding were deprived for increasing Iengths of
time.. ..................................................................................................................... 63
Chapter l
INTRODUCTION
A. Tetranychus urticae
The two-spotted spider mite (TSSM) Tetranychus urticae Koch (Acarina:
Tetranychidae) is an important pest in British Columbia vegetable greenhouses,
affecting three major crops: tomatoes, long English cucumbers, and bel1 peppers.
TSSM colonizes the undersides of leaves, where it punctures leaf cells and feeds on
plant fluids. This results in physiological damage to plant cells and reduced growth of
al1 organs(Tomczyk and Kropczynska, 1985). Infested plants become brittle, develop
a chlorotic mottling and become covered with a fine webbing. TSSM damage is
correlated with a reduction in yield of tomatoes (Stacey, 1985). Damage to tomato
greenhouse crops in B.C. has been increasing over the past ten years and there are
currently no satisfactory methods of control for TSSM on tomatoes.
A new control method rnust be compatible with the integrated pest
management approach recommended for vegetable greenhouses in B.C. (B.C.
Ministry of Agriculture, Fisheries and Food, 1996). A number of biological control
agents are released in greenhouses including Encarsia formosa for the control of
whiteflies, and Aphidius rnafricariae and Aphidoletes aphidimyza for the control of
aphids. Since chemical pesticides could interfere with these natural enemies, their
use is kept to a minimum. Growers of greenhouse crops also prefer biological control
over chemical control for a number of other reasons including: cheaper cost, reduced
exposure to toxins, and public concems about health and the environment (van
Lenteren and Woets, 1988).
One chemical acaricide, Vendex (fenbutatin-oxide), is recommended for use
against TSSM on tomato (B.C. Ministry of Agriculture Fisheries and Food, 1996).
Growers must wait 5 days between the application of this chernical until the crop can
be harvested. Residues of Vendex are not tolerated in the US., where a large
proportion of tomatoes are exported. Furthemore, resistance of TSSM to this
pesticide is likely to develop if used extensively; some resistance to this pesticide has
been reported (Tian et al, 1992, Goodwin et al, 1995). Vendex, although highly
effective, is used by growers only as a last resort. To achieve adequate control of
TSSM on greenhouse tornatoes and to avoid or reduce the use of Vendex, an
effective natural enemy is needed.
The predatory mite Phytoseiulus persimiiis has had widespread success in the
control of TSSM on many greenhouse crops (van Lenteren and Woets, 1988). It is
commercially available to B.C. greenhouse growers and has been effective on
cucumber and pepper crops. However, P. persimiis has limited effectiveness on
greenhouse tornatoes.
Nihoul and Hance (1 993) reported that P. persimilis tended to disappear from
the crop and fail to control subsequent infestations. In another study, the predators
had difficulty in establishing in the top third of tomato plants, where spider mite
populations were increasing rapidly (Nihoul, 1993). These problem were attributed to
unfavorable abiotic conditions.
Other studies have shown that glandular trichomes covering the epidemis of
tomato stems inhibit the rnovement of P. persimiiis on tomato plants, and may explain
their inability to control new infestations (van Haren et al, 1987). Glandular hairs
were toxic to P. persimiiis, and the predator had a shorter life span and lowered
fecundity on tomato leaves than on bean leaves (Gillespie and Quiring, 1994).
Higher temperatures and light intensity may increase the density and size of these
hairs as the growing season progresses (Nihoul, 1993). A natural enemy able to
avoid tomato stems and petioles might prove more effective for TSSM on tornatoes.
To identify new potential biological control agents, a survey of natural enemies
of TSSM in the Fraser Valley was conducted in 1992 and 1993 (Gillespie et al, 1994).
Bean plants infested with TSSM were placed in the field for one week, after which al1
insects and mites were collected from the leaves. The most abundant species
collected was the predatory gall midge Feltiella acansuga Vallot, occurring at al1 three
sites sampled between May and September (Gillespie et al, 1994).
Of al1 the natural enemies collected, F. acarisuga was one of only three which
were specialists on spider mites. Of these three, only F. acansuga had the ability to
both reproduce under laboratory conditions and to avoid the sticky hairs of tomato
plants. Since this predator has a winged adult stage, it can fly to new TSSM
infestations without contacting the tomato stems and petioles. These factors made F.
acansuga a promising candidate for further study as a biological control agent for
TSSM.
B. Feltiella acarisuga
The adult female midges of F. acarisuga lay eggs on infested leaves, amongst
spider mite webbing. A single female may lay more than 30 eggs (Gillespie et al,
1994). The eggs hatch after about two days, and the emerged larvae begin to feed
on al1 developmental stages of TSSM. Even newly-hatched larvae are capable of
feeding on adult spider mites. Atter feeding for 4-6 days, larvae spin a cocoon,
usually near a vein. Adults emerge after a pupal stage of approximately 4-6 days.
Developmental time is strongly affected by temperature, ranging from 35 days at 15
OC to less than 10 days at 27°C (Gillespie et al, 1994). Humidity has a strong effect
on the rate of predation, which is highest in the 80-90% range (Opit, 1995).
Feltiella acarisuga has a cosmopolitan distribution which spans North America
and most of Eurasia (Gagne, 1995). In various parts of the world, F. acarisuga and
related species have been recognized as important mite predators and described as
voracious predators (Barnes, 1933). F. acansuga was found at densities as high as
160 lawae 1 152 cm2. of eggplant leaf in Mauritius (Moutia, 1958). Species of Feltiella
were the dominant predators of spider mites on strawberty plants in Califomia
(Oatman et al, 1985) and in Japanese cedar plantations (Takizawa and Torri, 1974).
F. phi was one of the three most abundant predators found associated with spider
mite infestations in Texas corn fields (Pickett and Gilstrap, 1986). The number of
mites consumed by F. acarisuga was estimated to be 8ight times as much as P.
persimilis (Opit et al, 1997).
Despite its voracity and widespread abundance, F. acarisuga has had
unpredictable success in controlling mites. One problem in the field has been that
the species tends only to respond numencally to spider mite denstty late in the
growing season (Gagne, 1995, Barnes, 1933). Its dependency on high mite density
may prevent it from playing a role in controlling mite populations earlier in the year
(Gagne 1 995).
F. acansuga rnay be a more effective predator in the greenhouse situation
because the favorable environment may allow it to persist for most of the year. This
predator has had some success in greenhouses in the U.K., where it is produced
commercially (Shaddick, 1995). F. acarisuga is now also available commercially in
British Columbia and is currently used by cucumber, pepper and tomato greenhouse
growers in British Columbia. Some B.C. greenhouse growers are reporting that they
are achieving successful control of spider mites using F. acarisuga, while others
remain unsatisfied. The lack of knowledge about the biology and population
dynamics of F. acarisuga makes it difficult to understand the reasons for its erratic
performance and to recommend this predator to growers.
C. Predicting the Success of a Biological Control Agent
Predicting the performance of a biological control agent has always been
difficult due to the cornplex interactions involved in the population dynamics of a
predator or parasite. In practice, a trial- and- error approach is typically used,
and there has been an ongoing debate over whether this approach is sufficient
or whether biological control should have a more scientific, predictive basis (Van
Lenteren, 1980, Kareiva, 1990).
A better understanding of a biological control agent and a comprehensive
theory of its role in reduction of the pest may help a) provide information on rnethod
and rate of release b) identify the conditions, such as temperature and crop, under
which the agent is successful or unsuccessful, so that these conditions can be best
manipulated c) give insight on the attributes or the type of organisms leading to
successful biological control under different circumstances. Such knowledge will aid
in the selection of future biological control agents.
Existing theory has resulted in the development of many Iists of attributes for
the evaluation of natural enernies. These include some essential criteria such as the
ability to develop to the aduR stage in or on the host, the ability to develop and
reproduce in the climatic conditions under which they will be used, the lack of
negative effects on any other natural enemies or other nonpest organisms, and good
method of mass production (Van Lenteren and Woets, 1988).
0 t h criteria have been concerned with density-responsiveness including
aggregation and searching efficiency (Van Lenteren, 1980, Van Lenteren and Woets,
1988). It was thought that good density responsiveness led to a stable equilibrium
and that stability in turn led to better biological control (Beddington et al, 1976). Both
of these premises are probably false; Murdoch et al (1985) demonstrated that a
stable equilibnum is not required for successful biological control Also, the emphasis
on long-term control rnight not be relevant on the time scale of a growing season in
the greenhouse, and populations unstable Iocally (Le. at the plant level) can be stable
at the larger spatial scale of a greenhouse (Noldus and Van Lenteren,l990, Kareiva,
1990). Furthemore, aggregation of natural enemies to high-density patches rnay or
rnay not lead to stability (Murdoch, 1990) or to successful biological control (Hirose et
al, 1 990, Noldus and Van Lenteren, 1990). Consequently, screening for density-
dependent traits in natural enemies rnay not be useful.
Other criteria deemed important for a biological control agent concem the
relative ability of the natural enemy to increase in numbers and to suppress the Pest
population, including a high pest kill rate, high fecundity, fast generation time, and
high larval survival (Van Lenteren and Woets, 1988, Van Lenteren, 1980). These
traits can Vary depending on a number of factors including prey density.
