HABITAT, HOST-FINDING AND HOST ACCEPTANCE
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Characteristics of the Habitat Influence Natural Enemies
Host Food Affects Suitability for Parasitization
Habitat Diversity vs. Similarity Affects Population Stability
[Please refer also to Selected Reviews
Although a few species of parasitoids attack only a single host species, most of them attack several different hosts in nature. No parasitoids are completely indiscriminate, however. Under natural conditions, a parasitoid will attack only a fraction of the species on which development is actually possible.
The processes in host selection involve four main steps: (1) host-habitat finding, (2) host-finding, (3) host acceptance and (4) host suitability. A fifth criterion, host regulatory capacity, is sometimes proposed, but it refers to the ability of the parasitoid to change biochemical reactions in the host. It is confused with the ability of the parasitoid to regulate its host's population density, and therefore is a poor choice of terms.
Habitat Effects on Natural Enemies
Picard & Rabaud (1914) observed that many parasitic Hymenoptera attack larvae of species in different families and even different orders, provided that the hosts feed on the same species of food plant. Cushman (1926) cited two cases where the same parasitoid attacked two different insects belonging to two different orders because of its habit of parasitizing leaf miners. It was recognized that the systematic relationship was not important, but rather the fact that both hosts were mining in a leaf.
Laing (1937) observed that Alysia manducator (Panzer) was attracted to the odor of decomposing meat even in the absence of hosts, which in this case were carrion flies. She also observed that Nasonia vitripennis was attracted to carrion, but that Trichogramma evanescens West was rather attracted by the sight of the host and not by odor of the eggs of Sitotroga cereallella (Olivier). This and other work led her to propose three steps in the attack activity of a parasitoid: (1) attraction to the host habitat, (2) attraction to host individuals in the habitat and (3) acceptance or rejection of the host.
Flanders (1937) working in the same time period observed a fourth step in the parasitization process. His proposed steps were (1) host habitat finding, (2) host-finding, (3) host acceptance and (4) host suitability.
There have been many restatements of these procedures in host selection that did not add anything significant to those rather clearly and thoroughly outlined above, although new species of natural enemies were considered (Hodek 1966 with coccinellids; Monteith 1955 with tachinids; Salt 1935, 1958 with parasitic Hymenoptera; and Thorpe & Caudle 1938, with ichneumonids, to mention just a few). As a forerunner of the idea of a sequence of events leading to host selection, Davis (1896) observed, without indicating the cause, that some plants such as Nicotiana, Pelargonium, Datura, Eucalyptus, etc., were repellent to Encarsia formosa Gahan, a whitefly parasitoid.
The behavior of the natural enemy to be attracted to a specific habitat rather than directly to the host in the habitat is very important in biological control, and ignoring this important step in natural enemy attack behavior still continues to lead novice biological control workers astray. Flanders (1940) even indicated that the presence of uninfested plants having greater attractiveness than infested plants may prevent the establishment of the colonized parasitoid.
Salt (1935) considered that, "It is obvious in the first place that in order to interact, the parasite and the host must meet. Now, it is certain that some parasites, and probably more, are first attracted not to a particular host but to a certain type of environment." Smith (1949) believed that, "Recognition must be given to the possibility that the host plant may confer on the host insect a kind of immunity to parasitization." With these and many more statements over the years emphasizing the importance of habitat or environment, there is no excuse for errors to continue to be made.
The term "ecologically incomplete parasitism" has been coined for situations when the number of host habitats in which a highly suitable host is susceptible to attack is less than the total number of habitats occupied in common by this host and its parasitoid (Flanders 1953). For example, prior to 1940 the lack of attractiveness to the parasitoid by citrus trees could account for inadequate control of the black scale by its parasitoid in southern California (Flanders 1940).
Van Steenburg as early as 1934 observed that when a species is liberated in a habitat which is not suitable for it, it soon disappears, even in the presence of suitable hosts. This was demonstrated with two species of Trichogramma in peach orchards. The native species of parasitoid persisted and the imported ones which were released disappeared.
Characteristics of the Habitat that Attract or Repel Natural Enemies
The external leaf structure effects natural enemy activity. Downing & Moilliet (1967) found the highest populations of predaceous mites in the varieties Spartan and McIntosh apples having hairy leaves and pronounced veins, which create more sheltered areas for phytoseiids and more protection from macropredators such as Hemiptera. The Delicious variety had the lowest numbers of predators presumably due to the smoothness of the leaves.
