FILE: <bc-21.htm> Pooled References GENERAL INDEX [Navigate
to MAIN MENU ]
DETERMINATION OF PROGENY NUMBER
(Contacts)
---- Please CLICK on desired underlined categories [to search for Subject Matter, depress
Ctrl/F ]:
References
[Please
refer also to Selected Reviews |
|
Overview
Although the sex ratio can ultimately affect the number of progeny in
the next generation, there are many more direct influences on the final count
of offspring, and these shall be treated separately. One should try to
separate the forces at work in determining sex ratio as discussed in the
previous section from those forces determining progeny number directly. Behavioral
and Ecological Phenomena Courtship & Copulation.--Sibmating is common among parasitic Hymenoptera and males
typically emerge as adults before their female siblings, but the timing may
vary among species. Gordh & Evans (1976) reported that Goniozus
aethiops males emerge 1-2 days before female siblings and
copulate with siblings before they emerge from their cocoons. Similar
observations have been made for Goniozus natalensis
Gordh (Conlong et al. 1984). George & Abdurahman (1986) noted that males
of Goniozus keralensis Gordh also emerge a few hours
before females and copulate within female cocoons. Virgin females copulate
after emergence from the cocoon, but inseminated females reject subsequent
copulatory attempts by males. Females of this species will return to the
cocoon during the preovipositional phase of post-emergent life. Similar
behavior has been noted in several other species of Goniozus
(G. Gordh, pers. comm.). Nickels et al. (1950) reported that Goniozus punctaticeps
(Kieffer) females copulate within one hour and three weeks after emergence. Among
pteromalid parasitoids attacking synanthropic Diptera, although males
generally emerge about one day before females, they do not remain in the
vicinity to mate with their sisters, but rather disperse to more distant sites.
Hence, sibmating does not seem to be common among such species (E. F. Legner,
unpub.).
Host Location.--There
have been little comprehensive studies on the modalities used by the female
parasitoid to locate the area in which the host resides. George &
Abdurahmian (1986) indicated that female Goniozus keralensis
are attracted to fecal pellets of the host Lamida moncusialis.
Conlong et al. (1988) reported that Goniozus natalensis
apparently are attracted to frass of the host. Nickels et al. (1950) found that female Goniozus punctaticeps
"cut one or more holes in a cocoon" of the Acrobasis caryae
(Grote) larva before attacking the host. Nickels et al. (1950) reported that Goniozus punctaticeps
(Kieffer) attacked shuckworm larvae feeding inside Phyloxera
galls, but "have difficulty in attacking shuckworm larvae when feeding
inside pecan shucks." Host Attack & Paralysis.--The
site of venom injection and the behavior associated with envenomization
merits comparative study. For example, female Goniozus nephantidis
sting their host 3-4 times at the posterior end of the host's abdomen. In
contrast, Goniozus punctaticeps sting the
shuckworm host larvae on the ventral surface of a thoracic segment as much as
four times prior to oviposition. Many species sting the host in or near the
ventral nerve cord. Thus Goniozus
marasmi stings its host in
the sternal region between the first pair of thoracic legs (Venkatraman &
Chacko 1961a). An early account of host attack is provided by Busck (1917)
who observed Goniozus emigratus attacking Pectinophora gossypiella (Saunders). In this
species the female parasitoid stings the host larva into paralysis by
injecting venom, usually into the region behind the thoracic legs. Sting
behavior of Goniozus triangulifer is noteworthy
because females apparently inject venom into the host several times
subsequent to paralysis. Legaspie et al. (1987) observed venom injected into
the middle and posterior part of the caterpillar and in the ventral portion
of the thoracic region. The response
of the host to attack by the parasitoid can sometimes result in death of the
female parasitoids. This has been observed in Goniozus gordhi
attacking P. gossypiella (Gordh 1976) and G. emigratus attacking the same host species (Busck 1917). Nickels et al. (1950) reported that Goniozus
punctaticeps is often killed
by nut casebearer larvae, but rarely is injured by shuckworm larvae. Factors
which may contribute to parasitoid injury or death may be the size of other
physical features of the ost, the age or physiological condition of the
female parasitoid, and the site of attack or ineffectiveness of the venom
injected by the female parasitoid.
Host Preference.--The female parasitoid can prefer to attack a particular
host species, or she can demonstrate preference for a particular instar, or
she may prefer to attack a host during a particular period during a stadium.
Several species of Goniozus apparently display preference for
larger bodied hosts. This observation was made for Goniozus natalensis
(Conlong et al. 1988). In contrast, Venkatramen & Chackao (1961a,b) found
that Goniozus marasmi preferred medium sized host larvae
while rejecting full-grown larvae. Iwata (1949) reported that Goniozus
japonicus attacks several larval instars of the pyralid Cichocrocis
chlorophanta Butler, but prefers to attack the host during the
quiescent period before ecdysis.
Host Transport.--Movement
of the host from a place of encounter and paralysis to a place of concealment
where oviposition occurs is not well documented in Goniozus,
although annecdotal comments regarding host movement have been reported for
several species this genus. Goniozus gordhi has
been observed with this behavior with paraslyzed hosts (Gordh 1976).
Venkatramen & Chacko (1961a) noted that G. marasmi
transport paralyzed larvae of M. trapezalis. George
& Abdurahmian (1986) reported that G. keralensis
Gordh may move Lamida moncusialis (Walker). Legaspie et
al. (1987) observed similar behavior in G. triangulifer
attacking Cnaphalocrocis medianalis (Guenee).
Circumstantial evidence suggests prey transport may be used by Goniozus
gracilicornis (Kieffer). Evans (1987) reported this species may
move Choristoneura occidentalis Freeman. Other Goniozus
may transport hosts including G.
raptor Evans (Evans 1978).
Incipient prey transport is noted in Bethylus and Epyris.
A distinction should be made between random movement of hosts and hosts transported
from one place to another for the purpose of concealment.
Progeny Defense.--This
kind of behavior is manifested in several ways. George & Abdurahmian
(1986) reported that female Goniozus keralensis destroys
and consumes the eggs of other females when encountered on a parasitized host
with her mandibles, but never destroys her own eggs. Venkatraman &
Chackao (1961a,b) noted that G. marasmi females destroy
the eggs and larvae of conspecific females when a parasitized host larva is
encountered. The female will subsequently oviposit on the host. In response
to cannibalism, predation or both, some female Goniozus will
actively defend a host while parasitoid progeny develop. Conlong et al.
(1984) noted that female G. natalensis remain with their
progeny until they pupate. Antony & Kurian (1960) reported maternal care
for G. nephantidis, and Chaterjee (1941) reported it for
Bethylus distigma. Goniozus triangulifer
females guard hosts from conspecific females. Remarkably when inexperienced
females encounter parasitized hosts, they consume the extant eggs and
frequently oviposit a new complement of eggs. Experienced females usually
reject hosts which have been parasitized (Legaspie et al. 1987). Oviposition Restraint.--Female
Ooencyrtus kuwanai (Howard) can restrain oviposition
and, therefore, distribute eggs in a nonrandom fashion. The retention of eggs
does not last for more than four days initially, which is due to intrinsic
pressure of egg accumulation (Lloyd 1938). The gregarious Nasonia vitripennis
(Walker) is able to fertilize a smaller percentage of the eggs laid at high
parasitoid/host ratios (Wylie 1966). The reduces wastage of both sperm and
immature parasitoids. Sperm wastage was reduced because fewer sperm were used
to produce female offspring. The mortality of female larvae was higher
because starvation affects the female larvae more than the males. The solitary Spalangia
drosophilae Ashmead was restrained from ovipositing on
already-parasitized hosts (Simmonds 1956). This restraint broke down after
three encounters with parasitized hosts. Females adapt their egg laying
according to the number of hosts available. Host / Parasitoid Density.--A
well recognized characteristic of parasitic Hymenoptera whose adults possess
a high inherent fecundity, are long-lived and actively search, is their
ability within a generation to increase progeny production in response to
rising host densities (characterized by decreased ovisorption). Smirnov &
Wladimirow (1934) apparently were the first to demonstrate this response,
using the fly Phormia and the parasitoid Nasonia vitripennis.
Flanders (1935) described the same response for Trichogramma on
Sitotroga eggs. DeBach & Smith (1941a) showed quantitative relations
with Muscidifurax raptor Girault & Sanders
and Nasonia vitripennis on the house fly, Musca
domestica L. Burnett (1951) showed it for Dahlbominus fuscipennis
(Zetterstedt) on Neodiprion sertifer (Geoffroy). Work on Spalangia
drosophilae Ashmead, Spalangia cameroni
Perkins, Spalangia endius Walker and Muscidifurax
spp. pupae showed that the increase was greater in female than in male
progeny. It was suggested that this increase came about through mechanical
and sensory processes (Legner 1967a,
1967b; Legner et al. 1966). Madden &
Pimentel (1965) showed similar data for Nasonia vitripennis
but did not attempt to describe the processes involved. Significant
contributions have been made by Wylie (1965, 1966a,b) concerning the
behavioral mannerisms whereby this acceleration becomes possible. Wylie
(1966b) also offered credible evidence for the greater acceleration in the
female line with Nasonia vitripennis. Burnett
(1951) studied searching in Dahlbominus fuscipennis on
its host Neodiprion sertifer (Geoff.), the European pine
sawfly. In one series of experiments he varied the area of search while
keeping the number of hosts a constant 25. In another series he varied the
number of hosts in a constant area of search, and the number of parasitoids
was kept constant. The results showed that varying host density by changing the area of search or the number of hosts
available did not affect the
relationship between the host density and the number of hosts parasitized nor the number of
eggs laid. At lower host
densities, the rate of increase of the parasitoid was rapid, but at the higher
host densities it tended to level off. In a single parasitoid generation the
relation between parasitism and host density approximated the curve: y = a + blnx,
where y = No. hosts attacked
or No. parasitoid eggs laid, lnx
= natural logarithm of host density, and a & b are
constants. Salt (1937)
examined the relation between parasitoid density and effective rate of
reproduction of Trichogramma evanescens West. As the
density of parasitoids in a fixed population of hosts was increased, there
was an increase in superparasitism. The number of parasitoid progeny reached
a maximum and then decreased. It was concluded that the parasitoid regulates
the number of eggs per host according to the amount of food available. DeBach &
Smith (1947) studied the effects of variation in the density of the
parasitoid Nasonia vitripennis on the rate of change of
populations of the parasitoid itself and of populations of a laboratory host Musca
domestica. They concluded that the higher the parasitoid density
in relation to that of the host, the greater, up to a certain point, was the
total increase of the parasitoid population. Above this point there may be a
decrease in total parasitoid progeny because of competition and overlapping
in the search for hosts and because of superparasitism. Utida (1950,
1953, 1957) examined the effect of parasitoid density on the interaction of a
bean weevil, Callosobruchus frinensis (L.) and its
parasitoid Neocatolaccus mameyophagus Ishii &
Nayasawa. There was an increase observed in parasitoid progeny with increase
in parasitoid density. Beyond a certain high density the number of parasitoid
progeny remained constant. Burnett
(1953) working again with the D. fuscipennis and N.