If a natural enemy only performs well in areas of high density, it rnay not be
able to suppress the pest below the economic threshold, which is the goal of
biological control programs. If Pest density becomes too low, traits such as survival
and fecundity rnay be affected such that the natural enemy cannot keep up with the
pest or rnay be driven to extinction. This rnay explain why it is now thought that
natural enemies found in areas of low density, rather that those isolated during an
outbreak, make the best biological control agents (Waage, '1990). For these reasons,
it will be useful to examine the response of biological control agents under conditions
of prey limitation, which is the focus of this thesis.
Studying specific attributes in isolation rnay give important insight into the
biology and behavior of a biological control agent, but it has little predictive value.
Waage (1 990) referred to this as the reductionist approach; in reality, traits are not
independent of one another and some combinations rnay be rarely found. Van
Lenteren (1 980) pointed out that since the criteria are relative (i.e. 'high' fecundity,
'good' searching ability) they are difficult to rate.
A more integrated approach can be aided by mathematical models of
biological control, which can be used to predict predator-prey or host-parasite
population dynamics under different conditions (eg Sabelis, 1981, Van Roermund et
al, 1997, Hulspas-Jordan and Van Lenteren, 1989). Models have been criticized as
lacking direct relevance to the practical ope rations of biolog ical control (Van
Lenteren, 1980, Kareiva, 1990). However, the increasing sophistication of modeling
techniques aided by computers gives thern a greater potential to fine-tune biological
control programs and increase our understanding of factors leading to success. A
greenhouse provides an ideal environment for the development of theoretical models,
as it is an enclosed, homogeneous environment with controlled temperature.
To provide data that can be incorporated into models, the behavior and life
history of natural enemies needs to be documented and explained, focusing on
aspects known to have an effect at the population level.
D. Rationale and Objectives
The experiments in this thesis were designed to study the effects of limited
prey availability on the survival, mite consumption, pupal size and developmental
tirne, of F. acarisuga lawae. Two different patterns of prey limitation were studied. In
the first experiment, larvae were contained with different levels of daily prey supply
throughout their development. In the second, two-day-oid larvae were deprived of
prey for increasing periods of time, then subsequently re-fed.
F. acarisuga Iarvae could conceivably be exposed to these conditions in the
greenhouse because of the spatial and temporal variation in the abundance of their
prey. T. urticae occurs in a clumped distribution both among and within leaflets
(Johnston, 1997, Sabelis, 1985). The adults of F. acarisuga preferentially lay their
eggs in high-density patches when given a choice (Basalyga, 1997), thus newly-
hatched larvae are provided with nearby prey. However, the patch may be of less-
than-optimal quality or may decline in quality during the course of larval development
due to predation on or dispersa1 of the mites.
Prey availability during the developmental period has been shown to have an
effect on a variety of life history traits in insects and mites including survival (Eveleigh
and Chant, 1982, Beddington et al, 1976, Glen, 1973), prey consumption (Zheng et
al, 1993a, Fleschner, 1950, Scott and Barîow, 1984), growth rate (Mills, 1981, Zheng
et al, 1993a), developmental time (Pickup and Thompson, 1990, Zheng et al, 1993a),
pupal or adult weight or size (Scott and Barlow, 1984, Zheng et al, 1993a, So and
Dudgeon, 1989) and fecundity (Honek, 1993, Visser, 1994, Zheng et al, 1993b,
Tammaru et al, 1996, Pitcairn and Gutierrez, 1992, Xue and Ali, 1994 ). These are
al1 important cornponents of the population dynamics of a predator which will greatly
affect its performance as a biological control agent.
The prey consurnption per larva of F. acarisuga under different conditions of
prey availability will directly influence rates of predation in the greenhouse. The prey
death rate, concerned with the number of prey consumed in relation to prey
distribution and abundance, is one of the main cornponents of arthropod predation
(Hassel1 et al, 1976). Knowledge of the prey requirements of Iarvae may also help
explain whether prey densities in the greenhouse are sufficient for the survival of
predators and whether larvae can reach pupation on a single tomato leaflet, thus
avoiding the glandular hairs of tomato stems.
Survival, developmental rate, and fecundity of predators al1 directly influence
the rate at which the predator will increase in numbers (Le. the numerical response),
which is the other main cornponent of arthropod predation (Beddington et al, 1976).
The ability to survive at low prey densities or without prey affects whether the
population will persist over time in the greenhouse. F. acansuga is currently released
comrnercially in the pupal stage, and the emerging adults lay eggs in patches
throughout the greenhouse. If the resulting larvae cannot survive to adulthood at the
mite densities found in the greenhouse, then new predators would have to be
released in each generation. This would increase costs to the grower.
In order to avoid extinction, a minimum population size is required (Goodman,
1987, Stewart and Hutchings, 1996). Fecundity will likely be proportional to the body
size of adults as it is in many other insects (Honek, 1993, Visser, 1994, Zheng et al,
1993b). Prolonged developmental time will delay production of eggs by the next
generation. Thus, reduced body sire and prolonged developmenta1 time also
influence the viability of subsequent generations of predators.
In addition, Iarval sire is likely to influence consumption rate at any given tirne.
Thus, if larvae do not reach maximum size under certain conditions, they will not
express the highest potential consum ption rates.
Information from the two aforementioned experiments will be used in the
development of models to describe the relationship between F. acafisuga and TSSM.
The information will also be useful in the commercial rearing of the insect, as it will
indicate the number of prey required per larvae for their survival, for rapid
development, and for the production of the highest quality adults.
Chapter 2
EFFECTS OF CHRONIC LOW MITE AVAILABIUTY ON PREY CONSUMPTION,
SURVIVAL, AND DEVELOPMENT OF E ACARISUGA LARVAE
A. Introduction
Limited resources during development can prevent insects from feeding and
growing at the optimal rate. As the availability of resources decreases below a level
required for basic maintenance, mortaIity will reach 100%. Even at feeding rates well
above the minimum requirements, mortality due to 'food stress' occurs in many
arthropods (Beddington et al, 1976). However, many insects have the ability to
complete their development under a wide range of less-than-optimal prey densities
without high mortality. When this occurs, food limitation will invariably have effects on
aspects of development and behavior, as the animal needs to compensate in some
way for the limitation in food.
The functional response, describing the number of prey killed per unit time as
a function of prey density, generally increases with prey density according to an s-
shaped curve or a saturation curve until it reaches a plateau (Holling, 1966, O'Neill,
1989). When food levels fa11 below the point of this plateau, consumption rate of prey
decreases and therefore less energy is available for growth. Growth rate was found
to have a linear relationship with consumption rate in coccinellids (Mills, 1981) and a
variety of other arthropods (Beddington, 1976).
Because growth is slower than that at higher prey densities, an animal feeding
at a low prey density cannot possibly become an adult at both the optimal time and
size. This discussion primarily refers to animals with complex life cycles (Wilbur,
1980) that undergo some type of metamorphosis between the immature stages and
adulthood. In these animals, energy acquisition for growth is usually confined to the
larval stage whereas reproduction is confined to the adult stage. If the time of
metamorphosis to adulthood occurs at fixed tirne, then a reduction in prey density will
resuR in smaller adults. On the other hand if adult size is fixed, then developmental
time would need to be extended to reach this size.
If both developmental tirne and size were fixed and inflexible, then only
individuals feeding at a prey density allowing the optimal growth would obtain this
size in the available time. At lower densities, 100% mortaIity would occur. To survive
a food shortage where optimal growth rate is not possible, an animai must either
becorne a smaller than normal adult or have a longer developrnental tirne, or both.
However, both a smaller adult size and a longer developmental time will
reduce the fitness of the animal. In a wide range of insects, adult size or weight is
correlated with fecundity or with other fitness components such as longevity or
searching efficiency (Honek, 1993, Visser, 1994, Tammaru, 1996, Pitcairn and
Gutierrez, 1992). Developmental time is also likely to lead to a decrease in fitness
due to the delayed production of offspring, increased chance of random rnortality and
increased exposure to predators.
Because of these fitness consequences, there is a tradeoff between pupating
at a reduced size and continuing to feed, extending the developrnental tirne.
Consequently, many animais have sorne degree of flexibility in both their
developrnental time and size at varying food densities inctuding fish (Taylor and
Freedberg, 19841, spiders (Turnbull, 1965). lygaeid bugs (Solbreck et al, 1989),
mosquitoes (Tirnmermann and Briegel, 1993), Iacewings (2 heng et al, 1993b),
coccinellid lanrae (Baumgaertner et al, 19811, and syrphid flies (Cornelius and
Barlow, 1 980).
Total prey consumption can also be affected by food availability. lnsects such
as lacewings can complete their development after feeding on a greatly reduced
number of prey relative to undeprived individuals (Fleschner, 1950, Zheng et al,
1993a). This usually occurs if developmental time in a deprived individual is not
prolonged. However in other species, such as the noctuid Pseudaletia unipuncfata
(Haworth), lamal developmental time is greatly increased and total food consumption
is greater that that of undeprived individuals (Mukerji and Guppy, 1970). Thus, a
range of interactions between developmental time, developmental size, and
consumption are possible when food is limited.
Flexibility in developmental time, size, and prey requirements enables an
animal to survive under a greater range of prey densities; this may be an adaptation
to a variable habitat. Since TSSM exist in a patchy distribution, it was hypothesized
that F. acarisuga would also have flexibility in their larval feeding and development,
enabling them to survive over a range of prey densities. Tfierefore, this experiment
was designed to test the effects of varying IeveIs of prey availability on survival, mite
consumption, pupal weight and developmental time of F. acarisuga.
