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HABITAT, HOST-FINDING AND HOST ACCEPTANCE
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Characteristics of the Habitat Influence Natural Enemies |
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Host Food Affects Suitability for Parasitization |
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Habitat Diversity vs. Similarity Affects Population Stability |
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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. Host Finding 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). Parasitoids generally seem to be more attracted to higher
densities of the host and to certain patterns of host distribution (Legner 1967, 1969a). 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). Host Acceptance 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). Salt (1935) termed host acceptance a "Psychological Selection." Huffaker (Doutt
1959) suggested that it be called "Ethological
Selection." 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." Host Suitability 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. This same phenomenon was reported by Smith 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. Host Regulation 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? REFERENCES: [Additional references
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pretiosum (Hym.: Trichogrammatidae) under greenhouse conditions.
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A. P. 1962. Influence of host tree on abundance of Itoplectis conquisitor
(Say) (Hymenoptera: Ichneumonidae), a polyphagous parasite of the European
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haemolymph that induces oviposition in a parasitic insect. Nature (London)
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(Thomson) (Hymenoptera: Eucoilidae) through a kairomone produced by Drosophila
melanogaster. J. Chem. Ecol. 2: 125-36. Doutt,
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