sertifer combination, varied parasitoid number from two to 24,
while the host number was kept constant. At lower parasitoid densities the
rate of increase in hosts parasitized varied approximately inversely as the
parasitoid density. AT the higher parasitoid densities the rate was more or
less constant. At lower parasitoid densities the number of parasitoid eggs
laid tended to vary as the square-root of parasitoid density. At the higher
densities the relationship was almost linear. With an increase in parasitoid
density, the number of eggs per parasitized host increased slightly and the
oviposition rate per female parasitoid decreased. In a later
study (Burnett 1956) close agreement was obtained between laboratory and
field experiments using D. fuscipennis on N.
sertifer. The number of hosts parasitized and the number of
parasitoid eggs deposited increased rapidly with an initial increase in the
number of parasitoids released in the field. With further increases in
parasitoids, parasitism increased more slowly. There was an increase in
superparasitism with an increase in the number of parasitoids released. There
was an optimum density of adult parasitoids for maximum parasitism by the
average female parasitoid. In 1958
Burnett allowed a constant number of Encarsia formosa
females to search for increasing numbers of greenhouse whitefly hosts.
Parasitization decreased as the searching area increased. In any fixed
searching area, the parasitoids found increasing numbers of hosts as host
density was increased. Harry S. Smith (1939) stated that,
"...at a given average density, and providing the entomophagous insect
originates within the area of heavy infestation, the actual distance which it
must travel to find a succession of hosts is less where the individuals are
closely grouped than where they are uniformly separated. For this reason,
within certain limits, the more the host dispersion tends towards the colonial type, the more effective an
enemy of given powers of discovery is in maintaining its average density at a
low value." Smith considered Rodolia cardinalis
(Muls.) successful on cottony-cushion scale, and another coccinelid, Rhizobius
ventralis Erichson, as a failure on black scale. Burnett
(1958b) testing Smith's hypothesis, used white flies and Encarsia formosa.
He kept the area of search and number of parasitoids constant, but modified
the patterns in which the
parasitoids were exposed: ________
_______ _______ | .
. . | | | |...
... | | . . . . . | | ..... | |.. ..
| | .
. . . |
| ..... | | | | . . .
. | | ..... | | | | .
. . . |
| ..... | |
... .. | | . . . . . . | | | | .. ... | | | | | | | dispersed center corner Results
showed that parasitoid efficiency was increased by cololonial host
distributions; and attack rate was increased with increased number of hosts.
Burnett thought that a colonial distribution was merely more easily found. When the
parasitoid numbers were increased, the parasitoids found hosts in proportion
to the natural logarithm of parasitoid density. The increasing number of
parasitoids nullified the effect of host distribution because they saturated
the environment. The initial
ratio of parasitoids/hosts is important in determining the interaction
between the species in subsequent periods of time (Burnett 1960). Legner (1967b) reporting on the behavior of several ectophagous
pteromalids, suggested that two behavioral changes might account for
increased rates of attack at higher host densities: (1) parasitoids spend
less time examining puparia before ovipositing and (2) they lay more eggs in
the same time period at a high host density than at a low. Superparasitism
and differential sex mortality were also thought to be greater at lower
densities. Studies with Spalangia
drosophilae Ashmead showed that mixed groups of linear
and clumped host distributions
caused parasitoid behavioral changes, which resulted in, reduced progeny
production compared to a single
distribution alone (Legner 1969b). Continual observations of searching females showed that the
all clumped distribution
elicited the greatest overall initial attraction for hosts but stimulated
subsequent accelerated movements to other areas. It was concluded that maximum host destruction resulted
when completely random behavior
was involved. A recognition of this, however, required a knowledge of
behavior, host condition and progeny production (Legner 1969b). This study furnished proof that predictions of field
performance of exotic introduced natural enemies would require an infinite number of experiments! When a
parasitoid species reproduces generation after generation in a constantly
favorable environment, it attains its greatest seasonal abundance when it is not host regulative (Flanders 1963,
1968). Under such conditions the number of adult female parasitoids per adult
female host is minimum. When
the parasitoid Venturia regulates its host Anagasta
at very low densities and is the only significant host mortality factor, the
female parasitoid/female host ratio was about 20/1 in Flanders' experiments.
For balance of the system, 20 female parasitoids are needed to find and
destroy all but two of the larval progeny of an Anagasta.
Temperature.--Temperature influences the efficiency of host
parasitization and oviposition. Low temperatures lower the oviposition
capacity of Neodiprion sertifer and also act in conjunction
with host density to reduce the number of hosts contacted by the parasitoid
(Burnett 1951).
Investigations on the effects of temperature on the population ecology
of a whitefly, Trialeurodes vaporariorum, and its
internal chalcid parasitoid Encarsia formosa, were
conducted in a greenhouse at 18°, 24° and 27°C (Burnett 1949). The greatest
influence of temperature resulted from its differential effect on the
fecundity and rate of development of the host and parasitoid. At 18°C, the
whitefly had a fecundity of 319 eggs/female, while the parasitoid had
30/female. Rate of development was the same for both host and parasitoid.
However, at 27°C, the fecundity of the whitefly was equal to the parasitoid,
while the ratio of development of the parasitoid was nearly double that of
the host. Therefore, greenhouse temperatures had to be kept above 24°C for
parasitic control of whiteflies. Work on the
European pine sawfly and its parasitoid Dahlbominus fuscipennis
(Zett.) showed that an increase in temperature combined with increased host
density caused a greater percentage of parasitoids to emerge in a single
parasitoid generation (Burnett 1951). This illustrated the importance of
optimum temperature in maximum host destruction. Parallel results were shown
in a field experiment with these species (Burnett 1956). As temperature
increased, the number of hosts parasitized increased as did the number of
eggs laid. This work is probably the first case where laboratory predictions of field
results have proven feasible. Additional
greenhouse studies showed that there is a rapid increase in the percent
parasitism of the immature forms of the greenhouse whitefly by its parasitoid
Encarsia formosa as the season progresses from January
to March (Burnett 1953). With an increase in temperature in the greenhouse,
the efficiency of the parasitoid increases and the percent parasitism rises.
Towards the end of February radiation from the sun is more intense, and the
first and second larval instars of the host that are exposed to it are
killed. Thus, the parasitoid population is increasing at this time while the
host population is decreasing. Consequently, there are more parasitoids
searching for fewer hosts, and the number of hosts attacked increases rapidly
until host density is markedly reduced.
Host Size.--Nasonia
vitripennis can judge the size of the host and adjust the number
of eggs accordingly (Edwards 1954). The larger the host the more eggs laid
per host individual in this gregarious parasitoid. Dahlbominus fuliginosus
definitely favors parasitizing hosts in large cocoons. In fact, this species'
total fecundity was about one-third greater on large cocoons than on small
ones. Trichogramma spp. tend
to avoid ovipositing in hosts smaller than their own body size (S. E.
Flanders, pers. commun.). A
characteristic average size for ectophagous parasitoids was manifested in
several species attacking Hippelates
and Musca (Legner 1969a ). Also, when
ectophagous species oviposited on small hosts at high host densities,
emergence of their progeny was hastened, an effect not markedly evident in
the endophagous species studied (Legner 1969a ). A significant
theoretical effect on the regulation of fly hosts is indicated because small
hosts are usually indicative of exploding population densities. Parasitoids
being able to respond to such indicators can regulate their hosts.
Humidity.--Humidity influences the oviposition rate of Macrocentrus ancylivorus (Martin 1946,
Martin & Finney 1946). It has a more pronounced ecological effect than
physiological effect in that oviposition rate is affected. Higher humidities
generally promote longer adult longevities (Legner & Gerling 1967, Olton & Legner 1974 ). Adult Parasitoid Food.--Apanteles medicaginis Muesebeck has a higher fecundity and a greater
longevity in areas where natural adult food is abundant. In such areas there
was a higher parasitism of the host Colias
eurytheme Boisduval (Allen
& Smith 1958). Tiphia matura Allen & Jaynes lacks
effectiveness because it is limited by its adult food habits to areas smaller
than those occupied by its host, the Japanese beetle (Clausen et al. 1933). Edwards
(1954) demonstrated that host-feeding by Nasonia
vitripennis increased its
fecundity by allowing for a more rapid maturation of ovarian eggs. Wäckers & van Rijn (2005)
noted that parasitoids and predators also require plant-derived foods as a
source of nutrients. This vegetarian side of the menu may include various
plant substrates, such as pollen, or nectar and other sugar sources (e.g.
fruits, and honeydew. Plant-provided
foods can have a dramatic impact on longevity, fecundity, and distribution of
predators and parasitoids. As each of these parameters affects the local
number of carnivores, the availability of suitable plant-derived food can
have a major impact on mass-rearing programs, as well as on
herbivore-carnivore dynamics in the field. The level in which predators or
parasitoids depend on primary consumption varies. Wackers & van Rijn
(2005) distinguish between ‘life-history omnivory’, ‘temporal omnivory’ and
‘permanent omnivory’. Life history omnivores include those natural enemies
that are strictly dependent on plant-derived food during part of their life
cycle, such as hoverflies and many parasitoids. Temporal and permanent
omnivores supplement their carnivorous diet during part of their life (e.g.