B. Materials and Methods
i) Plant, Mite, and lnsect Colonies:
Lateral shoots of tomato plants were obtained from Gipaanda Greenhouses,
Surrey, B.C., dipped in rooting hormone, and planted in trays containing Sunshine
Mix 1, Sun Gro Horticulture Ltd. The trays were placed at 20" C with a photoperiod of
16 h Iight: 8h dark and uncontrolled humidity. After approximately two weeks, shoots
were transplanted into 10.5 cm. pots containing a mixture of heat-sterilized soi1 with
10g slow-release fertilizer pellets per 10 1 of soil. These plants were maintained
under the same conditions and removed as needed. Whole plants were removed for
the rearing of T. urticae and leaflets were removed both for oviposition of T. urticae
and for leaf disks used in the experimental procedures.
Two-spotted spider mites were obtained from infested tomato leaflets at
Gipaanda Greenhouse Ltd., Surrey, B.C. and placed on tomato plants in cages in a
room which ranged between 18 and 26 C, and 40 to 60% humidity. New tomato
plants were added to the cage as needed, and heavily damaged plants removed.
This colony was the source of mites used in al1 experimental work.
Selecting mite eggs directly from the colony was difficult due to the large
amounts of webbing. Also, TSSM eggs mature and hatch within a period of 2-3 days.
To prevent hatching during the experiment, and to obtain a steady supply of mite
eggs, the following protocol was used. Several tomato leaflets were placed top-
down on wet cotton in a petri dish, or held upright in floral tubes. Ten to fifteen adult
female mites, removed from the colony, were placed on each leaflet and left in the
same room. Freshly laid eggs were taken daily from these leaflets as needed.
F. acarisuga eggs were obtained either from mite-infested bean leaves sent by
courier from either Agriculture and Agri-food Canada Research Station, Agassiz, B.C.
or from Natures Alternative Insectary Ltd., Nanoose Bay, B.C.. Leaves were
maintained at 7 O C after arriva1 for up to 4 days and removed before use. Eggs with a
red eye-spot, indicating they were close to hatching, were chosen at the start of each
experiment.
i;;) Gc-perimental Arenas for F. acarisuga larvae
In order to cany out these studies, a method of containing and observing
individual larvae of F. acarisuga was needed, and several problems precluded this.
The larvae are extremely small and are very active when hungry, so they tend to
escape most containers. The larvae also require high hurnidity, drying up easily
when exposed to typical lab conditions. Finally, the larvae along with their prey
needed to be easily observed under the microscope without disturbance. For these
reasons, containing the larvae effectively was initialty a major setback to performing
deprivation experiments.
The following protocol was developed which keeps F. acarisuga larvae
contained, maintains high humidity and allows larvae to be viewed from either the top
or bottom of a leaf disk. A 90mm petri dish was filled to 5mm with hot agar solution
(at a concentration of 2.2 g powderl 100 ml.). When the agar had set, eight holes
were cut from it with a 16mm cork borer, and a 16mm tornato leaf disk was placed in
the bottom of each hole. To provide uniformity, Ieaf disks were always cut so that the
midvein bissected them, and T. urticae eggs were placed one third on the rnidvein
and a third each on either side of it. To reduce potential hiding places for F.
acarisuga larvae, only Young, very flat leaflets with small midveins were selected.
The resulting cells were approximately 5 mm deep and 16 mm diameter. Each cell
was sealed with a square of clear plastic which had four small pin holes in it (Fig. 1).
Preliminary trials showed that F. acarisuga could develop to adulthood inside
these cells and the leaf disk did not dry out. The larvae did not appear ?O be
disturbed when the dish was tumed upside duwn for observation. The humidity
inside the cells could not be detemiined but is likely near saturation.
iii) Eicperimental Procedures
This experirnent was conducted under a 16h light / 8 h dark cycle at a
temperature of 24'1 O C . Using the experirnental arenas as described above, four
different densities of mite eggs were placed on the leaf disks in each cell: 1) 60 eggs
(observed to be approxirnately the maximum rate of feeding), 2) 30 eggs, 3) 15 eggs,
and 4) 5 eggs. Eggs were nomally selected the day before they were used and
stored overnight at 70 C. E acarisuga eggs were placed individually, using a fine
pin, on the midvein of leaf disks in cells containing the appropriate number of mite
eggs. F. acarisuga eggs which had hatched within a six-hour interval were marked
and the remainder were discarded. Those that had hatched were placed on shelves
in random positions.
On subsequent days, the larvae were checked at 24 hour intervals, the
number of eggs eaten was recorded and pupation or death observed. On their first
day, Iawae are extremely small and delicate and so they were left in the same cell to
avoid handling them. The number of eggs eaten was recorded and these eggs were
replaced. Any dark colored eggs, indicating they were close to hatching, were also
replaced with fresh ones. On al1 foilowing days, Iawae were transferred each day to
a new ceil with new eggs in a fresh agar petri dish. To transfer a larva, its side was
gently touched with a fine pin, to which it would stick, and then it was gently brushed
off against the new leaf disk. Seventy-two hours after its pupation was first observed,
each pupa was removed from its cocoon and placed in a drying oven at 40% At
least one week later, each pupa was weighed on a Cahn electrobalance to the
nearest 0.1 pg.
It was necessary to perform this experiment in 4 batches. A chi-square
analysis (Zar, 1984) was performed using al! 4 batches pooled together to determine
whether suwival was significantly affected by feeding treatment. These batches were
also pooled for a linear regression of pu pal size vs. egg consumption.
In al1 further analyses, one of the batches was discarded since it included only
larva at the two lowest feeding rates. Batch was included as a randorn factor in these
analyses. Daily egg consumption during the first four days was analyzed by a 3-way
GLM procedure in SAS (version 6.1 1) with batch, age, and feeding treatment as
factors. Developmental time, pupal weight, and egg consumption were ail analyzed
by 2-way GLM procedure with batch and feeding treatment as factors. Prior to the
analyses, a log transformation was performed on the pupal weight data and a
squareroot transformation on the egg consumption data. The Bonferroni procedure
was used for multiple comparisons between treatrnent groups.
C. Results
A chi-square analysis showed that limited availability of eggs significantly
affected the survival of Iarvae (p< 0.001). No larvae survived to pupation at densities
of 5 eggs per day and nearly haIf the larvae in this treatment group disappeared
(Table 1). Missing lame were presumed to have escaped, since larvae were
sometimes seen crawling through the ventilation holes. Suwival rates were 69.6% at
15 eggs per day and 88.9% at the two highest egg densities of 60 and 30 eggs per
day.
The effects of food availability on developmental time are displayed graphically
in Figure 2. Lanrae pupated after an average of 5.4 k1.1 days, 5.8 +1 .O days, and
8.0 f 2.9 days for the 60, 30 and 15 eggsl day densities respectively. However, no
significant effects were detected among the developmental times of these three
groups (pc 0.1 9) and the power of this test was found to be quite high (0.86).
Despite the lack of significant differences among the mean developmental
times of the three treatment groups, two trends in the data can be obsenred from Fig.
2. a) The number of larvae pupating at the minimum time of 5 days decreased as
egg availability decreased. When 60 eggs per day were available, al1 larvae pupated
at the minimum time of 5 days with two exceptions. When only 15 eggs per day were
available, al1 surviving individuals delayed pupation by at least one day. b) Mite
availability limited to 15 eggs per day appeared to increase the variabitity in
developmental time relative to those larvae provided with 30 or 60 eggs per day. The
coefficient of variation (C.V.) of developmental time was similar for the larvae
provisioned with 30 (C.V. = 20.3%) and 60 (C.V. =17.4%) mite egg, but was nearly
doubled for Iarvae provided with 15 eggs per day (C.V.= 36.5%) (Fig. 2).
Daily egg consumption during the first four days after hatch increased
significantly with feeding treatrnent (pc0.0001) and with the age of the larva
(pc0.0001). There was also a significant interaction between feeding treatment and
age (p<O.OOOI)(Table 2). Batch had no significant effect on daily egg consumption
by larvae (pc0.32).
Among the three treatments with surviving larvae, feeding treatment had a
significant effect on both total egg consumption (p< 0.0003) (Fig. 3) and pupal weight
(pc 0.0007) (Fig. 4). Batch also had a significant effect on egg consumption
(p~0.02)~ but not on pupal weight (pc 0.13). Multiple comparisons revealed that al1
levels of feeding treatment differ significantly from one another in both egg
consumption and pupal weight.
When data from al1 batches were combined, there was a strong correlation
between egg consumption and pupal weight (h 0.91) and the dope of the
regression Iine was significantly different from zero (p<0.001). Pupal weight
increased Iinearly with the number of eggs eaten between a minimum weight of 8.3
pg and a maximum of 28.Opg (Fig. 5). Whereas variation in developmental time was
highest arnong larvae at the lowest feeding treatment of 15 eggs per day, the reverse
was true for pupal weight (Fig 7). The coefficient of variation of the pupal weight
increased as egg density increased, and nearly doubled between the 15-egg-per day
treatment (C.V. = 7.9 %) and the 60-egg-per-day treatment (C.V. = 13.7%).
D. Discussion
This study has demonstrated that larvae of F. acariçuga can respond to
continuously low prey availability by both extending their developmental time and
pupating at a smaller size, in common with rnany other insects which frequently
encounter food shortage.
