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Overview	Adult Parasitoid Food	Glands
Behavioral and Ecological	Larval Competition	Chemical Communication
Courtship & Copulation	Ant Activity	Genetic & Extranuclear
Host Location	Learning	Exercises
Host Attack & Paralysis	Physiological phenomena	References
Host Preferences	Nutrition (host-feeding)	Host Transport
Temperature	Progeny Defense	Humidity
Oviposition Restraint	Selective Breeding	Host / Parasitoid Density
Mating	Temperature	Ovisorption & Ovulation Effects
Host Size	Humidity	References [Please refer also to Selected Reviews & Detailed Research ]

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:

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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, larval competition can be eliminated by the female not fertilizing her eggs under conditions where superparasitism is possible. 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 predatism. 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 scar = 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].

Exercises:

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.

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