host-feeding parasitoids) and throughout their lifecycle (e.g. predatory
mites and ladybird beetles, respectively. Parasitoids emerge with a limited
supply of energy. At emergence, their energy reserves often cover no more
than 48 hours of the parasitoid’s energetic requirements. Sugar feeding can
increase a parasitoid’s lifespan considerably; up to 20-fold under laboratory
conditions (Jervis et al. 1996, Wackers 2001). This means that parasitoids that fail to replenish their
energy reserves through sugar feeding will suffer severe fitness
consequences. Sugar feeding can benefit a parasitoid's fecundity, not only
through an increase in reproductive lifespan, but also through a positive
effect on the rate of egg maturation (Jervis et al. 1996). Life history omnivores with a
predatory larval phase (such as lacewings, gall midges, wasps and ants) use
nectar as energy source in their adult phase as well, increasing their
reproductive lifespan or their foraging range. Some of these life history
omnivores also feed on pollen. In hoverflies and certain lacewings, this
protein-rich substance appears to be essential to maintain egg production. Permanent omnivores (such as
anthocorid bugs, ladybeetles, and predatory mites) often use both prey and
plant provided food (pollen and nectar) for survival and reproduction. This
diet expansion allows them to extend the seasonal period of performance. The fact that fitness of adult
biological control agents can be dramatically enhanced through the simple
provision of food supplements has been long engrained in mass rearing
practice. To facilitate rearing, adult insects are commonly provided with
pollen or sugar sources such as (diluted) honey, honeydew, sugar water or
fruits. The actual choice of the supplementary food source is usually based
on criteria like convenience (availability, shelf-life), economy (cost) or
compatibility with existing rearing methods. The relative suitability of food
sources for the predator or parasitoid has received little attention. Those
studies that have investigated food suitability show that substantial
differences exist among different types of pollen (van Rijn & Tanigoshi
1999), as well as nectar and honeydew with regard to their chemical
composition and nutritional value (Wackers 2000, Lee et al. 2004). Given this
variation, the issue of food suitability should receive more attention. Wäckers & van Rijn (2005) noted that biological pest
control workers have regularly suspected that the absence of pollen and/or
sugar sources in agriculture could impose a serious constraint on the effectiveness
of natural enemies in the field (Illingworth 1921, Hocking 1966). Hocking (1966) pointed out that lack of
food availability could also prevent introduced parasitoids from establishing
in classical biological control programs. We still have little data on the
nutritional status of natural enemies under field conditions (Casas et al.
2003, Lee & Heimpel 2003).
However, recent studies indicate that natural enemies can indeed be
food deprived in the absence of flowering vegetation (Wackers & Steppuhn
2003). Thus, adding food sources to agro-ecosystems could be a simple and
effective way to enhance the effectiveness of biological control programs.
Three types of approaches have been proposed to alleviate the shortage of
food in agricultural systems. Food sources can be provided by
enhancing plant diversity in agro-ecosystems, either through the use of
non-crops in undergrowth or field margins (van Emden 1965, Altieri &
Whitcomb 1979), or through mixed cropping with crops featuring flowers or
extra floral nectaries. However, not all plant-provided food is suitable as a
food sources for parasitoids and predators. Flowers may not be perceived by
(some) natural enemies, or can be unattractive or even be repellent (Wackers
2004). Other flowers may be
attractive, but hide their pollination rewards within constricted floral
structures that prevent those natural enemies with unspecialized mouthparts
to exploit these food sources. In more diverse systems there might be a
further snake in the grass. Many herbivores are dedicated flower feeders as
well. This drawback can be avoided by selecting flowers that cater for
biological control agents, while being unsuitable for herbivores (Baggen et
al. 1999, Wackers 1999). An alternative to the use of
(flowering) plants is the use of artificial food supplements such as food
sprays (Hagen 1986). Food sprays
typically consist of a carbohydrate solution in combination with a source of
protein/amino acids. Insects that utilize honeydew as food source may be especially
adapted to exploit this ‘artificial honeydew’. Many studies have identified
short term increases in numbers of natural enemies such as parasitoids, lady
beetles, lacewings, and predatory bugs as a result of food sprays, although
impacts on pest numbers have rarely been investigated (Rogers & Potter
2004). The fact that nutritional requirements of natural enemies often differ
considerably from those of pest insects can be used to develop selective food
sprays, i.e. food sprays that sustain biological control agents without
providing a nutritional benefit to the pest insect (Wackers 2001, Romeis
& Wackers 2002). Some crops produce suitable food
supplements themselves. Many crops flower during part of their growing
period. In crops grown for their seeds or fruits (e.g. cereals, citrus,
beans) this flowering period may coincide with the period that the plant is
specifically vulnerable for herbivore attacks. Some crops, such as peppers
and tomatoes, even flower during a large part of the growing season, thereby
maintaining populations of predatory mites and anthocorid bugs, that can
effectively suppress thrips pests (van den Meiracker & Ramakers 1991). Other crops provide nectar also
outside the flowering period. These so-called ‘extra floral nectaries’ may be
found on leaves, stems or fruits. By producing extra floral nectar, plants
attract carnivores in order to obtain their protective services (Turlings
& Wackers 2004). Extra floral
nectaries have evolved independently numerous times. This shows that during
evolution, food supplements have proven to be a successful method to enhance
biological control. The extra floral nectar trait is also found in a number
of crops and can be a useful element in biological pest control. Examples of
extra floral nectar producing crops include Prunus spp. (cherry, plum, peach, almond), cassava, faba bean,
zucchini, pumpkin, cashew and cotton
(Wäckers & van Rijn 2005). The crop-produced nectar may
suffice as food sources for predators and parasitoids. In other cases, there
may be room for plant breeding to improve the timing, quantity and quality of
nectar production, to better match the nutritional needs of biological
control agents (Wäckers & van
Rijn 2005). Larval Competition.--It is well known that competition among parasitoid larvae
can influence the progeny number. Parasitoids are unique in that they are
often able to lay their eggs in such a way so as to deliberately avoid such
competition (Salt 1961). Lloyd (1940) first demonstrated avoidance of
already-parasitized hosts. When superparasitism does occur, the excess eggs
or larvae die. Gregarious parasitoids can discriminate the volume of the
host, avoiding some competition. A good many
parasitic Hymenoptera, but not all, are able to recognize hosts that have
already been parasitized, although their ability may be imperfect or only
temporary (Salt 1961). Under some conditions they are able to restrain
themselves from laying additional eggs in those hosts. Under other
conditions, principally when healthy hosts are scarce, their restraint may
break down, and they then lay eggs in hosts that are already parasitized.
Therefore, for lack of or by failure of the discriminative ability, or by
breakdown of restraint, superparasitism occurs. More parasitoid progeny find
themselves in or on a host than can develop on its tissues. When this happens
competition takes place. Tables 1a-1e (CLICK to view) present an updated account of examples where natural enemies
compete e or tend to avoid competition. There are usually four modes of
competition: (1) deliberate physical attack, (2) physiological suppression,
(3) accidental injury and (4) selective starvation. Supernumerary
larvae of gregarious parasitoids are not necessarily eliminated at an early
stage as they are among solitary species. Often final instar larvae are found
dead. Shortage of food leading to the death of the weaker competitors has
usually been implied, and the fact that dwarf individuals often emerge when
there has been severe competition supports this idea. Starvation is not the
only factor because suffocation has been shown to be operative in some
examples. There are no direct observations of deliberate physical attack on each other by gregarious
external parasitoids. In Nasonia
vitripennis, the female not
fertilizing her eggs under conditions where superparasitism is possible can
eliminate larval competition. Resultant male larvae are better able to
compete under crowded conditions than would females (Wylie 1966b).
Superparasitism can also create just enough food shortage to reduce the
survival and size of adult Nasonia
(Wylie 1965a). The percentage of females in the adult progeny can also be
reduced, but there appears to be no effect on rate of development, ability to
emerge or in the incidence of diapause. A genetical
approach to reducing the problems of superparasitism in entomophage culture,
which involved breeding, was presented by Wajnberg & Pizzol (1989) and
Wajnberg et al. (1989).
Ant Activity.--Homopterous
agricultural pests are known to become exceptionally abundant when the
reproductivity of their natural enemies is markedly depressed by attending Argentine
ants (Flanders 1943). The presence of ants retards the parasitization
activity of Metaphycus luteolus, Metaphycus helvolus
and Coccophagus gurneyi. Parasitization
activity is enhanced in the presence of ants with some species, however
(e.g., Coccophagus rusti, Coccophagus capensis,
Coccophagus scutellaris and Metaphycus stanleyi (Flanders 1943, 1958). Additional effects of ants
on parasitism and predation have also been reported (Bartlett 1961, Pontin
1958, Stary 1966).
Learning.--Learning implies a genetical flexibility which if channeled
could significantly benefit biological control programs. Several studies have
suggested that adult parasitoids are capable of learning (Alloway 1972).
Taylor (1974) explored stochastic models in Nemeritis canescens
and suggested that learning potentially stabilizes the dynamics of
host-parasitoid systems. Legner (unpub. data) has observed a gradual increase
in wariness for escape, among adult parasitoid Muscidifurax and Spalangia
species that were confined in small screened cages. After one week of daily
exchanges of host puparia, the parasitoids had become better adept at
escaping during the transfer process. Physiological Phenomena Nutritional (Host-feeding).--Female parasitoids sometimes consume the body fluids or
tissue of an organism which could, based on host records or observation,
serve as a shost for that female's progeny. Distinctions have not always been
made between female parasitoids feeding upon a potential host and female parasitoids
feeding and then ovipositing upon a potential host. The phenomenon of host
feeding is commonly encountered within parasitic Hymenoptera. Host-feeding
was first observed by Paul Marchal (1905) in Tetrastichus sp. The ovipositor was found to be used more
often for host-feeding than for oviposition. Doten (1911) considered host
feeding important not only for prolonging the life of the female but also to
supply protein needed for oogenesis. The newly
emerged synovigenic hymenopteran female may not have ripe eggs in her
ovaries. Paul DeBach believed that newly emerged Nasonia vitripennis
females have ripe eggs in the ovaries but will not oviposit until after host
feeding (Moursi 1946). Aphytis spp. will oviposit immediately
on emergence, but if withdrawn from hosts in middle age, host feeding is
required for additional oviposition thereafter. Newly emerged Metaphycus
helvolus and Tetrastichus sp. do not contain ripe
eggs, but oviposition often occurs before host feeding (Flanders 1936). Host-feeding is an indicator that oogenesis is in
process. When host-feeding stops, oogenesis has ceased (Flanders 1935).