Putman & Herne (1966) found the same relationship with peach varieties: mirid predators of Panonychus ulmi were more abundant on hairy-leafed varieties.
A higher Heliothis egg parasitism by Trichogramma was recorded on the smooth upper surface of corn leaves than in any other part of the plant (Phillips &
Barber 1933); and Milliron (1940) obtained the highest parasitism of the greenhouse whitefly by Encarsia formosa on smooth leaves, and the lowest parasitism on pubescent leaves.
Thompson (1951) explained the failure to establish twelve species of coccinellids in Bermuda for diaspine scale control on cedar, on the fact that the cedar leaves were so short, rigid and hard to move that the beetles could not grip the scale bodies.
Leaf exudations can influence parasitoid activity. Rabb & Bradley (1968) found that Trichogramma and other parasitoids failed to attack Manduca eggs on fresh tobacco leaves because parasitoids became stuck in the gummy exudate of the trichomes. Milliron (1940) observed that droplets of honeydew disturbed Encarsia formosa on the whitefly host.
Odor of the host food is thought to have a very significant influence on natural enemy activity. The ichneumonid Nemeritis canescens Gravenstein, which is parasitic on Ephestia kuhniella (Zeller), is first attracted to the odor of the larval food, oatmeal (Thorpe & Jones 1937). Alysia manducator and Nasonia vitripennis are attracted to decomposing meat on which the maggots of their host feeds (Laing 1937). Edwards (1954) refuted Laing's finding by recognizing that the attraction of Nasonia was actually to the combination of decomposing meat plus the presence of host larvae, but not to either alone.
Thorpe & Caudle (1938) observed that immature females of Pimpla ruficollis Gravenstein were repelled by the odor of oil secreted by Pinus silvestris, whereas sexually mature females were strongly attracted. This was especially significant because the period of repellency coincides with the period in which the host caterpillar (pine shoot moth) is not yet available for the parasitoid. An identical situation with another parasitoid, Eulimaeria eufifemur Thorn, was found. Parker (1918) had found something similar with Chloropisca glabra Meigen, but did not recognize it as repulsion. In this case attraction occurred only when ovarian development was complete.
The tachinid parasitoid of Diprion hercyniae (Htg.) is strongly attracted by the odor of old plant growth. There were thirteen times as many attacks when the host occurred on new growth (Monteith 1966). In fact both hosts and parasitoids apparently preferred old growth.
Host Food Affects Suitability For Parasitization
Numerous authors have observed that the food of the host may affects its parasitoids. Simmonds (1944) reported three to four times more parasitism by Comperiella bifasciata Howard on Aonidiella aurantii Maskell on oranges than on lemons. He attributed this to the fact that since host-feeding is involved the scale body fluids acquire a distinctive character from the host plant that could affect the parasitoids' vitality and fecundity. Smith (1957) observed this also but did not relate it to Simmonds' work.
Hodek (1966) gave an example of food toxicity to natural enemies. Rodolia (Novius) cardinalis Malshant did not prey on Icerya purchasi Maskell when it was feeding on two plants in the family Viciacae, Sparticum tunceum and Genista aetnesis. The yellow pigment genistein and alkaloids that these plants contain are harmful to Rodolia. Other examples are Morgan (1910), Gilmore (1938), Flanders (1942) and Lawson (1959).
Other Influences of Habitat
Collyer (1958) registered higher populations of Typhlodromus tilliae Ondems on larger plants than on smaller plants. She concluded that the rate of development of the predator depended on the size of the host plant.
Graham & Baumhoffer (1927) and Arthur (1962) reported that bud size of different pine tree species influenced the degree of parasitism on lepidopterous pests of these plants. The smaller the buds, the higher the percent parasitism. Smaller buds do not afford adequate protection to host larvae.
Franklin & Holdaway (1960) found that the parasitoid of the European corn borer, Lydella grisescens Robineau-Desvoidy was significantly more attracted to a certain hybrid of corn than to any other variety. Fleschner & Scriven (1957) observed higher rates of oviposition of Chrysopa californica (Coquillett) on lemons growing on loose sandy soil than on trees growing on compact silt soil. Soil type influenced natural enemy abundance on the plant. Monteith (1964) obtained two to four times as many attacks by Drino bohemica Mesnill and Bessa harveyi Towns on sawflies exposed on unhealthy plants as on larvae exposed on healthy plants. Therefore, host plant health was found to determine degree of parasitism, and was very important to host regulation in cases of severe attacks.