Flexibility in developmentai tirne and size allowed larvae to survive over a
range of prey availability between 15 and 60 mite eggs per day. A decrease in the
prey availability from 60 to 30 eggs per day had no apparent effect on survival, but at
15 eggs per day, survival was reduced to 69.8%. Five eggs-per-day was not
sufficient for any larvae to survive to pupation under the conditions of this experiment.
Mortality will occur when the availability of prey is not sufficient to cover the
energy costs of growing to reach the minimum size. At very low food levels, no
larvae can cover such costs, while at slightly higher levels a few succeed. Above a
certain level, all larvae can reach the minimum size so that the percentage pupation
stays the same (Gilpin and McClelland, 1979). In mosquito larvae, percentage
pupation increased as a function of log of the food density, reaching about 95% at
higher levels (Gilpin and McClelland, 1979).
Random mortality in deprived larvae rnay also increase due to the longer iarvai
life span. It is also possible that the daily transferring of these delicate larvae with a
pin contributed to their mortality, and had more effect in the deprived larvae due to
their smaller size and greater food stress.
Mean total consumption by the larvae supplied with 15 eggs per day was
about half the mean consumption by lanrae supplied with the maximum number of
eggs. Similar values occurred in deprived lacewing larvae (Zheng et al, 1993a).
Consurnption in F. acarkuga was similar for a11 groups on the first day of feeding, but
large differences in consumption occurred from day 2 on (table 2). The larger size of
older larvae increases their maximum daily consumption, such that the provided egg
numbers become more and more Iimiting. Even the highest egg provisioning level of
60 eggs appeared to be limiting on the fourth day, when larvae consumed most of the
eggs provided. Nagakawa (1986) reported that Feltiella sp. was capable of
consuming 80 eggs per day at temperatures up to 25 OC.
The daily consumption rates observed in this experiment are based on the
assumption that predators will remain in an area with a given density, and thus may
not be accurate under natural conditions. Under low prey conditions, lanrae of F.
acansuga tend to leave tomato leaflets sooner (Johnston, 1997). Therefore, l a ~ a e
that were able to survive and reach pupation with the prey provided in this
experiment may have actually left the area had they not been confined. Had they
Ieft, their survival and consumption would be determined by their ability to locate new
patches of spider mites, The abilfty of larvae to locate new patches on tornato
leaves needs to be investigated.
No significant differences in developmental time were found among the
treatrnent groups. The high variation in developmental time, especially in the lowest
feeding treatrnent, rnay have made it difficult to detect any differences. Another
problem is that the tirne to pupation was only measured to the nearest day. Any
differences in developmental time rnay have been too small to be detected
statisticaily. More detailed experiments would be required to determine the effects of
prey density on developmental time of F. acarisuga. However it is clear from these
results that F. acafisuga can pupate over a large range of ages from 5 to 16 days,
thus their developmental period can be extended more than 300% of the minimum
time. Many other insects also extend their developmental tirne to varying degrees
when food is limited. While developmental time in Mefasyrphus corollae could be
extended by only 15% when prey was limited (Scott and Bariow, 1984), that of the
pitcher plant mosquito was extended by 50% (Moeur and [stock, 1980) and Ephydra
cinera by over six hundred percent (Collins, 1980). P. persimilis extended its
nymphal stage by 30%; the stage had a duration of 2.6 days at limited prey density
compared with 2 days at ample supply (Eveleigh and Chant, 1982).
A large range of sizes is also possible for F. acarisuga, clearly dependent on
egg availability and consumption. A linear relationship between consurnption and
pupal weights was also reported for the lacewing Chrysoperia camea (Zheng et al,
1993a). The minimum weight value, describing the lowest percentage of the optimal
weight at which an insect can pupate, can be as low as 12% in some insects (AngeIo
and Slansky, 1984). Judging from this value, the flexibility in pupal size of F.
acatisuga appears to be not as great as in other insects; in this experiment, the
smallest pupa had a weight 29.6% of the largest one. However, when pupae from
several greenhouses were collected and weighed (data not shown), the dry weights
ranged from 20.9 to 60.7 pg, thus pupal weights up to double the maximum found in
this experiment are possible.
A number of theories have been developed to explain the size and time of
metamorphosis in anirnals with complex iife cycles, including amphibians and
holometabolous insects. Wilbur (1 980) defined a complex life cycle as one that
involves an abrupt, irreversible switch in morphology and physiology, usually
associated with habitat change. At rnetamorphosis, F. acarisuga switches from a
larval growth stage with limited mobility, confined to the 2-dimensional surface of the
leaf, to the winged adult reproductive stage.
The data as presented in Fig. 6 appeared to show an inverse relationship
between the size and timing of metamorposis in F. acarisuga. According to a model
developed for mosquitoes, this type of relationship can be explained simply by
minimum thresholds of time and size required for metamorphosis (Carpenter, 1984,
Gilpin and McCleIland, 1979). When food is limiting, larvae will grow more slowly and
take more tirne to reach the minimum size. When food is abundant, larvae will grow
quickly and become much larger than the minimum mass when they reach the
minimum time.
This mode1 may explain in part the results of the experiment described in this
chapter. Latvae of F. acarisuga apparently require a minimum time of 5 days and a
minimum mass of approximately 8 pg to pupate (fig 6). Latvae supplied with the
highest daily egg density nearly always pupated at the minimum time. These larvae
had also relatively high variability in their pupal mass, which probably depended on
the variable amount of prey they were able to encounter and consume in the limited
time period. Conversely, at the lowest daily egg density, larvae were al1 close to the
minimum mass and had relatively high variability in their developmental time,
probably dependent on the variable amount of time taken to reach this minimum
mass.
Other theories consider also the trade-offs between mortality risk and growth.
If one knows the relationship between growth rate, size, and mortality on fitness, then
the size at metamorphosis that maximizes instantaneous population growth rate can
be determined (Werner, 1986). Under limited food density, growth rate is slower and
mortality is increased, shifting the optimal size to a smalter one.
Size and timing of metamorphosis in F. acansuga could also be explained by
stochastic dynamic theory (Mangel and Clark, 1988). According to this theory, larvae
would make decisions which lead to optimal lifetime fitness based on their
physiological state. Once a larva has surpassed the minimum size for pupation then
it has the option, within each time period, of either pupating or continuing to search
and feed. If it pupates, it will sacrifice the potential of becoming larger and having
greater fecundity as an adult. On the other hand if the larva continues feeding, then
its lengthened Iarval period exposes it to a greater chance of mortality due to
predation, stan~ation, or random factors. The lower the prey density, the less
additional size a larva gains per unit time by continuing to feed. Thus when prey
density is low it is likely to becorne more advantageous to pupate at a reduced size,
even if fecundity wiil suffer.
Collins (1980) suggested that the degree to which an insects extends its
developmental time under food stress should be inversely related to the mortality
risks of its environment, and the degree to which it reduces its size under stress
should be related to the importance of size to adult fitness. It appears from the
results in this chapter that when exposed to food stress, larvae of F. acansuga first
sacrifice size, and only extend their developmental time when the extension is
necessary to reach the minimum size. This may suggest that it is more crucial to the
fitness of individuals of F. acansuga to develop quickly than to reach the maximum
possible size. On the other hand, growth constraints may make it physically
impossible to reach the maximum possible size at low prey densities.
Although this experiment was intended to test the effects of constant low
densities on the development of larvae, in effect prey denstty was not held constant.
Larvae were fed only once per day. As they consumed eggs, the density became
lower until it reached zero. Larvae supplied with 15 eggs per day, for exarnple,
tended to consume al1 the eggs within the 24-hour period, after the first few days. It
is not known at what point during the 24-hour period that this normaily occurred, but
in separate observations, hungry larvae were observed to consume a single mite egg
in between one and 4 minutes when 2-3 days old, and 20 to 60+ minutes when only
1 day old. Depending on the efficiency of searching for eggs, it is possible that the
larvae in the 15-egg/ day treatment group typically consumed al1 the eggs within the
first few hours, and then were subjected to over 20 hours of starvation.
Thus, it may not be a low prey density perse that causes larvae to pupate at a
reduced size, but continuously fluctuating densities. This is an unavoidable
consequence of the experimental design used for this study. Another problem is that
larvae fed at the same 'rate' do not have the same feeding history; chance plays a
large role in how many eggs larvae ate since their search paths are random. Thus
random success in searching could account for much of the variability in this
expenment, particulariy in developmental the. A 'lucky' larva which happens to
locate an egg within the first few minutes of being transferred to a new cell may
behave very differently from an 'unlucky' one. In an ideal experiment, larvae would
be fed a set amount of eggs at set time intervals to overcome these problems. Due
to the short life span, high consumption, and small size of the larvae, such an
experiment is not practical.
The association of F. acarisuga with high mite densities was suggested to be a
limiting factor in its potential as a biological control agent (Sharaf, 1984, Pickett and
Gilstrap, 1986). However, high densities of spider mite populations have only been
common after the advent of synthetic pesticides (Huffaker et al, 1970). Congdon et
al (1993) showed that the mite predator Stethorus punctum picipes, previously
thought of as a 'high density' predator, was actually adapted to low mite populations
and capable of locating rare patches early in the season. The ability of larvae of F.
acarisuga to develop and survive to adulthood with limited number of prey suggests
that they might be adapted to surviving under low prey densities in nature, and
therefore might perform well under similar conditions in the greenhouse.