Host-feeding is unknown in certain species altogether. Included are
proovigenic species, synovigenic parasitoids of mealybugs, some species in
which males and females differ in their host relations and species where
yolk-deficient eggs are stored in the oviducts which require immersion in the
body fluids of the host in order to nourish embryonic development. The close
association of host feeding and oviposition in many kinds of parasitic
Hymenoptera probably indicates that the habit of ovipositing in other insects
evolved from the adults' host-feeding habits. Adult predaceous habits preceded
parasitic oviposition. Host feeding
has its direct effects on the host, of course. Such species as Tetrastichus
asparagi Crawford kill a
significant number of hosts by feeding directly on the, and this is
believed to be as important in checking the host as parasitic development, if
not more so (Johnston 1915). However, the young stages of the aphid Myzus
persicae Sulzer, are killed along with parasitoid eggs they
contain, and therefore host-feeding appears to defeat the primary purpose of parasitism
(Hartley 1922). DeBach (1943) observed that the proportion of
parasitoid-containing hosts destroyed by predatism increased with the
increase in number of adult parasitoids, so that the production of adults
tends to level off instead of increase. The effects
of host-feeding in host regulation
have been considered by Flanders (1953). At low population density it is more
effective to have the mortality result from parasitism rather than predation.
Under such conditions the protein requirement of the parasitoid are at a
minimum. The eggs produced by a parasitoid, but not deposited, are absorbed
and the egg material is used to prolong life (Flanders 1950, 1953). Higher
minimum host population densities are needed to maintain the existence of host-feeding
species than are needed by non host-feeding species. Nevertheless, the
host-feeding habit of adult parasitoids appears to be of value in the
reduction of heavy host populations; and it might also be advantageous in
periodic inundative releases. Host feeding
must be distinguished from malaxation, where the integument is not actually penetrated.
Several lines of circumstantial evidence suggest that malaxation occurs
frequently and host feeding does not occur or is far more limited than suggested
in the entomological literature. First, virtually all records imply that
feeding precedes oviposition. So called "feeding" has not been
reported in any species following oviposition. Another line of reason
involves observations on Goniozus emigratus. Host
feeding was not mentioned by Busck (1917) in his report on this species,
although the parasitoid malaxates its host (Gordh & Hawkins 1981). Goniozus
triangulifer also malaxates but does not host feed (Legaspie et
al. 1987). The host feeding
habit in adult parasitic Hymenoptera was reviewed by Bartlett (1964). He
concluded several interesting facts pertaining to the habit. He reasoned that
the widespread occurrence of the predatory habit among adults of 20 families
of the Hymenoptera gives very little evidence of the evolutionary pathways
through which adult parasitoid predatism might have developed. In the
primitive Tenthredenoidea, e.g., the adults of certain species are known to
masticate and consume the entire body contents of their hosts (Rohwer 19l3).
In Ichneumonoidea adult predatism is commonly encountered in the form of
-host-feeding in both the Ichneumonidae and Braconidae. The habit appears
more universally among the Ichneumonidae than in any other family, with the
adult of some species completely consuming their hosts. In the
Chalcidoidea the host-feeding habit is very frequently encountered in the
Pteromalidae and in the eulophid subfamilies Aphelininae and Tetrastichinae.
Host feeding is almost the rule in a number of pteromalid genera, and in the
eulophid genera Tetrastichus and Aphytis. It is
prominent in certain encyrtids such as Metaphycus and Microterys,
but is conspicuously absent in several species of these genera, even among
those known to have continuous ovulation (e.g., Metaphycus lounsburyi
and Metaphycus stanleyi). The habit appears sporadically
among species of the Eupelmidae, Eurytomidae and Spalangiidae, and has been
reported infrequently in the Trichogrammatidae. In the
Cynipoidea the habit of adult predatism is poorly represented, the closest
approximation to the habit being found among certain of the parasitic
Figitinae which feed as adults on decaying animal matter inhabited by their
carnivorous hosts. In the
Bethyloidea host-feeding is of general occurrence among many of the
Bethylidae where there is complete dependence for sustenance and reproductive
nutrients on the habit by the adults of certain species. The phenomenon has
been claimed to occur in the genus Goniozus
where it can represent a significant mortality factor (Jayaratnam 1941a).
However, Dr. G. Gordh has not observed host feeding by any Goniozus, and believes that
many records are erroneous. Females of this genus do malaxate their hosts (Gordh 1976, Gordh & Evans 1976, Gordh
& Hawkins 1981, Gordh et al. 1983, Gordh & Medved 1986).
Superficially the behaviors involved are similar with the female chewing or
kneading the integument with her mandibles. However, females which malaxate
do not penetrate the integument and do not feed on haemolymph. Some species
which malaxate their hosts apparently induce wounds which become necrotic,
thereby underscoring the erroneous conclusion that host feeding has occurred.
In the
Scolioidea adults of some species of the Tiphiidae chew the bodies of their
hosts to obtain fluids; and some mutillids take body fluids from their hosts.
Feeding upon body fluids and tissues of arthropods is, of course, general
among the Formicidae. In Sphecoidea
adult predatism occurs commonly in Sphecidae and Dryinidae and is
occasionally found in Ampulicidae. In Vespoidea there is general feeding on
insects by adults in Vespidae and some species of the Thynnidae. In
Serphoidea adult predatism has been noted only in Scelionidae. Generally
speaking, although a few cases are known where specific stages of certain
hosts are preferred, there usually is less specificity shown in host-feeding
than in ovipositional attack. Host-feeding tendencies probably developed in
individuals coincident with ovigenesis depletion. For example, Microterys flavus (Howard) host feeds only after its day's supply of
eggs is laid. The quantity
of hosts destroyed by feeding varies with host size, parasitoid age and
parasitoid species. Microterys
flavus feeds on host species
that are unsuitable for parasitization and could, therefore, effect some
control on them. Enzymatic yeast and soy hydrolyzates as food supplements to
a honey diet satisfies the reproductive nutrient deficiency of parasitoids
equally as well as does host-feeding in most cases. Host-feeding
by parasitoids such as Aphytis
is often associated with the host-mutilation
habit to the detriment of parasitoid reproduction, with occasionally
even associated species being affected (Flanders 1951a). In this way pupae of
Aspidiotiphaga, Comperiella, Coccophagoides, etc. have been
destroyed by Aphytis in what
is known as a stilleto effect. The mass culture of Aphytis on California red scale
has shown the following: First-instar scale = ca. 75% killed by mutilation. Second-instar = ca. 50% killed by mutilation Third-instar (early) = ca. 25% killed by mutilation Sometimes
mutilation has been referred to as frustrated host-feeding when the host did not bleed freely.
It has been suggested that host-feeding tends to defeat the primary purpose
of parasitism: the regulation of host densities, by destroying hosts
inhabited by parasitoid young (Flanders 1953b, Hartley 1922). Parasitic
Hymenoptera do not have to host-feed to obtain amino acids, which are found
in honeydew or on plant nectaries (Zoebelein 1956a,b, 1957). Host-feeding
has a pronounced effect on
oogenesis-ovisorption. Nasonia
vitripennis females that
were fed on glucose possessed only 4-5 well-developed eggs in the ovaries
after 12 days, while those fed on host blood had ovaries bulging with eggs
(Roubaud 1917). When deprived of hosts many parasitic Hymenoptera resorb the
mature eggs present in their ovaries. Flanders (1935b) counted all the resorbed eggs in female Metaphycus helvolus by means of their aeroscopic plates, which was
the first quantitative work of its kind. Grosch (1950) also counted the
number of eggs in the ovaries of Habrobracon
juglandis (Ashmead) at
various stages of starvation and noted fewer eggs as starvation progressed. Using the
foregoing observations as a basis, Edwards (1954) treated Nasonia vitripennis females in three ways: (1) starved, (2) fed on
honey and (3) fed on host blood. When starved
the parasitoids died in five days. Rapid resorption occurred and at death
there were only three eggs in the ovaries. When fed on honey the ovaries contained 22 eggs after two days, then
a slow cycle of maturation and resorption began so that for 16 days their
condition did not change. After 16 days resorption was more rapid and by 28
days there were only one or two mature eggs. When fed on host blood the eggs matured rapidly. After five days the
ovaries contained 40 mature eggs even though 260 had been deposited.
Parasitoids which were then starved, resorbed eggs very rapidly and died in
48 hours, but those fed on honey lived for at least eight days and rapid
resorption did not occur. In an
experiment with Spalangia cameroni Perkins (Gerling &
Legner 1968) parasitoids
were treated in three ways also: (1) fed on honey only with no hosts, (2) fed
on honey and hosts continuously and (3) fed on honey and hosts for 24 hours
followed by separation for two days from hosts and then repeating the regime.
In the first case with honey only,
the 3-4 eggs per ovariole retained their compact arrangement for 10 days,
then resorption at the caudal end of the ovarioles began. Females died before
all ripe eggs could be resorbed. In the second case with honey and host fluids, females
deposited one or more eggs on the first hosts encountered, then host-fed. The
host-feeding triggered further development of immature oocytes. Finally,
where host fluids were offered for 24
hours followed by honey only for two days and then hosts again,
ovisorption began abruptly, and oocyte development stopped, apparently at the
stages of development which they had reached while the female was with hosts.
