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THE ROLE OF
PARASITOIDS, PREDATORS
AND PATHOGENS IN NATURAL
CONTROL
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Overview Thousands of species of phytophagous insects rarely, if
ever, manifest population epizootics that result in severe defoliation and
death of the host plant. This is generally true in natural, relatively
undisturbed ecosystems. However, in the highly artificial agroecosystems with
their monocultures of fields and orchards, competition between humans and
insects is often intense. Upsets sometimes result from insecticidal
application; other times from the lack of suitable imported natural enemies.
Most of all, they appear due to the complete artificiality of the
agroecosystem, or a condition that accentuates the potency of a native pest.
Examples may be found in nonresistant plants and in the apple maggot, Rhagoletis
pomonella (Walsh). It may seem almost an oversimplification to suggest that
the relatively homeostatic nature of the populations of potential pest
insects is due solely to the density dependent forces of effective natural
enemies. However, evidence from four main sources suggests just that. In the
first case, the many successful examples of biological control of pest
insects by importation and release of natural enemies supports the density
dependent hypothesis. Secondly, pest outbreaks can be produced when natural
enemies are excluded by pesticides or other experimental means. Thirdly,
Varley & Gradwell (1963) gave strong evidence from long term
determinations of the complex interrelationships of insect populations.
Finally, there are the often overlooked accidental cases of detrimental
biological control, which support the density dependent hypothesis, such as
Dutch elm disease, Chestnut blight, the decline of Bermuda cedars; and of
course all cases of invaded pests that cause a drop in the average density of
a plant or animal population. Modern population theory has begun to suggest that balance is not a normal situation for living
populations, but rather that great instability
is demonstrated from year to year. This is believed to be a reflection of constant
changes in weather and climate. There is no argument with this theory, but
there has to be a distinction between instability at high population
densities versus instability at low densities, the latter often
reflecting less than 1% of what would be considered a high population density
when natural enemies are effective. There are also some examples where population stability
does not appear related to the activity of natural enemies. For example, the
whole genus Matsucoccus, scale insects attacking conifers, is not
known to possess any parasitoids, and no really effective predators have been
found. Many natural enemy populations possess behavioral
adaptations that are required to maintain pest populations at non-economic
densities. Some of these are: they coexist in time and space, they possess a
high reproductive response to slight increases in host density, and some show
seasonal reproductivity equal to or greater than that of the pest population.
When host scarcity causes a reversal in the relative rate of natural enemy
increase, the efficiency of host-finding by the individual natural enemy
tends to increase. Undisturbed biomes offer good examples of stability. in the
Chaparral biome, the brush plant species are fed on by mealybugs, scarabs,
weevils, wood borers, scales, gall-forming midges, etc. The mealybugs are
attacked by parasitoids and predators; one gall midge has 12 species of
parasitoids. Coyote brush has 54 species of primary plant feeders which in
turn are attacked by 23 species of predators and 62 species of parasitoids.
The interinvolvements among constituents of this biome are believed to
produce the observed stability. In the Sagebrush, Grassland & Range biomes, over 200 species of grasshoppers, Mormon crickets, soft
scales, moths, tent caterpillars, aphids, scarabs, wireworms, etc. about on
Great basin plants. The factors that either limit or regulate the abundance
of these insects are not definitely known, but hyperparasitoids attacking
parasitoids and predators of the phytophagous insects have been implicated in
outbreaks. The Oak Woodland biome of California sustains 35 species of microlepidoptera that
feed only on live oaks. The complex on all oak species is much larger.