Chapter 3
EFFECTS OF TEMPORARY DEPRIVATION ON SURVIVAL, PREY
CONSUMPTION, DEVELOPMENT, AND ACTIVITY OF E ACARISUGA LARVAE
A. Introduction
The previous chapter demonstrated that pupal mass, developmental time,
mortality, and prey consumption of F. acarisuga are al1 affected by the number of
prey provided daily. However, due to the patchy distribution of TSSM, prey may not
be so consistently available to F. acarisuga in the greenhouse situation. The density
of spider mites varies temporally and tends to crash due to predation or
overexploitation of the leaf by the spider mites (Sabelis and Dicke, 1985). In addition,
lanrae of F. acarisuga are more likely to leave an area when the mite density is low
(Johnston, 1997), and may therefore have to travel across areas devoid of prey until
a new spider mite patch is located. The effects of periods of 24 hours or more
without prey on F. acarisuga larvae need to be investigated.
When animals are deprived of food, energy intake is no longer available for
growth and metabolism. In order to meet rnetabolic needs, body reserves will be
metabolized and if these are depleted, mortality will occur. In contrast to an adult,
which can go on reproducing when starved until it has exhausted its reserves,
mortality in a lania means that no reproduction will even take place (Zeigler, 1985).
Thus, adaptations to prolong survival are important in larvae likely to experience
ternporary starvation.
The risk of mortality from starvation will depend on both the amount of storage
reserves and the speed at which they are used up. Animals often store greater-than-
normal energy reserves in preparation for predictable periods of time without food,
such as migration or pupation (Pond, 1981, Downer and Matthews, 1976, Dixon et al,
1993). Anirnals that frequently experience unpredictable food shortages may store
greater reserves than those living under more stable food conditions (Santini and
Chellani, 1995, White, 1968). In addition, a reduction in metabolic rate during
stanration has been observed in many anirnals including leeches (Man, 1956),
freshwater snails (Calow, 1974), mantids (Matsura, 1981), and crabs (Mandsen et al,
1973). The greatest reductions in metabolic rate are often found in those animals
needing to survive long periods of time without food such as spiders (Tanako and Ito,
1982a, Anderson, 1974), ticks, (Lighton and Fielden, 1995), and high-shore lirnpits
(Santini and Chelazzi, 1995). These mechanisms allow animals to survive temporary
periods at food densities that would not be adequate on a longer-terni basis.
A temporary petiod of starvation can also affect prey consumption,
developmental time, and developmental size. Developmental time can be extended
because of the interruption in growth. However, many insects display an increased
rate of feeding after a starvation period (Slansky and Rodriguez, 1987, Zheng et al,
1993a, Rollo, 1984, Sangpradub and Giller, 1994). Increased consumption after
deprivation can enable some anirnals to increase their growth rate and 'catch up' to
undeprived individuals. Compensatory growth has been docurnented in
fish(Pederson et al, 1990, Dobson and Holmes, 1984) and rnammals and birds
(Wilson and Osborne, 1960) but similar studies on insects are lacking.
If animals are able to fully compensate for a period of starvation, there may be
no effects on developmental time or size. However, if the length of the deprivation
penod increases such that it is impossible to catch up to undeprived individuals, then
either size, developrnental time, or both will inevitably be affected. Under such
conditions, two opposing strategies are possible when food becomes available after a
deprivation period. First, the deprived animal might try to partially compensate for the
interruption in developrnent by increasing its developmental rate, becoming an adult
as soon as it reaches its minimum size. Altematively, the animal may extend its
developmental time even further in order to reach its maximum size.
In the first situation, prey consumption may be greatly reduced because the
animal sacrifices additional food in order to reach adulthood sooner. In the second
situation, prey consumption by an animal experiencing deprivation may be equal to or
greater than that of an undeprived individual, because the animal resumes feeding
until the maximum size is attained.
This experiment was designed to determine the effects of different lengths of
starvation on survival, pupal weight, mite consumption, and developmental time on
lama8 of F. acarisuga. The deprivation period started two days after hatching, when
lawae were still below the minimum size for pupation (8.3 pg) observed from the
previous experiment. The effects of a period without food may depend on the
amount of food available before and after the starvation period, therefore this
experiment also tested the above effects on both 'poorly-fed' and 'well-fed' larvae.
Starved animals will often change their behavior in relation to unstarved
individuals (Bell, 1991). In insects and mites, deprivation can increase speed of
movement (Dixon and Russel, 1972, Rotheray and Martinat, 1984, Glen, 1975) and
percentage of time spent moving (Blommers et al, 1977), both of which should
increase the chances of locating a new patch of food. However, in order to survive
penods of starvation, animals may need to reduce movement to conserve energy;
thus there are two conflicting possible strategies. To examine whether larvae of F.
acarisuga increase or decrease their level of activity over an extended period of time
without prey, the behavior of each larva (searching or resting) was recorded on each
day of the starvation period.
B. Materials and methods
The procedure described previously for containing F. acarisuga larvae was
modified for this experiment because there were two main difficulties with the
experimental arenas that needed to be addressed. Firstly, in the previous
experiment a large number of the larvae went missing at the lowest feeding rate of
five eggs per day. On a number of occasions, small larvae had been observed in the
process of escaping through the holes in the cover, or their tracks were observed on
the agar outside the cell. Therefore it was assumed that larvae were able to escape
through the pin-holes, and that they tended to do so when food was severely limiting.
For this reason larvae were almost certain to escape during a starvation period
of several days, and so pin holes were not used, and the glass coverslips were used
in place of plastic squares. The lack of pin holes resulted in increased condensation
within the cell, but this was considerably reduced when the concentration of agar was
increased to 3.0gI 100mL. Any condensation was cleared off the coverslip during the
daily observations.
The second problem was that the agar would usually become contaminated
with fungi and bacteria when left for several days. The longest starvation period in
this experiment was 6 days. Because disturbance could possibly change the
behavior of larvae in response to starvation, it was desirable to leave them in a single
cell for the entire period rather than transferring daily.
To avoid contamination during this period, the agar was autoclaved and the
petri dishes were prepared in a laminar flow hood using sterile technique. During
preparation of the agar cells and during transfer or observation of larvae, the work
space and al1 equipment used were cleaned with 70% ethanol. Furthemore, smaller
petri dishes (55mm) and wells cut individually (one per dish instead of 8) also helped
to reduce disturbance and contamination and to randomize the experiment.
After autoclaving the agar, ethanol was run through the hose of a pipette
pump, which was used to measure 11 rnL of agar into each petri dish. Agar-filled
petri dishes were left in the flow hood ovemight to cool, then stored in sealed plastic
bags at 70 C for up to one month. One day before use, cells were prepared as
descnbed in chapter 2 by placing either 15 or 60 eggs on each leaf disk. Individual
eggs of F. acarisuga having a red eye spot were placed in the center of each leaf
disk, and those that did not hatch within a four-hour period were discarded. Those
that hatched were randomly assigned to one of four groups which would experience
differing lengths of starvation: control (no starvation), 2,4 or 6 days starvation. Since
larvae were also already divided into well-fed (60 eggs per day) and poorly-fed (1 5
eggs per day) groups, this resulted in a 2 X 4 factorial design. This experiment was
performed in two batches, and in the second batch an extra treatment of 1 -day
starvation was added, resulting in a 2 X 5 factorial design.
For two consecutive days after F. acarisuga hatched, the number of mite eggs
eaten per day was counted at 24-hour intervals. The deprivation period began at
two days of age, when al1 remaining prey eggs were removed from the treatment
groups and the larvae were left without food for the appropriate length of tirne.
Controls continued to be fed daily at the same rate of 15 or 60 eggs per day.
During the starvation period, each lama was observed every 24 hours and
recorded as either alive or dead. If alive, it was recorded as either 'searching' or
'resting'. Some lawae were moving only their head; they were included as
'searching' in the analyses. The coverslip was lifted for a few seconds each day to
provide for exchange of gases.
After the end of the starvation period, lawae were again transferred daily to
fresh cells containing 15 or 60 mite eggs. The number of eggs eaten per day was
subsequently recorded until death or pupation. Three days after pupation, pupae
were dried and weighed, as in chapter 2.
A 3-way contingency table and further tests for partial dependence (Zar, 1984)
were used to examine the effects of deprivation time and feeding treatment on
survival of larvae to pupation. Pupal weight and egg consumption data were
transformed by taking the log and squareroot respectively. The transformed data
were analyzed using the GLM procedure in SAS (version 6.1 l), with batch included
as a randorn factor. Multiple comparisons were performed on these data in SAS,
using a contrast to compare the effects of deprivation times to the controls at each
feeding level. The number of eggs eaten on the third day of feeding (immediately
following the starvation period) was subjected to GLM analysis and multiple
comparisons performed using the Bonferroni procedure. The GLM procedure was
also performed on developmental time to test for a possible interaction between prey
density and starvation time.
C. Results
ln both the pooriy-fed and well-fed groups, survival decreased with increasing
deprivation time (Fig. 7 and 8). Chi-square analysis revealed that survivat,
deprivation time and feeding treatment were not independent of one-another
(0.005<pc0.01). Tests for partial dependence showed that deprivation time had a
significant effect on survival (p<0.001), but that survival was independent of feeding
treatment (0.75<p<0.9).