A continuation of oocyte development was not thought to be due entirely to
host-feeding because feeding on host body fluids alone or yeast hydrolyzate
did not produce a resumption of development. A combination of actual oviposition plus host-feeding did produce
continued development (Gerling & Legner 1968). There are
still other effects of host-feeding on the performance of parasitic
Hymenoptera. Host-feeding may be a handicap
to parasitoids whose hosts produce honeydew that attracts ants. The ant
activity may interfere with host-feeding and hinder optimum oogenesis
(Flanders 1951b). This is because the process of host-feeding requires a
longer time than oviposition. Withholding food from some pteromalids and from
Signiphora results in a decrease
in the longevity and average fecundity of the females. Intermediate results
are obtained with partial food (honey) (Legner & Gerling 1967, Quezada 1967). Quezada thought that host-feeding would not occur
after five days of starvation, by which time exhaustion of all mature eggs
through ovisorption had occurred and the germarium was no longer able to form
new eggs due to the lack of needed protein which is normally obtained from
the host body fluids (Signiphora
reproduces by thelytoky). Opposite results were obtained with the pteromalid Muscidifurax uniraptor also reproducing by
thelytoky, as previously mentioned (Legner & Gerling 1967). Temperature.--Lund (1934) observed that the product of time required for
development and effective temperature is a constant in parasitic Hymenoptera.
This work involved two races of Trichogramma
minutum, and actually
related Krogh's
hyperbola to temperature responses. A linear relationship existed
between developmental time and temperature for Trichogramma within the 20-30°C range. In Trichogramma evanescens, adult longevity was
increased with temperature in the optimum range of 24-30°C (Lund 1938). There is a gradual
increase in mortality of the different stages of Nasonia at increased periods of low temperature exposed
(Moursi 1946). However, van Steenburgh (1934) showed results with Trichogramma pupae in host eggs
stored at 35-45°F for 75 days where there was little mortality but about 50%
reduction in fecundity. Schread &
Garman (1934) concluded with work on Trichogramma
that mortality was gradual below 47°F and increased with the length of
exposure. DeBach (1943)
working with Nasonia vitripennis, showed that
storing larvae at different low temperatures slowed down their development,
but dramatically increased the fecundity of surviving adults. Similarly,
three species of parasitoids, Muscidifurax
raptor, Muscidifurax zaraptor
and Spalangia endius attacking the common
house fly Musca domestica, also showed
increased reproductive potential, longevity and fecundity and/or produced
progeny with a total greater biomass when the developing larvae were stored
at 10°C for 55 and 180 days (Legner 1976). The fat cells in
adults of Tetrastichus
stored at low temperatures for two weeks as pupae were scarce as compared to
unrefrigerated ones (Flanders 1938); and there was a lowered fecundity and
longevity observed in Trichogramma
when immature stages were reared at high temperatures (above 85°F) (Bowen
& Stern 1966). Humidity.--Larval mortality in Trichogramma
during cold storage appears to be due primarily to desiccation of the host
egg (van Steenburgh 1934). Mortality apparently varies more with humidity
than with temperature (Lund 1934). Selective Breeding.--The
average number of offspring of Microplectron
fuscipennis Zett. was
increased from 48 to 68 by selection of the most productive mothers. This was
partly due to a decrease in the number of sterile females and by extending
the mean length of life (Wilkes 1942. 1947). Eight to 10 generations were
required to get the desired effect, and larval mortality was also reduced in
the process.
Horogenes molestae (Uchida) was successfully bred on the potato tuberworm, Phthorimaea operculella (Zeller), through
selective breeding. It was formerly unable to reproduce on tuberworm (Allen
1954). The parasitoid was slated for another field host and convenience of
tuberworm rearing was desired. Hybridization techniques may be useful in increasing the fecundity of parasitic
insects (Legner 1972, 1988c, 1989a). However,
crosses should probably be restricted to strains from similar climatic zones
because negative heterosis could result as observed in a cross between a
temperate zone species with its strain from the tropics (Legner 1972).
Mating.--A high percentage of nonhatching eggs is often observed in
the ectoparasitoid Melittobia
chalybii, in which close
breeding is normal. In unmated females the percentages of eggs that do not
hatch is much greater because mating is a prerequisite of normal oviposition.
Females mated with males of a different species also oviposit normally
(Schmieder 1938). The low hatch probably results from an abnormally high
number of partially absorbed eggs being deposited in the absence of mating. Old males of Dahlbominus fuliginosus are not as
successful in insemination; and females that were inseminated by them
produced fewer female progeny (Wilkes 1963). In species of
Microbracon and Trichogramma the female may be
less fecund after mating, possibly because she exercises greater
discrimination in host selection with the consequent greater amount of
ovisorption. In species of
Hymenoptera not characterized by polymorphic females, oviposition occurs as
readily before mating as afterwards. Sex ratios in these species is
determined partly by the amount of oviposition prior to mating. In Aphelinids
where oviposition instincts are permanently changed by the act of mating,
male production is obligatory before mating, facultative after mating. In
polyembryonic species fertilized eggs give rise to twice as many embryos as
unfertilized eggs. In uniparental species the unfertilized eggs are usually
female. However, such eggs are usually destroyed by fertilization because the
resultant triploids are lethal (Flanders 1956 on Encyrtus fuliginosus).
In thelytokous Muscidifurax uniraptor Kogan & Legner
random mating with adventitious males resulted in a general lower survival
and progeny production, but was accompanied by a rise in the sex ratio to ca.
50% females by the F6 generation (Legner 1988d). The interinvolvement of microorganismal extranuclear
factors was considered. Mating has a
profound and irreversible effect on behavior in the pteromalid Muscidifurax raptorellus Kogan & Legner.
In this species heritable traits for fecundity and other reproductive
behavior are believed to be expressed immediately after mating by the female
at an intensity dictated by the male's genome through an extranuclear phase
of inheritance (Legner 1987b, 1988a, 1989a,
1989b ). Ovisorption and Ovulation Effects.--The storage of ovulated ripe eggs in muscular oviducts of hydropic species
is correlated with the ability to discharge a large number of eggs quickly
during one insertion of the ovipositor, or a large number of eggs singly if
hosts are available. This rapidity of egg deposition probably is responsible
for the fact that an exceptional number of braconid species yield a
preponderance of male progeny (Clausen 1940). In anhydropic species
with short oviducts, ovulation occurs only when environmental conditions are
favorable for immediate egg deposition, so that the rate of oviposition may
be governed by the number of ovarioles (Clausen 1940). In gregarious species
the number of eggs deposited per host may be influenced by the number of ripe
eggs in the ovarioles (Flanders 1942). In anhydropic species oosorption may
preclude ovulation. This may account for the fact that in such species the
responsiveness to oviposition stimuli seems to be a function of the frequency
of oviposition (Flanders 1942). In this sense it was thought that early
oviposition confounded with host-feeding influenced progeny production in
some pteromalid species (Legner & Gerling 1967, Gerling & Legner 1968). Females of anhydropic
species may lose the ability to respond to oviposition stimuli if withheld
from the host for a long time (Jackson 1937 on Pimpla examinator).
King (1962) found that fecundity is sometimes lowered after ovisorption has
occurred. The number of
ovarioles varies in parasitic Hymenoptera from two (Chelonus) to 657 (Poecilogonalos
thwaitesii) (Clausen 1929).
Glands.--Accessory glands secreting acid substances, serve to
paralyze hosts and to soften the host integument. Dufour's gland secretes alkaline
substances such as lubricants for oviposition, coatings of eggs which protect them from desiccation,
phagocytosis (encapsulation) and to construct feeding tubes. Chemical Communication.--Various complex chemical compounds elicit behavioral
responses in entomophages. Some common terminologies are as follows: Allomones: chemical
substances, produced or acquired by an organism, which when contacting an
individual or another species in the natural context, evoke in the receiver a
behavioral or physiological reaction which is adaptively favorable to the
emitter (Beth 1932, Brown 1968) Kairomones: chemicals
produced or acquired by one organism which mediate behavioral or
physiological response in another organism which is favorable to the receiver
but not the emitter (Brown et al. 1970).
Some research on cotton insects shows some negative effects of
applying these compounds to insects in the field [ Please
refer to Chiri & Legner 1982-86 ]. Pheromones: chemical
compounds secreted by an animal which mediate behavior of an animal belonging
to the same species (Karlson & Butenandt 1959). Semiochemicals: Naturally
produced chemical compounds which influence insect behavior. They mediate
interactions between organisms (Law & Regnier 1971, Nordlund et al.
1981). Genetic
and Extrachromosomal Phenomena Females of Muscidifurax raptorellus increase their
longevity, daily parasitization rates and fecundity when mated with males of
a second race (Legner 1989a), and of course
the progeny resulting from such crosses also show increased fecundity over
either of their parents as was previously discussed (Legner 1988a, 1988b, 1988c). These results suggest that new species of parasitoids
liberated for biological control might thus be advantaged to overcome environmental
resistance by mating them to males of other races during the establishment
phase. The performance of resident parasitoids similarly could be improved
through liberations of exotic male races (Legner 1988d). [Please see research on Genetics]. Exercise 21.1--What factors influence progeny number in parasitic
insects? Exercise 21.2--How may natural enemies tend to avoid competition? Exercise 21.3--What is host-feeding? How does it affect natural
enemy reproduction? Exercise 21.4--Explain how host-feeding is involved in host
population regulation. Exercise 21.5--Explain and discuss ways in which selective breeding,
mating and ovisorption may influence progeny number. Exercise 21.6--Are the terms functional and numerical response new?
Ate the concepts new? Explain. REFERENCES: [Additional
references may be found at MELVYL Library ] Allen, H. W. 1954. Propagation
of Horogenes molestae, an Asiatic parasite
of the oriental fruit moth, on potato tuberworm. J. Econ. Ent. 47: 278-81. Allen, H. W. & R. F. Smith. 1958.
Some factors influencing the efficiency of Apanteles medicaginis
Muesebeck (Hymenoptera: Braconidae) as a parasite of the alfalfa caterpillar,
Colias philodice eurytheme
Boisduval. Hilgardia 28: 1-42. Alloway,
T. M. Learning and memory in insects. Ann. Rev. Ent. 17: 43-56. Altieri, M. A., and W. H. Whitcomb. 1979.
The potential use of weeds in manipulation of beneficial insects.
Horticulture Science 14:12-18. Arthur,
A. P. 1966. Associative learning in Itoplectis
conquisitor (Say) (Hymenoptera:
Ichneumonidae). Canad. Ent. 98: 213-23. Arthur,
A. P. 1967. Influence of position and size of host shelter on host-searching
by Itoplectis conquisitor (Hymenoptera:
Ichneumonidae). Canad. Ent. 99: 877-86. Arthur,
A. P., B. M. Hegdekar & L. Rollins. 1969. Component of the host
haemolymph that induces oviposition in a parasitic insect. Nature (London)
223: 966-67. Baggen, L. R., G. M.