Numerous parasitoids are associated with these Lepidoptera, and outbreaks are
rare. The California oakworm, Phryganidia californica
Packard, cyclically defoliates the live oak in northern California, despite
parasitoids and pathogens. This is thought to be due to a relatively
"recent" increase in the range of the host to the north. Southern
California oaks are not as severely affected, presumably because of the
longer period of residence of the pest in the south, and the greater number
of acquired natural enemies. There is no precise explanation for the stable
low density balances at which another group of insects, the tent
caterpillars, occur in the Oak Woodland biome, in view of the fact that their
natural enemies are strangely not host specific. Over 100 important forest pests occur in the Coniferous Forest
biome of North America;
but, the total potential pests is much greater. Most investigations in the
coniferous forest are made when pests are in an epizootic phase rather than
endemic phase, because economic thresholds are quite high. This may explain
why the status of natural enemies as regulatory agents is generally not known
even though most workers accept their importance in the ecosystem. The pests
in this biome are primarily beetles, caterpillars, scale insects, sawflies
and gallflies. Foresters generally strive to obtain natural balances between
destructive species and their predators even in the absence of scientific
support for the value of any natural enemy species. Most foresters seem
convinced of the importance of natural enemies by such indirect evidence as
the observation that hyperparasitoids are implicated in causing outbreaks of
the lodgepole pine needle miner, and the upsets caused by malathion to
populations of the white pine needle scale. The major lakes that occur in several biomes of East Africa contain many
endemic fish species, especially cichlids, which interact as herbivores,
carnivores, and scavengers to produce wonderfully stable, unpolluted, clear
waters with a high fish biomass. Agroecosystems, although potentially less stable than natural biomes,
still offer the best evidence for the importance of natural control. The
relative simplicity and the lesser number of species living in a crop
monoculture, permits easier detection and more fruitful analysis of the
interrelationships between pest and natural enemies. Agroecosystems contain
examples of crops that rarely exhibit pest outbreaks as well as ones that
show frequent epizootics. Variations of the degree of ecological stability are often
correlated with crop longevity and "exoticness." The agroecosystems
which appear the most stable in regards to the frequency of pest outbreaks
are tree fruit and nut crops, followed by vineyards and perennial field
crops. The least stable are the annual vegetable and field crops. Another part of the agroecosystem, the irrigation system,
can produce a high fish biomass when a balance exists between effective
herbivores and predatory fish (e.g., Sarotherodon, Tilapia,
bass and catfish). The dairy and poultry agroecosystems also produce great
quantities of desirable fertilizer, if management is properly conducted. The
problem here is to favor decomposition while minimizing noxious fly
densities. Outbreaks of pests have been known to be caused by
pesticides in all biomes, especially the agroecosystem. When an insect rises
to economic prominence through pesticide action on its natural enemies, we
call it a pest resurgence. Resurgence
invariably involves some form of physiological or behavioral resistance to
the pesticide. Pest upsets can subside if resistance to the pesticide
develops in the natural enemy population, as has been shown with certain
parasitoids and predatory mites. Measuring the
Force of Natural Control There are still "ecologists" who consider that natural
enemies rarely, if ever, regulate prey populations: climate is thought
to be the key factor. A distinction must be made between the mechanisms
involved in regulation of prey populations by natural enemies and the end
results; i.e., the fact and degree of control or regulation by enemies.
DeBach (1971) has listed several requirements for evaluating natural control
forces. The size of the study area is considered to be of prime
importance: it must be large enough to exclude outside influences that would
adversely affect natural enemies. Cultural practices in a field must be
typical of the normal culture situation. A sufficient period of time must be
given to a comparison, which invariably involves three years or more.