Figs. 8 and 9 show the change in developmental time of the surviving larvae
with increasing length of deprivation. For the surviving larvae in the well-fed 4-day
and 6-day starved groups, deprivation generally increased developrnental time
beyond the length of the deprivation period and increased the variation in
developmental time. There were significant effects of both deprivation time
(pc0.0001) and feeding treatment (pc0.0006) on deveiopmental time. However there
was no significant interaction effect between the two factors (pe0.82) and plots of
developmental time vs deprivation time had nearly identical slopes for the well-fed
(slope =1.31) and poorly-fed (slope = 1.27) treatment groups (fig. 9). Batch had no
significant effect on developmental time (~~0.88) .
Among the surviving larvae, both feeding treatment (pc0.0001) and
deprivation time (p<0.0002) had a significant effect on total egg consumption (Fig 10)
and there was an interaction between the two factors (pc0.0053). Similariy, both egg
density (pc0.0001) and starvation time (p<0.0006) had a significant effect on pupal
weight, but no interaction effect was detected (pc0.088) (Fig 11). Batch had no effect
on pupal weight ( ~ ~ 0 . 6 1 ) or mite egg consumption (~~0 .87 ) .
When multiple cornparisons were performed at each IeveI of egg density
comparing the 4 treatments to the control (alpha = 0.05/4 = 0.0125), there were no
significant differences in egg consumption or pupal weight among any of the poorly-
fed groups. However, some differences were detected among the well-fed groups.
Among the well-fed larvae, 1 and 2 day starvation periods caused significant
differences in both pupal weight and egg consumption, compared to the unstarved
controls, and those starved only one day had the lowest egg consumption and the
smallest pupal weight of al1 groups. 4- and 6-day starvation periods had no
significant effect on either pupal weight or egg consumption compared to the
controls.
For the well-fed larvae, starvation also had a significant effect on egg
consumption on the third day of feeding, i.e. the day immediately following starvation
(p<0.01). Egg consumption on that day increased for larvae starved only one day,
but then decreased after the longer starvation times (fig 12). For the group starved
one day, al1 larvae consumed very close to the maximum number of eggs (60) but the
mean consumption was not significantly different from that of the control larvae. Onty
the egg consumption after 4- and 6-days starvation was significantly different from
the controls.
Activity levers of larvae are displayed graphically in Fig 13. Nearly al1 larvae
were 'searching' on the first and the second day of starvation as compared with day
zero (immediately before the starvation period), when a high proportion were 'resting'.
During the first two days, often a maze of tracks was seen on the coversiip of the
cells, showing that larvae had circled the cells many times. The proportion of latvae
'searching' began to decrease on day three, and after three days the majority of
larvae became sedentary. Those which were still classed as 'searching' on day four,
five and six were doing so very slowly, often only moving their heads. 'Resting'
larvae were often seen with their heads raised.
P. Discussion
In the aforementioned expenment, mortality in F. acarisuga lawae after a
starvation period of 1 or 2 days was similar to that of the controls, whereas a 4- or 6-
day starvation period resulted in a large proportion of the larvae dying before
reaching pupation. A similar pattern occurred in mosquito larvae that were starved at
48 hours of age; there was no die-off until day 3, after which larvae died in
exponential fashion over the next 4 days (Gilpin and McCleIland, 1979).
Previous observations suggested that latvae of F. acarisuga were capable of
surviving extended periods of 10 days or more (Gillespie, 1992, personal observation,
1995), but it appears that only a small proportion of the original population would be
capable of doing so. Several factors put small populations at risk of extinction,
including a lessened ability to find mates, loss of genetic diversity, and the greater
potential for random effects to wipe out the entire population (Goodman, 1987,
Stewart and Hutchings, 1996). Thus the high mortality of E acarisuga after several
days without prey may limit the viability of subsequent generations in the
greenhouse.
Survival ability under natural conditions or in the greenhouse may be different
from that observed in the laboratory. Larvae with greater ability to avoid starvation
might be selected for under conditions where mite density is low. The larvae used in
this experiment were obtained from colonies, which are presumably fed ample prey.
Therefore, survival ability would not have been selected for, and rnay have been
lower than it would be in nature either due to genetic drift or due to antagonistic
pleiotropy with other important traits. Furthemore, in a natural setting larvae would
not be isolated from other individuals, and cannibalism could play a role in extending
survival. Further studies are needed to understand the importance of F. acarisuga
larval survival to higher-level phenomena.
Among the larvae that did survive, starvation had a significant effect on
developrnental time (Fig. 9). This was inevitable due to the fact that the starvation
period in most groups extended beyond the minimum developmental time of 5 days.
Only larvae starved for one day had the potential to pupate at the minimum time of 5
days; these larvae in fact tended to do so (Fig 8). In al1 other groups, developmental
time was extended by stanration. The effect of starvation on developmental time was
the same in poorly-fed and well-fed larvae; the slopes were nearly identical (Fig. 9).
Since both slopes were greater than 1 (Fig. 9), it appears that on average, larvae
extend their developrnental time by a length greater than that of the starvation period.
This may be partially due to the reduction in consumption rates of the larvae starved
for the longer times (Fig.l2), requiring additional days of feeding to compensate.
In chapter 2, the effects of chronic prey availability on developmental time
were difficult to assess and no significant differences were detected among the
developmental time of Iarvae supplied with 60,30 or 15 eggs per day. However the
results from this chapter show significant differences in developmental times of larvae
provided with 60 or 15 eggs per day, and this difference occurred across al1 the
different deprivation times, including the control. Thus, it can be concluded that
chronic low prey availability of 15 eggs per day significantly increases developmental
time cornpared to 60 eggs per day.
Deprivation also had significant effects on both the total lifetime egg
consumption and the pupal weight of the surviving larvae. The graphs of egg
consumption (Fig 10) and pupal weight (1 1) appear very similar and the analyses of
both factors gave very similar results.
Multiple cornparisons revealed that none of the poorly-fed groups differed
significantly from one-another in either egg consumption or pupal weight. The control
larvae fed only 15 eggs per day are perhaps consuming the minimum number of
eggs required, and pupating at the minimum size that is physiologically possible.
Therefore neither egg consumption nor pupal weight can be further decreased
sign ificantly by starvat ion.
However, deprivation had significant effects among the well-fed groups. Only
the egg consumption and pupal weights of larvae starved for 1 or 2 days were
significantly smaller than the controls. Lawae starved for the longer periods of 4 and
6 days were were not significantly different in mite egg consumption or pupal weight
from the control larvae. Arnong the well-fed larvae, al1 starvation times resulted in
very few larvae over 25 pg, which were fairly common in the undeprived control
group.
The minimum developmental time of 5 days and the minimum mass of 8 pg,
observed in the previous chapter, was confirmed by this experiment (figs. 6,14).
Furthermore, larvae of F. acarisuga pupate at five days even if they have
accumulated enough mass before this time. In a preliminary experiment (results not
shown) larvae were starved after 3 days of feeding. Larvae that had consumed a
minimum of approximately 50 eggs, resulting in a mass of approximately 8 pg,
tended to pupate during the starvation period, but they waited until day 5 to do so.
Those that had not consumed 50 eggs did not pupate until more prey was provided
following the deprivation period.
In the current experiment, al1 the deprived larvae in the well-fed group had
pupal weights much larger than the weights displayed by the larvae in the poorly-fed
group (Fig. I I ) . Similarly, the total egg consurnption of larvae was always much
higher in the well-fed larvae compared with the poorly-fed larvae, regardless of
deprivation time (Fig 10). One extended period of starvation does not have nearly as
great an effect on these larvae as a chronic shortage of prey. The well-fed larvae
kept feeding even when they had surpassed both their minimum time and size for
pupation, and recovered to nearly-normal size.
The results for larvae deprived only one day appear sornewhat different.
These larvae had lower average pupal weight than any other group (fig 11). ln
addition, most of these larvae also did not extend their developrnental time but
pupated on the sarne day as the unstarved controls.
The reason for this may be related to the limited ration of 60 eggs available.
The data on consumption rates on the third day of feeding suggest that larvae initially
increase their consumption after one day of deprivation (Fig 12). The control larvae,
on their third day of feeding, consumed a highly variable number of eggs behveen 20
and 55, out of a total of 60. By contrast, al1 larvae in the 1 -day stanration group
consumed between 54 and 60 eggs on the first day that they were re-fed.
In this experiment, the consumption following one day of starvation was not
significantly different from consurnption by the controls. However, the differences
may have been more pronounced if the maximum number of eggs supplied was
higher than 60, since the stawed larvae in particular were probably capable of
consuming more than 60 eggs. A number of other insects greatly increase their
consumption rates after starvation (Barton-Browne, 1975, Rollo, 1984, Sangpradub
and Giller, 1994) Third instar larvae of the lacewing Chrysopeda carnea were able to
compensate for previous deprivation consurning numbers of prey which exceeded
that of undeprived larvae, even though their size was smaller (Zheng et al, 1993a).
These anirnals have a digestive system capable of a much greater feeding rate than
that which typically occurs under non-starvation conditions, which may be an
adaptation to frequent starvation.
Further expenments using either a greater number of prey or a shorter time
period after starvation are needed to understand whether larvae of F. acarisuga also
significantly increase consumption rate after deprivation. However it is obvious that
somewhere during the 24-hour feeding period, larvae which had been previously
starved for one day became deprived of food a second time. This second
deprivation rnay be the factor leading to the smaller pupal weights and the lack of
extension in developmental time of the larvae starved for one day, and rnay be
having lesser effects among the iawae deprived for 2 days. If these lawae had
access to an unlirnited number of prey following deprivation, it is likely that they would
be able to exploit these prey and obtain pupal weights closer to those of the control
larvae.