Still other influences of the habitat on natural enemy activity are recorded by Flanders (1935) who observed that the excreta of the host insect attracts natural enemies. Gullman & Hodson (1961) found attraction to certain plant sexual structures; Ullyett (1949) to certain host pupation depths; (Chandler (1966, 1967) to visual stimuli of the plant, and McLeod (1951) to the height of host location. Davis (1896) and Speyer (1929) observed repellent effects of the plant and Stary (1964) found that when a host insect is dioecious (eg., aphids), the host is attacked by different parasitoid complexes depending on the type of habitat in which it occurs.
Other references on this subject are Nishida (1956), Richards (1940), Salt (1958), Tamaki & Weeks (1968), Zwolfer & Kraus (1957), Seamans & McMillan (1935), Sol (1966), Skuhravy & Novak (1966), DeBach, Fleschner & Dietrick (1949), Clausen (1962), Beirne (1962), Hodek (1966), Iperti (1966), Klausmitzer (1966), and Dusek & Laska (1966).
Habitat Diversity vs Similarity Affects Population Stability
DeLoach (1970) discussed ways to alter the habitat that produces better control. He believed that habitat diversity is an effective situation to increase the effectiveness of natural enemies, particularly parasitoids and predators. Examples of areas where habitat diversity favors greater pest population stability are in the Canete Valley of Peru, the Waco, Texas area, the San Joaquin Valley of California, and the Mississippi delta area of southeastern Missouri.
Once the host habitat is located, the hosts are subsequently found by a combination of random and directed searching such as occurs in Angita sp., a parasitoid of Plutella maculipennis Curtis (Ullyett 1943, 1947, Doutt 1959). Considerable research shows that various combinations of random and directed movements (taxes) are involved. Chemotactic, phototactic, hydrotactic and geotactic responses, among others, all seem to play a part in the host-finding process. These responses are variously modified by olfactory, visual and other physical stimuli that characterize a parasitoid's prey. The sense of smell seems to be widely used by parasitoids in locating hosts. Ullyett (1953) found Pimpla bicolor Bouche swarmed around the pupae of the lepidopteran Euproctis terminalis Walker on pines in South Africa. In fact, olfaction is widely used by parasitoids in locating hosts. Bouchard & Cloutier (1985). Female Aphidius nigripes Ashmead were attracted to odors of conspecific females (Bouchard & Cloutier 1985, Dicke et al. 1985, van Alphen & Vet 1986) and this behavior may be acquired (Vet 1983, 1985). Host trail odors may facilitate searching (Price 1970). Other olfactory stimuli exist (Vet & Bakker 1985, Vet & van Alphen 1985), and some physical host characteristics affect host selection (Weseloh 1969, 1971a,b, 1972; Weseloh & Bartlett 1971, Wilson et al. 1974).
The addition of kairomones to a habitat has resulted in some parasitoids being able to locate their hosts more efficiently (Gross et al. 1975, Jones et al. 1971, Altieri et al. 1982, Gardner & van Lenteren 1986). For example, Trichogramma respond to chemical extracts of host moth body scales, while certain braconids respond to extracts of host larval frass. Synthesis of these kairomones is currently being attempted in order to permit their use for biological control on a broader scale (Lewis et al. 1971, 1972; Vinson 1968, 1975, 1976; Weseloh 1974). In some instances kairomones may function to confuse parasitoids into lesser searching efficiency (DeBach 1944, Chiri & Legner 1983, 1986).
Eran Pichersky (2004) noted that what we perceive as fragrances are actually sophisticated tools that plants utilize to entice or discourage other organisms. Although volatile plant compounds probably evolved to repel hebivores, they are now known to perform a remarkable range of functions. Most of the animals that interact with plants are insects that detect volatile compounds through the antennae, or the maxillary palps. Specialized cells on the antennae contain a single type of protein receptor that recognizes and binds specific volatile compounds. The array of receptor-decorated cells sends signals to the brain by way of the nervous system. Although each cell contains only one receptor type, a single compound can be recognized by more than one receptor. Thus the pattern of neuronal firing that results by a specific compound or mixture will be unique. This system is extremely sensitive and some receptors can detect an airborne volatile at concentrations of a few parts per billion.