Gurr, and A. Meats. 1999. Flowers in tri-trophic systems: mechanisms allowing
selective exploitation by insect natural enemies for conservation biological
control. Entomologia
Experimentalis et Applicata 91:155-161. Bartlett, B. R. 1961. The
influence of ants on parasites, predators and scale insects. Ann. Ent. Soc. Amer.
54: 543-51. Bartlett,
B. R. 1964. patterns in the host-feeding habits of adult parasitic
Hymenoptera. Ann.
Ent. Soc. Amer. 57: 344-50. Bellows,
T. S., Jr. & T. W. Fisher, (eds) 1999. Handbook of Biological Control:
Principles and Applications. Academic Press, San Diego, CA. 1046 p. Beth
1932. [Allomones]. Naturwissenschaften
20: 177-83. Bowen, W. R. & V. M. Stern. 1966.
Effect of temperature on the production of males and sexual mosaics in a
uniparental race of Trichogramma
semifumatum (Hymenoptera:
Trichogrammatidae). Ann.
Ent. Soc. Amer. 59: 823-34. Broodryk,
S. W. & R. L. Doutt. 1966. The biology of Coccophagoides utilis
Doutt (Hymenoptera: Aphelinidae). Hilgardia 37: 233-54. Brown
1968. [Allomones]. Amer.
Nat. 102: 188-91. Brown et al. 1970. [Kairomones].
Bioscience 20: 21-22. Burnett,
T. 1949. The effect of temperature on an insect host-parasite population.
Ecology 30: 113-34. Burnett,
T. 1951. Effects of temperature and host density on the rate of increase of
an insect parasite. Amer. Naturalist 85: 337-52. Burnett,
T. 1953. Effect of temperature and parasite density on the rate of increase
of an insect parasite. Ecology 34: 322-28. Burnett,
T. 1956. Effects of natural temperature on oviposition of various numbers of
an insect parasite (Hymenoptera, Chalcididae, Tenthredinidae). Ann. Ent. Soc. Amer.
49: 55-59. Burnett,
T. 1958a. Effect of host distribution on the reproduction of Encarsia formosa Gahan (Hymenoptera: Chalcidoidea). Canad. Ent. 90:
__ - __. Burnett,
T. 1958b. Effect of area of search on reproduction of Encarsia formosa
Gahan (Hymenoptera: Chalcidoidea). Canad. Ent. 90: 225-29. Burnett,
T. 1958c. Dispersal of an insect parasite over a small plot. Canad. Ent. 90:
279-83. Casas, J., G. Driessen,
N. Mandon, S. Wielaard, E. Desouhant, J. Van Alphen, L. Lapchin, A. Rivero,
J. P. Christides, and C. Bernstein. 2003. Energy dynamics in a parasitoid
foraging in the wild. Journal of Animal Ecology 72:691-697. Cedaña, S. M. 1937. Studies
on the biology of Coccophagus
(Hymenoptera), a genus parasitic on nondiaspine Coccidae. Univ. Calif.
Berkeley Publ. Ent. 6: 337-99. Clausen, C. P. 1929. Biological
studies on Poecilogonalos thwaitesii (Westw.), parasitic
in the cocoons of Henicospilus.
Proc. Ent. Soc. Wash. 31: 67-79. Clausen,
C. P. 1940. Entomophagous Insects. McGraw-Hill Book Co., Inc., New York &
London. 688
p. Clausen, C. P. 1950. Respiratory
adaptations in the immature stages of parasitic insects. Arthropoda 1: 197-224. Clausen, C. P., H. A. Jaynes & T. R.
Gardner. 1933. Further
investigations of the parasites of Popillia
japonica in the Far East. U.
S. Dept. Agric. Tech. Bull. 366: 59 p. Corbet,
S. A. 1968. The influence of Ephestia
kuehniella on the
development of its parasite Nemeritis
canescens. J. Exp. Biol. 48:
291-304. Cornell,
H. & D. Pimentel. 1978. Switching in the parasitoid Nasonia vitripennis
and its effects on host competition. Ecology 59: 297-308. DeBach,
P. 1943a. The effect of low storage temperature on reproduction in certain
parasitic Hymenoptera. Pan-Pacific Ent. 19: 112-19. DeBach, P. 1943b. The
importance of host-feeding by adult parasites in the reduction of host
populations. J.
Econ. Ent. 36: 647-58. DeBach,
P. 1944. Environmental contamination by an insect parasite and the effect on
host selection. Ann.
Ent. Soc. Amer. 37: 70-74. DeBach, P. & H. S. Smith. 1941.
The effect of host density on the rate of reproduction of entomophagous
parasites. J.
Econ. Ent. 34: 741-45. DeBach, P. & H. S. Smith. 1947.
Effects of parasite population density on rate of change of host and parasite
populations. Ecology 28: 290-98. Doten,
S. B. 1911. Concerning the relation of food to reproductive activity and
longevity in certain hymenopterous parasites. Univ. of Nevada Agric. Expt.
Sta. Tech. Bull. 78: 30 p. Doutt,
R. L. 1959. The biology of parasitic Hymenoptera. Ann. Rev. Ent. 4: 141-82. Doutt,
R. L. 1964. Biological characteristics of entomophagous adults, p. 141-67. In: DeBach, P. (ed.),
Biological Control of Insect Pests and Weeds. Reinhold, New York. Edwards,
R. L. 1954. The effect of diet on egg maturation and resorption in Mormoniella vitripennis (Hymenoptera,
Pteromalidae). Quart. Rev. Micro. Sci. 95: 459-68. Evans,
H. E. 1978. The Bethylidae of America North of Mexico. Mem. Amer. Ent. Inst.
27: 332 p. Faure,
J. C. 1940. Maternal care displayed by mantids (Orthoptera). J. Ent. Soc. S.
Afr. 3: 139-50. Fisher,
R. C. 1961. A study in insect multiparasitism II. The mechanism and control
of competition for possession of the host. J. Exp. Biol. 38: 605-28. Fisher,
R. C. 1963. Oxygen requirements and the physiological suppression of
supernumerary insect parasitoids. J. Exp. Biol. 40: 531-40. Fisher,
R. C. 1971. Aspects of the physiology of endoparasitic Hymenoptera. Biol.
Rev. 46: 243-78. Fisher,
R. C. & V. K. Ganesalingam. 1970. Changes in the composition of host
haemolymph after attack by an insect parasitoid. Nature (London) 227: 191-92. Flanders,
S. E. 1935a. Effect of host density on parasitism. J. Econ. Ent. 28: 898-900. Flanders, S. E. 1935b. An
apparent correlation between the feeding habits of certain pteromalids and
the condition of their ovarian follicles (Pteromalidae, Hymenoptera). Ann. Ent. Soc. Amer. 28: 438-44. Flanders, S. E. 1936. Japanese
species of Tetrastichus
parasitic on eggs of Galerucella
xanthomelaena. J. Econ. Ent. 29: 1024-25. Flanders, S. E. 1938. The
effect of cold storage on the reproduction of parasitic Hymenoptera. J. Econ. Ent. 31: 633-34. Flanders, S. E. 1942. Oosorption
and ovulation in relation to oviposition in the parasitic Hymenoptera. Ann. Ent. Soc. Amer. 35: 251-66. Flanders, S. E. 1943. The
Argentine ant versus the parasites of the black scale. Calif. Citrograph
28(5): 117, 128, 137. Flanders,
S. E. 1950. Regulation of ovulation and egg disposal in the parasitic
Hymenoptera. Canad. Ent. 82: 134-40. Flanders,
S. E. 1951a. Mass culture of California red scale and its golden chalcid
parasites. Hilgardia 21: 1-42. Flanders,
S. E. 1951b. The role of the ant in the biological control of homopterous
insects. Canad. Ent. 83: 93-98. Flanders,
S. E. 1953a. Variations in susceptibility of citrus-infesting coccids to
parasitization. J.
Econ. Ent. 46: 266-9. Flanders, S. E. 1953b. Predatism
by the adult hymenopterous parasite and its role in biological control. J. Econ. Ent. 46: 541-44. Flanders, S. E. 1956. The
mechanisms for sex-ratio regulation in the (parasitic) Hymenoptera. Insectes
Sociaux 3: 325-34. Flanders,
S. e. 1958. The role of the ant in the biological control of scale insects in
California. Proc. 10th Intern. Cong. Ent. 4: 579-82. Flanders,
S. E. & M. E. Badgley. 1963. Prey-predator interaction in self balanced
laboratory populations. Hilgardia 35: 145-83. Fried,
C. S. & D. Pimentel. 1986. Host parasitism and progeny production of two
strains of the parasitoid Nasonia
vitripennis (Hymenoptera:
Pteromalidae) on the house fly (Diptera: Muscidae). Environ. Ent. 15: 439-42. Fried,
C. S., D. A. Rutz & D. Pimentel. 1990. Host parasitism and progeny
production of two geographic strains of the parasitoid Nasonia vitripennis
(Hymenoptera: Pteromalidae) on house fly (Diptera: Muscidae) hosts. Environ.
Ent. 19: 322-6. Gerling,
D. 1966. Studies with whitefly parasites of southern California I. Encarsia pergandiella Howard (Hymenoptera: Aphelinidae). Canad.
Ent. 98: 707-24. 1968 Gerling, D. & E. F. Legner. 1968.
Developmental history and reproduction of Spalangia cameroni,
parasite of synanthropic flies. Ann.