By contrast, larvae starved for longer periods of 4 and 6-day (including only
those that eventually pupated) consurned significantly less eggs than the controls.
Thus, it appears that while the daily consumption capacity of F. acarisuga rnay
initially increase during food deprivation, it later decreases to well below that of the
controls. Similarly, Calow (1 375) found that the ingestion rate of snails increased
with starvation at a progressively reducing rate, and became reduced after 144 hours
stawation. In predatory mites, consumption rate increased after 2 days starvation,
but decreased after 4 or 6 days (Blomrners et al, 1977). This decrease in
consumption rnay be due to a slowing down of metabolic processes during food
limitation, or to physiological damage. Either way, a reduced capacity for feeding
rnay partially explain why 4-6 days stawation resulted in a small reduction in pupal
weight among the well-fed groups.
Furthemore, if these larvae starved for longer periods are consuming the
available eggs more slowly than those starved only one or two days, they are not as
likely to experience deprivation a second time. This rnay explain why these larvae
tended to continue feeding for several days after deprivation (fig 12) and why their
pupal weights were higher than those of larvae deprived for shorter periods of time.
The increased mortality with longer starvation times rnay not have occurred
randomly among larvae, and rnay have biased the analyses of the survivors. For
example, it rnay be that bigger larvae are more likely to survive than smaller ones.
Without this bias, the average pupal weights in the starved groups couid be expected
to be smaller than that actually obtained. However this would likely only cause a
important change in the data in the 6-day starved group, where mortality was highest.
The few surviving larvae in this group still had pupal weights that were over twice as
large as the minimum weight for F. acarisuga pupae.
The proportion of larvae observed moving was very low, especially in the well-
fed groups, immediately prior to sta~ation when the larvae had recently fed. After
one or two days starvation, this proportion increased dramatically (fig. 13). At 4 to 6
days starvation, the proportion moving was again close to zero. A similar pattern of
initially increased activity and then a decrease with prolonged starvation has been
observed in a number of animais such as fruit flies and predatory mites (Bell, 1991)
larval fish (Johnson and Dropkin, 1995) and abalone (Carefoot et al, 1993).
The differences in activity levels were probably much more pronounced than
that shown in fig. 13, because speed of movement was not taken into account.
Larvae which were moving on the first two days of deprivation tended to do so very
rapidly, while those 'searching' on the fourth to sixth day appeared very sluggish and
were often only moving their head. The reduction in activity may also explain the
reduced feeding capacity after four or six days of deprivation (Fig. 12).
The tendency of larvae to search actively on the first two days after starvation
may be a strategy to lead larvae away from areas of low prey density. Larvae of F.
acariçuga have been suggested to be very sluggish and to not exit the leaflet on
which they are placed as eggs. However, it is clear that larvae at first become very
active when deprived of food.
A switch from intensive, area-concentrated search to dispersal behavior
(increased speed and decreased tuming rate) when food is limited has been
documented in various insects (Bell, 1991). Hunger can increase both the speed of
movement (Dixon and Russel, 1972, Rotheray and Martinat, 1984) and the
percentage of time spent moving (Blommers et al, 1977). In larvae of F. acarisuga,
speed gradually increases and tuming rate gradually decreases after feeding on an
egg of T. urficae, and both begin to stabilize after about 15 minutes (Johnston, 1997).
It appears from this experiment that dispersal behavior rnay continue for 2-3 days in
the absence of prey.
It is difficult to interpret the reason for the decrease in movement with
increasing length of food deprivation. Zeigler (1 985) suggested that the best strategy
for an active predator when starved is to keep searching until death or exhaustion.
However, searching until exhaustion is not Iikely to be an advantageous strategy for
an individual unless the chance of quickly finding food is high, or long-terni survival is
not important, as for an adult. Since an adult's main goal is to reproduce, it can
continue to do so while actively searching for food. For a larva not yet big enough to
become an adult, survival is crucial. To keep searching until exhaustion rnay not be
the best way to maximize the chances of survival because energy reserves will be
exhausted very quickly.
Altematively, the sedentary behavior rnay be a strategy to decrease energy
expenditure. Tanaka and Ito (1 982) suggest that a reduction in activity following
starvation is useful for predators with mobile prey, such as spiders. In this way, the
predator can conserve energy while waiting for mobile prey to corne into the vicinity.
F. acarisuga rnay be slowing down due to a similar strategy; behavior rnay be
determined by the level of energy reserves. During the initial time of high activity the
larva's reserves rnay deplete to a point where, if no food is found, it ceases
movernent. The raised heads displayed by some F. acarisuga larvae could increase
the probability of detecting spider mites under these conditions.
In this experiment, along with a number of others perfonned on F. acarisuga,
the larvae were studied on clean Ieaflets devoid of spider mite damage or webbing,
and within a very limited space. The larvae might behave quite differently if 1) the 3-
dimensional surface of the plant were available, and 2) webbing were present.
Webbing could serve as a cue to keep an individual within a spider mite patch, thus
the dispersal behavior under low prey conditions might be less extensive than has
been observed. Spider mite webbing is known to affect the behavior of predatory
mites such as Ambleyseius bibens, which spent only half as much tirne walking when
webbing was present (Blommers et al, 19ï7). Future studies should investigate the
effects of spider mite webbing on F. acarisuga larval behavior, and the ability of
larvae to locate new spider mite patches on tomato plants under less confined
conditions.
Chapter 4
CONCLUSIONS
My experiments have demonstrated that F. acarisuga larvae can develop to
pupation over a wide range of prey availability, and will respond with variation in total
prey consumption, pupal weight and timing of metamorphosis. When prey density is
consistently low, larvae are able to consume fewer eggs and still reach pupation at a
smaller size. When ternporarily deprived, some larvae can survive up to at least 6
days with zero prey, reaching pupation at an extended developmental time. This
flexibility may be an adaptation to temporal and spatial variability in mite distribution,
and should allow an F. acaisuga population to persist at a greater range of prey
levels in the greenhouse than would be possible if the larvae had a fixed
developmental time and size.
The primary airn of biological control is to keep the pest population at
consistently low Ievels under the economic. According to Huffaker (1 970) there are
two opposing types of mite predators: a) those that are more effective at maintaining
low prey densities and b) those that have higher powers of consumption, good at
quickly suppressing outbreaks but not at rnaintaining low prey densities. Phytoseiid
mites are classed in the first category while most insect predators are assumed to be
in the second. However, it appears that F, acarisuga does have sorne traits which
may enable it to persist at low densities. The ability of F. acarisuga to adjust their
developmental time and pupal weight to the surrounding prey density means that its
overall rate of increase will be slower when less prey are available to each predator,
assuming fecundity is related to pupal weight. This, combined with reduced
consumption levels, may prevent F. acarisuga from overexploiting its prey.
These expenments have also revealed some limitations in the survival ability
of F. acarisuga. Larvae require a minimum of between 5 and 15 mite eggs daily;
below some threshold in this range, they cannot obtain enough nutrition to survive to
pupation. An ample supply of mites is particularly important after the second day of
age, as consumption capacity greatly increases. By comparison, P. persimillis adults
have lower daily prey requirements than F. acarisuga (J. Rogers, pers. com.) and
also require less prey to complete development; both nymphal stages required only
2-3 prey for optimal survival to the ne* stage (Eveleigh and Chant, 1981).
Therefore, P. persimilis may be more effective at continuously low densities than F.
acarisuga. Whether F. acarisuga will be better at responding to outbreaks after
temporary periods of complete deprivation remains to be seen. When completely
deprived of prey, approximately 30% of F. acarisuga larvae are capable of full
recovery to pupation after 6 days. Further studies may be necessary to determine
the importance of this strategy in the field, and whether the survivors are capable of
reaching a viable population size.
If they can survive periods of prey scarcity, the flexible developmental strategy
of F. acarisuga should help it respond quickly to increases in prey density. When
mite densities increase, the larvae will exert greater control by consuming more prey,
reaching a larger size and reaching pupation sooner, enabling the population of
predators to increase rapidly. F. acarisuga larvae are also able to respond to
increased prey density part-way through development. The results of the experiment
in chapter 3 showed that larvae achieved mite consumption levels and pupal weights
based on the surrounding prey density, previous deprivation of 1-6 days having only
minimal effects. This is a beneficial trait, because larvae will be able to efficiently
exploit higher mite densities as they arise, even after prey has been previously
limiting. A short period of time with no prey will have little effect on the final size of F.
acarisuga, if larvae are retumed to an optimal supply of mites.
Under field conditions, the developmental parameters measured in these
experiments will be affected by the searching capacity of latvae. Since larvae will not
be confined to cells, their prey consumption rate, and hence their survival,
developmental tirne and size, will depend on their ability to find prey. The expenment
in chapter 3 gave sorne information on the mobility and dis persal of F. acarisuga
l a ~ a e under conditions where no prey is present. The lanrae were found to have a
low level of activity at the start of each deprivation period, and then to dramatically
increase their activity level over the next two days. This may aid in the location of
new patches. After 3-4 days, larvae generally became sedentary, which may aid
larvae in surviving periods of temporary deprivation. If the patch that a lanrae is in
becomes depleted, larvae that do not locate a new patch of spider mites within 2
days are unlikely to do so. However the sedentary behavior may be adaptive
because spider mites tend to found new colonies on leaves close to the parental
colony (Sabelis and Dicke, 1985). Sedentary larvae on these nearby leaflets have
some chance of controlling new mite patches as they arise.