For biological pest control these findings are highly significant. Plants not only emit volatile compounds acutely, at the site where herbivores (mites, caterpillars, aphids, etc.) are consuming them, but also generally from non-damaged parts of the plant. These signals attract a variety of predatory insects that prey on the plant-feeders. In one example parasitic wasps can detect the volatile signature of a damaged plant and will lay their eggs inside the offending caterpillar. The ensuing parasitoid larvae eventually destroy the caterpillar. The growth of infected caterpillars is markedly retarded, to the benefit of the plant. Also, volatile compounds released by plants in response to herbivore egg laying can attract egg parasitoids and thereby prevent them from hatching (Pichersky 2004). Synthesis of many plant volatiles is possible, and their application with mass releases of parasitoids and predators offers promise for increasing the extent of pest control. However, extensive field experiments would be required to establish effectiveness for any given agroecosystem, as theoretical predictions may not be realized. For examples some instances such volatiles may function to confuse parasitoids into lesser searching efficiency (DeBach 1944, Chiri & Legner 1983, 1986).
Once physical contact has been made, only the reception of a proper combination of stimuli will trigger further behavioral responses, resulting in acceptance of the prey; i.e., resulting int he acts of oviposition and/or host-feeding. The stimuli for attack are known to involve, among other factors, host odor, host size, host location, host shape and even host motion, and the history of parasitoid larval development (Brydon & Bishop 1945, Legner & Thompson 1977, O. J. Smith 1950, Olton 1969).
Flanders maintained that the act of mating or the presence of sperm in the spermatheca has an effect on the psychology of the female. This was suggested by the fact that unmated females tend to attack more host species than mated ones. In certain Aphelinidae mating has a remarkable psychological effect because significant changes occur in the type of host selected and the manner of oviposition. Examples are found in the genera Aneristus, Casca, Coccophagus, Euxanthellus and Phycus, where females develop only as primary endoparasitoids of coccids and alyrodids. When unmated the females of some species in these genera oviposit only hyperparasitically in a host already parasitized by the same or similar species. Therefore, the male develops only as a primary parasitoid of the immature instars of its own or similar species, and the host of the male is never the host of the female, nor the host of the female the host of the male (Flanders 1937, 1943). In certain species of Prospaltella the male develops only as a primary parasitoid of moth eggs.
Many parasitoids are able to discriminate between parasitized and healthy hosts and thus avoid superparasitization. Flanders (1951) indicated that a spoor effect may be present (a special "marker" in some species). Simmonds (1943) indicated the existence of chemoreceptors on the ovipositor of I. canescens and Wylie (1965 thru' 1972) found the same in Nasonia vitripennis.
It was suggested by Dethier (1947) that in I. canescens, "Either the sensilla which are located on the shaft of each valvula subserve a chemoreceptor function, or the stimulating solutions diffuse through the general cuticle of the organ, or the solutions are advanced by capillarity up the egg tube formed by the oppressed surfaces of the valvulae to the region of the genital openings where they may act upon sensitive areas."
Narayanan & Chaudhuri (1954) believed that Stenobracon deesae (Cameron) could distinguish between parasitized and healthy hosts. They wrote, "It is probable that when a female Stenobracon inserts its ovipositor into a host to paralyze it before oviposition, she receives a stimulus from a healthy host which is different from that derived from a parasitized host."
The fact that a parasitoid has found a potential host within its respective habitat and has oviposited in or upon the same is no assurance that all criteria for maintaining a host-parasitoid relationship have been met. The host individual selected may prove unsuitable for parasitoid development. In other words, oviposition is no assurance of host suitability if the host individual proves to be resistant or otherwise unsuitable for parasitoid development.
A host may be unsuitable for (1) physical reasons (too small, too thick), (2) for nutritional reasons and (3) biological reasons: the host may be killed by the ovipositing female following host-feeding or mutilation. The host may move and dislodge externally attached parasitoid eggs or larvae. The host may molt and thus shed parasitoid eggs attached externally to the cast exuvium. Also, internally laid eggs and endoparasitoid larvae may be encapsulated by phagocytes. Phagocytes are blood cells that gravitate to and either ingest or surround foreign bodies that are introduced into the haemocoel of a host insect. The process is called phagocytosis.
Bess (1939) first recognized that oviposition by a parasitoid is not necessarily an index to host suitability, the attractiveness of the host being often independent of its suitability for parasitoid development.
Muldrew (1953) suggested that a once susceptible host population [that probably contained a few resistant individuals] may become totally resistant to parasitoid attack. In this case the larch sawfly host, Pristiphora erichsonii (Hartig), inhibited the embryonic development of its parasitoid Mesoleius tenthredinis Morley by encapsulation, with the deposition of phagocytic capsules around the embryos. Therefore, the non-susceptible host race displaced the susceptible host race. In some species encapsulation of diploid eggs and not haploid eggs occurs.