Entomol. Soc. Amer. 61(6): 1436-1443. Gordh,
G. 1976. Goniozus gallicola Fouts, a parasite of
moth larvae, with notes on other bethylids (Hymenoptera: Bethylidae;
Lepidoptera: Gelechiidae). U. S. Dept. Agr. Tech. Bull. 1524. 27 p. Gordh,
G. & H. E. Evans. 1976. A new species of Goniozus imported into California from Ethiopia for the
biological control of pink bollworm and some notes on the taxonomic status of
Parasierola and Goniozus (Hymenoptera:
Bethylidae). Proc. Ent. Soc. Wash. 78: 479-89. Gordh,
G. & B. Hawkins. 1981. Goniozus
emigratus (Rohwer), a
primary external parasite of Paramyelois
transitella (Walker), and comments
on bethylids attacking Lepidoptera (Hymenoptera: Bethylidae; Lepidoptera:
Pyralidae). J. Kans. Ent. Soc. 54: 787-803. Gordh,
G., J. B. Woolley & R. A. Medved. 1983. Biological studies on Goniozus legneri Gordh (Hymenoptera: Bethylidae) a primary external
parasite of the navel orangeworm, Amyelois
transitella (Walker) and
pink bollworm, Pectinophora gossypiella (Saunders)
(Lepidoptera, Pyralidae, Gelechiidae). Cont. Amer. Ent. Inst. 20: 433-68.
1983 Gordh,
G. & R. A. Medved. 1986. Biological notes on Goniozus pakmanus
Gordh (Hymenoptera: Bethylidae), a parasite of pink bollworm, Pectinophora gossypiella (Saunders)
(Lepidoptera: Gelechiidae). J.
Kans. Ent. Soc. 59: 723-34. Hagen, K. S. 1986. Ecosystem analysis: Plant cultivars (HPR), entomophagous
species and food supplements. Pages 153-197 in D. J. Boethel and R. D.
Eikenbary, editors. Interactions of Plant Resistance and Parasitoids and
Predators of Insects. John Wiley and Sons, New York. Hartley,
E. A. 1922. Some bionomics of Aphelinus
semiflavus (Howard), chalcid
parasite of aphids. Ohio J. Sci. 22(8): 209-36. Hocking, H. 1966. The influence of food on
longevity and oviposition in Rhyssa persuasoria (L) (Hymenoptera:
Ichneumonidae). Journal of the Australian Entomological Society 6:83-88. Illingworth, J. F. 1921. Natural enemies of
sugar-cane beetles in Queensland. Queensland Bureau Sugar experimental
Station Division of Entomology Bulletin 13:1-47. Jackson,
D. J. 1937. Host-selection in Pimpla
examinator F. (Hymenoptera).
Proc. Roy. Ent. Soc. London 12(A): 81-91. Jervis, M. A., N. A. C. Kidd, and G. E.
Heimpel. 1996. Parasitoid adult feeding behaviour and biocontrol - a review.
Biocontrol News and Information 17:11N-26N. Johnston,
F. A. 19l5. Asparagus-beetle egg parasite. J. Agric. Res. 4: 303-13. King,
P. E. 1962. The effect of resorbing eggs upon the sex ratio of the offspring
in Nasonia vitripennis (Hymenoptera:
Pteromalidae). J. Expt. Biol. 39: 161-65. Lee, J. C., and G. E.
Heimpel. 2003. Nectar availability and parasitoid sugar feeding. Proceedings
of the 1st International Symposium on Biological Control of Arthropods. Honolulu, Hawaii:220-225. Lee, J. C., G. E. Heimpel, and G. L. Leibee.
2004. Comparing floral nectar and aphid honeydew diets on the longevity and
nutrient levels of a parasitoid wasp. Entomologia
Experimentalis et Applicata 111:189-199. 1967a Legner, E. F. 1967. Two exotic
strains of Spalangia drosophilae merit consideration in
biological control of Hippelates collusor (Diptera: Chloropidae). Ann. Entomol. Soc. Amer. 60(2): 458-462. 1967b Legner, E. F. 1967. Behavior changes
the reproduction of Spalangia cameroni, S. endius, Muscidifurax raptor, and Nasonia vitripennis (Hymenoptera: Pteromalidae) at increasing
fly host densities. Ann. Entomol.
Soc. Amer. 60(4): 819-826. 1969a Legner, E. F. 1969. Adult emergence
interval and reproduction in parasitic Hymenoptera influenced by host size
and density. Ann. Entomol. Soc. Amer.
62(1): 220-226. 1969b Legner, E. F. 1969. Distribution
pattern of hosts and parasitization by Spalangia
drosophilae (Hymenoptera:
Pteromalidae). Canad. Entomol. 101(5): 551-557. 80. Legner, E. F. 1972. Observations on hybridization and
heterosis in parasitoids of synanthropic flies. Ann. Entomol. Soc. Amer. 65(1): 254-263. 1976 Legner, E. F. 1976. Low storage
temperature effects on the reproductive potential of three parasites of Musca domestica. Ann. Entomol. Soc. Amer. 69(3): 435-441. 1987a Legner, E. F. 1987. Transfer of thelytoky
to arrhenotokous Muscidifurax raptor Girault & Sanders
(Hymenoptera: Pteromalidae). Canad.
Entomol. 119(3): 265-271 1987b Legner, E. F. 1987. Inheritance of
gregarious and solitary oviposition in Muscidifurax
raptorellus Kogan & Legner
(Hymenoptera: Pteromalidae). Canad.
Entomol. 119(9): 791-808. 1987b Legner, E. F. 1987. Pattern of
thelytoky acquisition in Muscidifurax
raptor Girault & Sanders
(Hymenoptera: Pteromalidae). Bull.
Soc.Vector Ecol. 12(2): 517-527 1988a
Legner, E. F. 1988. Muscidifurax
raptorellus (Hymenoptera:
Pteromalidae) females exhibit postmating oviposition behavior typical of the male genome. Ann. Entomol. Soc. Amer. 81(3): 522-527. 1988b
Legner, E. F. 1988. Quantitation of heterotic behavior in
parasitic Hymenoptera. Ann. Entomol.
Soc. Amer. 81(4): 657-681. 1988c
Legner, E. F. 1988. Hybridization in principal parasitoids of
synanthropic Diptera: the genus Muscidifurax (Hymenoptera: Pteromalidae). Hilgardia
56(4): 36 pp. 1988d Legner, E. F. 1988. Studies of four thelytokous Puerto Rican
isolates of Muscidifurax uniraptor [Hymenoptera:
Pteromalidae]. Entomophaga 33(3); 269-280. 1989 Legner, E. F. 1989. Fly parasitic wasp, Muscidifurax raptorellus
Kogan & Legner (Hymenoptera: Pteromalidae) invigorated through insemination by males of different
races. Bull. Soc. Vector Ecol.
14(2): 291-300. 1989. Legner, E. F. 1989. Wary genes and
accretive inheritance in Hymenoptera.
Ann.
Entomol. Soc. Amer. 82(3): 245-249. 1967 Legner, E. F. & D. Gerling. 1967. Host-feeding and oviposition on Musca domestica by Spalangia cameroni, Nasonia vitripennis,
and Muscidifurax raptor (Hymenoptera: Pteromalidae)
influences their longevity and fecundity.
Ann. Entomol. Soc. Amer. 60(3):
678-691. 1977 Legner, E. F. & S. N. Thompson. 1977.
Effects of the parental host on host selection, reproductive
potential, survival and fecundity of the egg-larval parasitoid Chelonus sp. near curvimaculatus, reared on Pectinophora
gossypiella and Phthorimaea operculella. Entomophaga
22(1): 75-84. 1966 Legner, E. F., E. C. Bay & R. A.
Medved. 1966. Behavior of three native pupal parasites
of Hippelates collusor in controlled systems.
Ann. Entomol. Soc. Amer. 59(5):
977-984. Lloyd,
D. C. 1938. A study of some factors governing the choice of hosts and
distribution of progeny by the chalcid Ooencyrtus
kuwanae Howard. Phil. Trans.
Roy. Soc. London Ser. B, 229: 275-322. Lloyd,
D. C. 1940. Host selection by hymenopterous parasites of the moth Plutella maculipennis Curtis. Proc. Roy. Ent. Soc. London Ser. B,
128: 451-84. Lund,
H. O. 1934. Some temperature and humidity relations of two races of Trichogramma minutum Riley (Hym.
Chalcididae). Ann. Ent. Soc. Amer. 27: 324-40. Lund,
H. O. 1938. Studies on longevity and productivity in Trichogramma evanescens.
J. Agric. Res. 56: 421-39. Madden,
J. L. & D. Pimentel. 1965. Density and spatial relationships between a
wasp parasite and its housefly host. Canad. Ent. 97: 1031-7. Martin,
O. H. 1946. The effect of humidity on the oviposition activity of Macrocentrus ancylivorus. J. Econ. Ent. 39: 419. Martin,
C. H. & G. L. Finney. 1946. Control of the sex ratio in Macrocentrus ancylivorus. J. Econ. Ent. 39: 269-99. Moursi,
A. A. 1946. The effect of temperature on development and reproduction of Mormoniella vitripennis (Walker). Bull.
Soc. Fouad ler Entomol. 30: 39-61. Nagel,
W. P. & D. Pimentel. 1963. Some ecological attributes of a pteromalid
parasite and its housefly host. Canad. Ent. 95; 208-13. Nagel,
W. P. & D. Pimentel. 1964. The intrinsic rate of natural increase of the
pteromalid parasite Nasonia vitripennis (Walk.) on its
muscoid host Musca domestica L. Ecology 45:
658-60. Nordlund et al. (eds.).
1981. Semiochemicals. John Wiley & Sons. 1974 Olton, G. S. & E. F. Legner. 1974.
Biology of Tachinaephagus zealandicus (Hymenoptera: Encyrtidae),
parasitoid of synanthropic Diptera. Canad. Entomol. 106(8): 785-800. Pimentel,
D. 1966. Wasp parasite (Nasonia
vitripennis) survival on its
house fly host (Musca domestica) reared on various
foods. Ann.
Ent. Soc. Amer.
59: 1031-38. Pimentel, D. & R. Al-Hafidh. 1963.
The coexistence of insect parasites and hosts in laboratory ecosystems. Ann. Ent. Soc. Amer.
56: 676-8. Pimentel,
D. & F. Cranston. 1960. The house cricket, Acheta domesticus,
and the housefly, Musca domestica, as a model
predator-prey system. J.
Econ. Ent. 53: 171. Pimentel,
D. & F. A. Stone. 1968. Evolution and population ecology of parasite-host
systems. Canad. Ent. 100: 655-62. Pontin,
A. J. 1958. Some records of predators and parasites adapted to attack aphids
attended by ants. Entomol. Mem. Mag., London 95: 154-55. Quezada, J. R. 1967. Biological
studies of Signiphora "Borinquensis," new species
(Hymenoptera: Thysanidae), a primary parasite of diaspine scales. M. S.