The ability of F. acarisuga to locate prey patches on tomato plants, both as a
lanra and as an adult, should be investigated in the field. The mobility of F. acarisuga
adults could offset any survival advantage of other predators, because adults rnay be
better at locating rare patches in the greenhouse. In comparison with the adults, the
behavior of the larvae is probably of limited importance to the dispersal of this
predator. However, the behavior of the larvae is important to the survival of F.
acarisuga; in order reach pupation, larvae must obtain a minimum amount of prey. If
the patch they start out in depletes before this amount is obtained, the l a ~ a e will not
reach pupation unless they either locate a new patch, or to survive until the prey
numbers build up again. Unless a predator can survive periods of prey scarcity, it will
not be present to control any newly developed infestations. Additional factors
possibly influencing the performance of F. acarisuga under prey limitation that still
need to be investigated include predator density, abiotic conditions, and the
relationship between fecundity and pupal weight.
Population models should be able to help relate the information known about
F. acarisuga from these experiments and from others, to its performance in the
greenhouse. Ultimately we want to know under what conditions F. acansuga
regulates mite population growth. Such models could be used to determine the ideal
release rates and densities for best control, and to help narrow down important
directions for further experimental work. In addition, they may help explain which
features of the organism of interest are contributing to its control ability, in
corn parison with organisms that lack those features. In future, a comparative
approach may be the best way to determine which combinations of traits are most
important to the outcome of biological control programs, and explain why one agent
outperforms another (Murdoch and Briggs, 1996).
Comparing F. acarisuga with other organisms could shed light on how aspects
of this type of complex life history, with an abrupt shift from the predatory stage to a
dispersai phase, influence biological control. In addition to F. acarisuga, there are
aIso other cecidomyiid predators of mites whose control potential has not been
explored (Bames, 1933), including eight species in the genus Feltiella (Gagne,
1995). There are also cecidornyiid predators of other pests such as psyllids and
aphids (Barnes, 1933), including Aphidoletes aphidomyza, which is also used in B.C.
vegetable greenhouses to control aphids. Some predators in other families, such as
syrphid flies, aIso have a similar life history. Understanding the dynamics of F.
acarisuga and its prey may give insight on the role and potential of a large group of
similar insects.
Table 1. Cornparison of pupation in F. acarisuga lawae reared with four different densities of T: urticae eggs. At the Iowest density of 5 eggs per day, approximately half the larvae went missing and were presumed to have escaped, and none of the remaining larvae reached pupation.
Treatment Missing (No. eggs l a ~ a e
No. larvae remaining reaching
% pupation*
- -
*Does not include missing lawae
Table 2. The means and standard deviations of the daily number of eggs of 7. urticae eaten by lanrae of F. acarisuga during the f irst four days of feeding at three different densities of eggs.
Day 4 Day 3 Day 2 No. eggs
providedlday Day 1
Figure 1 : A diagram of experirnental arenas used to enclose and observe lawae of F. acarisuga. a) petri dish filled with agar b) hole cut out of agar c) plastic cover slip.
Fig 2. Number of F. acarisuga larvae reaching pupation on each day after eclosion, while feeding at three different prey densities. Larvae were reared in agar cells with 60,30, or 15 eggs of T. urticae per day. Symbols V indicate the mean developmental times for each treatment.
a) 60 eggd day
% pupating on day 5 = 87.5 C.V. = 20.3%
b) 30 eggs/ day
% pupating on day 5 = 46.7 C.V. = 17.4%
b) 15 eggsl day
% pupating on day 5 = O C.V. = 36.5%
Developmental Time (days)
Fig 3. Mean number of T: urticae eggs consumed by F. acarisuga during the entire larval period at three different prey densities. Error bars indicate 95% confidence intervals.
140 T !
15 30 60
Number of Eggs Available per Day
Fig. 4. Mean pupal dry weights of E acarisuga after feeding at three different densities of T. urticae eggs. Error bars indicate 95% confidence intervals.
15 30 60
4 Number of Eggs Available per Day
Fig. 5. The relationship between the totaI number of T. urticae eggs consumed by F. acarisuga larvae, and the dry weight of F. acarisuga at pupation. Data from larvae fed at al1 three prey densities are included. The regression equation for the line is Y = 0.21 x - 2.28 (8 = 0.91).
15 eggs per day i 30 eggs per day A 60 eggs per day
1 I 1 I I I I O 20 40 60 80 1 O 0 120 140
Total Number of Eggs Eaten
Fig. 6. The relationship between the developmental tirne of F. acarisuga and the dry weight at pupation. Data frorn larvae provided with three different prey densities are included. Larvae feeding at the highest density had greater variation in pupal weight, whereas those feeciing at the lowest density had greater variation in developmental time.
v 15 eggs per day O 30 eggs per day
60 eggs per day
O 2 4 6 8 1 O 12 14 16 18
Developmental Time (Days)
Fig 7. The mean proportion of lawae of F. acarisuga surviving to pupation after increasing periods of deprivation. Before and after deprivation, larvae were provided daily wiai two different levels of prey density. Error bars indicate the 95% confidence intetvals.
well-fed lawae O poorly-fed larvae
Deprivation Tirne (Days)
Fig 8. The effects of deprivation time and prey availability on the developmental time and survival of F. acarisuga. Vertical bars indicate the number of larvae pupating on each day after hatching. Horizontal bars indicate the total number of larvae surviving to pupation (shaded squares) out of the total number of replicates for each treatment group. Symbols V indicate the mean developmental times for each treatment.
Deprived 1 day
ul c - Ci Deprived 2 days
12 10 I
4 2 O Tw , 1
12 1
5 4 6 8 10 12 14 16 18 4 6 8 10 12 14 16 18 z
Deprived 4 days
4 6 8 10 12 14 16 18 4 6 8 10 12 14 16 18
10 - 8 - 6 - 4 - 2 - 0 -
12 1 O 8 6
4 2
O
rP n 12
12 12
10 10 - 8 - 8
6 6 - 4 4 - 2 2 - O O
Deprived 6 days
m
1 1 I 1
2 10 -
0 8 -
i
- 111 1 I 1 - 1 1
IL'I-..rl
4 6 8 10 12 14 16 18 4 6 8 10 12 14 16 18
12 -
5 6 - 4 - C
O 2 - z fi 0 - I
l L l 1
4 6 8 10 12 14 16 18 4 6 8 10 12 14 16 18 Tirne Since Hatching (Days)
12 10 - 8 - 6 - 4 - 2 - O
10 - 8 - 6 - 4 - 2 - O 1 I 1 1 1 1 1 r
Fig. 9. The relationship between deprivation tirne of F. acarisuga during larval development, and the total number of days taken to reach pupation. Lanrae were placed in cells with either 60 (well-fed) or 15 (poorly-fed) eggs of T. urficae per day before and after the deprivation period. The regression equations are Y = 1.27~ + 6.69, f = 0.68 (poorly-fed) and Y = 1.31~ + 4.74,8 = 0.75 (well-fed).
Deprivation Time (Days)
Fig. 10. The effects of feeding rate and increasing periods of larval starvation on total mite egg consumption of F. acarisuga larvae. Error bars indicate 95% confidence intervals
O poorly-fed larvae
H well-fed larvae n=13
De privation Time (Days)
Fig. II. The effects of feeding rate and increasing periods of larval starvation on dry weight of F. acarisuga pupae. Error bars indicate 95% confidence intewals.
well-fed larvae n=l 1
T
1 2 4
Deprivation Time (Days)
Fig.12, Mean number of eggs eaten by F. acarisuga lanrae on each day after hatching. Larvae were reared in agar cells with 60 eggs of f: urticae per day and stanred for 0,1,2,4, or 6 days. There were significant differences in the number of eggs eaten on the third day of feeding (marked with symbole) among the five treatment groups.
1 2 3 4 5 6 7 8 9 10 11
Day (from hatching) 6 1
Fig. 13. The proportion of larvae of F. acarisuga moving when observed at 24-hour intewals after food deprivation. Only those larvae that eventually recovered to reach pupation were included. Prior to and after the deprivatic period, either 60 (well-fed) or 30 (poorly-fed) eggs of T. urticae per day were availabie ?O each lawa.
Well-fed larvae - + deprived 1 day (n=6) + deprived 2 days (n=13) A deprived 4 days (n=10)
deprived 6 days (n-5)
- -O - - deprived 1 day (n=7) - - CI - - deprived 2 days (n=14) - -A - - deprived 4 days (n=4) - - v - - deprived 6 days (nS)
O 1 2 3 4 5 6
Day of Deprivation
Fig 14. The relationship between the developmental time of F. acarisuga and the dry weight at pupation. Larvae of F. acarisuga were placed in cells with either 60 (well-fed, filled symbols) or 30 (poorly-fed, unfilled symbols) eggs of T, uHicae per day, and after 2 days of feeding were deprived for increasing lengths of time.
A A control (not deprived) v w deprived 1 day o deprived 2 days
deprived 4 days O deprived 6 days
Developmental Tirne (Days)
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