Evidence exists that formerly susceptible host populations may become resistant to parasitoid attack. Cases are also known where otherwise normal hosts are rendered unsuitable by the host plants on which the host develops.
The host plant may confer on the host insect a kind of immunity to parasitization (Flanders 1953, J. M. Smith 1957). Habrolepis rouxi Compere suffers very little mortality of its immature stages when attacking Aonidiella aurantii (Maskell) on grapefruit; however, when the scale is grown on sago palm, 100% mortality of immature H. rouxi occurs. Smith reported this same phenomenon with Comperiella bifasciata Howard.
In a slightly different context, there are unpublished observations by workers at the University of California, Riverside and the U. S. Department of Agriculture in Texas that citrus trees which have received treatments of DDT or other insecticides actually change their nutritional value to favor pest insect species thereon. Scale insects were stimulated to reproduce and grow at a faster rate. Parasitoids were also eliminated by the treatments so that the host's increase was unchecked for some time following a treatment. The so-called "DDT check method" to exclude the activity of natural enemies, therefore, may give distorted data on the actual value of the parasitoids and predators eliminated because the hosts are artificially stimulated.
In summary, host habitat finding is important to the success or failure of natural enemies in regulating their host populations. During host searching, parasitoids often search first for the environment frequented by the host. Odor associated with these habitats is usually the attracting force. Host visibility only aids the parasitoid in pinpointing an object which has already exerted an attraction. Many parasitic Hymenoptera will oviposit in any suitable insect located in the favored habitat, the host plant occasionally being more attractive to the parasitoid than the host itself. Honeydew produced by aphids and coccids also can attract parasitoids. Moisture in the form of dew is required by many parasitic species.
Locomotion of the parasitoid may determine the extent to which the host habitat is selected and frequented. Phytophagous hosts are sometimes rendered immune to successful parasitization by certain plants upon which they feed. The plant on which the host is feeding may affect host selection, fecundity and longevity of the parasitoid.
This fifth category in the host selection process was proposed by Bradleigh Vinson of Texas A. & M. University to account for cases in which parasitism changes the host physiologically, causing it to behave in a different manner (Vinson 1976). It does not have anything to do with "regulation" of host numbers.
Manner and Place of Oviposition
Obviously those species that oviposit merely in the vicinity of hosts or randomly within their host's general habitat are not exercising as much discrimination as those parasitoids in which host-selection behavior is developed to the degree where a specific host organ or location on a host serves as the oviposition site.
Many species of Diptera and a few parasitic Hymenoptera, oviposit in habitats frequented by their hosts, but apart from any host individuals that may be present. These parasitoids may lay their eggs more or less at random upon plant foliage or other plant parts, and host contact is made when those eggs are subsequently ingested by their plant-feeding hosts. The eggs of some Hymenoptera hatch into small, motile larvae which usually can live without food for long periods of time and which attach themselves to passing host individuals. Some dipterous parasitoids are viviparous with the eggs hatching within the parasitoid female that subsequently larviposit within the vicinity of, but apart from, their hosts.
The eggs of many species of dipterous and hymenopterous parasitoids are deposited on the host. The larvae, after hatching, variously feed either externally as ectoparasitoids or enter the host and develop as endoparasitoids. The eggs of such parasitoids may either be glued to the host integument or anchored in place by peg-like extensions of the chorion which penetrate the host's integument.
It can generally be said that hosts living in exposed situations, such as leaf-skeletonizing larvae, tend to be attacked by endoparasitoids; whereas, hosts living in protected situations, such as galls, tunnels, galleries, mines, or in puparia or cocoons, tend to be attacked by ectoparasitoids. It follows that parasitoids of exposed hosts generally oviposit within their hosts. These eggs may simply be thrust into the host's haemocoel and left to float free in the blood, or the eggs may be inserted into specific host organs.
Exercise 13.1--Discuss how the character of the host habitat may influence natural enemy activity. How could this knowledge be useful in (1) foreign exploration and (2) in evaluation of natural enemy activity?
Exercise 13.2--What are some characteristics of the habitat that attract or repel natural enemies?
Exercise 13.3--What are the processes in host selection?
Exercise 13.4--How may insecticide applications alter the host habitat?
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