Thesis, Univ. of Calif., Riverside. 98 p. Quezada, J. R., P. H. DeBach & D.
Rosen. 1973. Biological and
taxonomic studies of Signiphora
borinquensis, new species
(Hymenoptera: Signiphoridae), a primary parasite of diaspine scales.
Hilgardia 41: 543-604. Rogers, C. E. 1985.
Extrafloral nectar: entomological implications. Bulletin ESA 31:15-20. Rogers, M. E., and D. A. Potter. 2004.
Potential for sugar sprays and flowering plants to increase parasitism of
white grubs (Coleoptera : Scarabaeidae) by Tiphiid wasps (Hymenoptera :
Tiphiidae). Environmental Entomology 33:619-626. Rohwer,
S. A. 19l3. Notes on the feeding habits of two adult sawflies. Proc. Ent.
Soc. Wash. 15: 148-9. Romeis, J., and F. L. W„ckers. 2002.
Nutritional suitability of individual carbohydrates and amino acids for adult
Pieris brassicae. Physiological Entomology 27:148-156. Salt,
G. 1937. The sense used by Trichogramma
to distinguish between parasitized and unparasitized hosts. Proc. Roy. Soc.
London Ser. B: Biol. Sci. 122: 57-75. Salt,
G. 1961. Competition among insect parasitoids. Symposia Soc. Exper. Biol. 15:
Mechanisms in Biol. Competition. p. 96-119. Schmieder,
R. G. 1938. The sex ratio in Melittobia
chalybii Ashmead,
gametogenesis and cleavage in female and in haploid males (Hymenoptera:
Chalcidoidea). Biol. Bull. 74: 256-66. Schread,
J. C. & P. Garmon. 1934. Some effects of refrigeration on the biology of Trichogramma in artificial
rearing. J. New York Ent. Soc. 42: 263-83. Simmonds,
F. J. 1956. Superparasitism by Spalangia
drosophilae Ashm. Bull. Ent.
Res. 47: 361-76. Smirnov,
E. & M. Wladimirowa. 1934.
Studien über die Vernehrungsfähigkeit der Pteromalidae, Mormoniella vitripennis
(Walker). Z. wiss. Zool. 145: 502-22. Smith,
G. J. C. & D. Pimentel. 1969. The effect of two host species on the
longevity and fertility of Nasonia
vitripennis. Ann. Ent. Soc. Amer.
62: 305-8. Stary,
P. 1966. Aphid parasites (Hym., Aphidiidae) and their relationship to aphid
attending ants, with respect to biological control. Insectes Sociaux 13(3):
185-202. Taylor,
R. J. 1974. Role of learning in insect parasitism. Ecol. Monographs 44:
89-104. Turlings, T. C. J., and F. L. Wackers. 2004.
Recruitment of predators and parasitoids by herbivore-injured plants. Pages
21-75 in R. T. Card‚ and J. Millar, editors. Advances in Chemical Ecology of
Insects Utida,
S. 1950. On the equilibrium state of the interacting population of an insect
and its parasite. Ecology
31: 165-75. Utida, S. 1953. Effect
of host density upon the population growth of two interacting species of
parasites. Experimental Studies on Superparasitism, 2nd Rept. Oyo-Kontyu 9: 102-7. Utida, S. 1957. Population
fluctuation, an experimental and theoretical approach. In: Cold Spring Harbor Symp. on Quantitative Biology 22:
139-51. Van den Meiracker, R. A. F., and P. M. J.
Ramakers. 1991. Biological control of the western flower thrips Frankliniella
occidentalis, in sweet pepper with the anthocorid predator Orius insidiosus. Mededelingen
van de Faculteit Landbouwwetenschappen, Rijksuniversiteit Gent 56/2a:241-249. van Emden, H. F. 1965. The role of
uncultivated land in the biology of crop pests and beneficial insects.
Scientific Horticulture 17:121-136. van Rijn, and J. Bruin,
editors. Plant-Provided Food for Carnivorous Insects: a protective mutualism
and its applications. Cambridge University Press, Cambridge van Rijn, P. C. J., and
L. K. Tanigoshi. 1999. Pollen as food for the predatory mites Iphiseius
degenerans and Neoseiulus cucumeris (Acari : Phytoseiidae): dietary range and
life history. Experimental and Applied Acarology 23:785-802. Wackers, F. L. 1999.
Gustatory response by the Hymenopteran parasitoid Cotesia glomerata to a
range of nectar and honeydew sugars. Journal of Chemical Ecology
25:2863-2877. Wackers, F. L. 2000. Do
oligosaccharides reduce the suitability of honeydew for predators and
parasitoids? A further facet to the function of insect-synthesized honeydew
sugars. Oikos 90:197-201. Wackers, F. L. 2001. A
comparison of nectar- and honeydew sugars with respect to their utilization
by the hymenopteran parasitoid Cotesia glomerata. Journal of Insect
Physiology 47:1077-1084. Wackers, F. L. 2004.
Assessing the suitability of flowering herbs as parasitoid food sources:
Flower attractiveness and nectar accessibility. Biological Control
29:307-314. Wackers, F. L. 2005.
Suitability of (extra-) floral nectar, pollen and honeydew as insect food
sources. in F. L. W„ckers, P. C. J. van Rijn, and J. Bruin, editors.
Plant-Provided Food for Carnivorous Insects: a protective mutualism and its
applications. Cambridge University Press, Cambridge. Wackers, F. L., and A.
Steppuhn. 2003. Characterizing nutritional state and food source use of
parasitoids collected in fields with high and low nectar availability. IOBC
WPRS Bulletin 26:203-208. Wackers, F. L., and P.
C. J. van Rijn. 2005. Food for protection: an introduction. in F. L. Wackers,
P. C. J. Wäckers,
F. L. and P.C.J. van Rijn .
2005. Plant food to enhance the
performance of natural enemies in mass rearing and the field. Encyclopedia of Pest Management (ed. D.
Pimentel, Cornell University) [in press] van
Steenburgh, W. E. 1934. Trichogramma
minutum Riley as a parasite
of the Oriental fruit moth (Laspeyresia
molesta Busck.) in Ontario.
Canad. J. Res. 10: 287-314. Wajnberg,
E. & J. Pizzol. 1989. The problem of superparasitism in the production of
natural enemies for inundative biological: a genetical approach. In: "Parasites", R. Cavalloro
& V. DeLucci (eds.). Proc. Scien. Congress,
Barcelona, Spain 1988. p. 437-44. Wajnberg,
E., J. Pizzol & M. Babault. 1989. Genetic variation in progeny allocation
in Trichogramma maidis. Ent. exp. appl. 53:
177-87. Walker,
I. & D. Pimentel. 1966. Correlation between maternal longevity and
incidence of diapause in Nasonia
vitripennis Walker
(Hymenoptera: Pteromalidae). Gerontologia 12: 89-98. Weseloh, R. M. 1969. Biology
of Cheiloneurus noxius, with emphasis on host
relationships and oviposition behavior. Ann. Ent. Soc. Amer. 62: 299-305. Weseloh, R. M. 1971. Influence
of host deprivation and physical host characteristics on host selection
behavior of the hyperparasite Cheiloneurus
noxius (Hymenoptera:
Encyrtidae). Ann.
Ent. Soc. Amer. 64: 580-86. Weseloh, R. M. 1971. Influence
of primary (parasite) hosts on host selection of the hyperparasite Cheiloneurus noxius (Hymenoptera:
Encyrtidae). Ann.
Ent. Soc. Amer. 64: 1233-36. Weseloh, R. M. & B. R. Bartlett. 1971.
Influence of chemical characteristics of the secondary scale host on host
selection behavior of the hyperparasite Cheiloneurus
noxius (Hymenoptera:
Encyrtidae). Ann.
Ent. Soc. Amer. 64: 1259-64. Wilkes, A. 1942. The
influence of selection on the preferendum of a chalcid (Microplectron fuscipennis
Zett.) and its significance in the biological control of an insect pest. Proc. Boy. Soc. Ser. B,
Biol. Sci. 130: 400-15. Wilkes,
A. 1947. The effects of selective breeding on the laboratory propagation of
insect parasites. Proc. Roy. Ent. Soc. London Ser B, 134: 227-45. Wilkes,
A. 1963. Environmental causes of variation in the sex ratio of an
arrhenotokous insect, Dahlbominus
fuliginosus (Nees)
(Hymenoptera: Eulophidae). Canad. Ent. 95: 183-202. Wylie,
H. G. 1958. Factors that affect host finding by Nasonia vitripennis
(Walk.) (Hymenoptera:
Pteromalidae). Canad. Ent.
40: 597-608. Wylie, H. G. 1963. Some
effects of host age on parasitism by Nasonia
vitripennis (Walk.) (Hymenoptera: Pteromalidae). Canad. Ent. 95: 881-86. Wylie, H. G. 1965a. Effects
of superparasitism on Nasonia
vitripennis (Hymenoptera:
Pteromalidae). Canad. Ent. 97: 326-31. Wylie,
H. G. 1965b. Some factors that reduce the reproductive rate of Nasonia vitripennis (Walk.) at high adult population densities.
Canad. Ent. 97: 970-77. Wylie,
H. G. 1966a. Survival and reproduction of Nasonia
vitripennis (Walk.) at
different host population densities. Canad. Ent. 98: 275-81. Wylie,
H. G. 1966b. Some mechanisms that affect the sex ratio of Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae) reared
from superparasitized fly pupae. Canad. Ent. 98: 645-53. Wylie,
H. G. 1971. Observations on intraspecific larval competition in three
hymenopterous parasites of fly puparia. Canad. Ent. 103: 137-42. Zoebelein, G. Z. 1956a. Der Honigtau als
Nahrung der Insekten. Teil I. Zeitschr. angew. Ent. 38: 369-416. Zoebelein, G. Z. 1956b. Der Honigtau als
Nahrung der Insekten. Teil II. Zeitschr. angew. Ent. 39: 129-67. Zoebelein, G. Z. 1957. Z. angew. Ent. 76:
1-64. |