Finally, statistical information on production and quality is also essential. The methods for measuring the force of natural control
involve three techniques which are (1) addition of natural enemies where they
do not exist, (2) exclusion of natural enemies, and (3) interference with
natural enemies. A good example of the addition method is given by Huffaker
and Kennett (1966) working on olive scale, Parlatoria oleae
(Colvee). In their experiment, 10 olive groves were chosen in which Aphytis
maculicornis (Masi) was added; another 10 groves received additionally
Coccophagoides utilis Doutt. The average density of the olive
scale was shown to be lower in the groves with two parasitoid species
present. Other good examples of the addition method are found in the
photographs taken before and after introduction of phytophagous beetles to
fields infested with Klamath weed (DeBach et al. 1964), in the reduction of
aquatic weeds and mosquito breeding habitats by herbivorous fish in aquatic
habitats (Legner et al. 1983), and in the reduction of Opuntia stands following
the importation of Dactylopius spp. on Santa Cruz island in California
(Goeden et al. 1967). Exclusion has involved the use of wire cages, electric
barriers, spatial isolation of host plant and pest away from natural enemies,
chemical treatment; but by far the most reliable exclusion method employed to
date for terrestrial insects was mechanical, involving hand-removal of
natural enemies (Fleschner et al. 1955). These were removed by hand on a 24-h
basis, for a period of 84 days. Natural enemy-free plots consisted of
individual branches or portions of a tree, which were then compared to the
rest of the tree that allowed normal natural enemy activity. Biological
control was shown to be responsible for the normally low pest population
densities in the experimental grove. The study included five potential pests
in diverse taxonomic groups: omnivorous
looper, Sabulodes caberate Girault 6-spotted mite, Eotetranychus
sexmaculatus (Riley) long-tailed
mealybug, Pseudococcus adonidum (L.) avocado brown
mite, Oligonychus punicae (Hirst) latania scale, Hemiberlesia
lataniae (Sign) Exclusion has also been used effectively to eliminate
herbivorous cichlid fish, Tilapia and Sarotherodon, from portions
of irrigation canals and measuring subsequent weed growth, dead weed
accumulation, and Culex tarsalis population density increases
(Legner 1986 , Legner et al. 1983 ). With the interference technique, natural enemies are not
completely excluded, but their performance is hindered. The biological check method employs ants to
"interfere" with the performance of natural enemies. The trap method, a variant of the insecticidal check
method, involves a central untreated plot surrounded by a chemically poisoned
zone which acts to kill natural enemies as they disperse to or from the
central plot. After a period of time, natural enemies may become greatly
decimated in the untreated (control) plot, thus permitting differential
increase of pests which previously had been held down by natural enemies. The trap method has been used with the cottony-cushion
scale (DeBach & Bartlett 1951), and with the citrus mealybug (Bartlett
1957). In the latter example, it was shown that certain natural enemies were
severely inhibited, and others very little. It was also observed that during
one month of the two seasons study, the natural controls had little effect in
keeping the pest population down. Another interference technique involves the addition of
metallic ions to Culex tarsalis breeding grounds, which
eliminates predatory hydra, and can result in mosquito epizootics. It is advisable that any material used in exclusion or
interference should have minimal or no effect on the pest's fecundity. It is
also advisable to use an additional form of a check method that does not
affect fecundity, as a desirable safeguard and check on the first method. In
other words, two or three methods are better than one. (See Luck et al. 1988
for a review of experimental methods). Nature of
Parasitoidism Parasitoids are organisms which live in, on or at the
expense of another organism. Parasitism may be viewed as a form of symbiosis
involving at least two unrelated species. One symbiont (the parasitoid) lives
at the expense of the other symbiont (the host). The parasitoid provides no
benefit to the host and eventually destroys it. Parasitism is complex and the
animals which participate in the lifestyle function as primary, secondary,
facultative, obligatory, external or internal
parasitoids. Insects which develop as parasitoids have been called Protelean Parasites (Askew 1971) in contrast to
other groups of organisms which develop parasitically. The term Parasitoid
was proposed for insects which develop in this manner (Reuter 1913), and it
has gained widespread acceptance among ecologically and ethologically
oriented workers. The term parasitoid may be viewed as a transitional
condition between predation and parasitism in the classical sense. The
parasitoid larva is parasitic during the early stages and epistatic during
later development. Attributes of Protelean parasitoids which distinguish them
from other parasitic animals are (1) parasitical behavior is expressed only
during the larval stage, (2) the adult stage is free living (3) the
parasitoid larva typically kills and consumes one host, (4) body size of the
parasitoid approximates that of the host, (5) the parasitoid life cycle is
relatively simple, (6) the parasitoid shares relatively close taxonomic
affinity with hosts and (7) Protelean parasitoids display reproductive
capacity between so-called true parasites and free-living forms. Occurrence of
Parasitoidism in Insects Insect parasitism appears focused on several orders of
Holometabola, including Hymenoptera, Diptera, Strepsiptera, Coleoptera and
Lepidoptera. Hymenoptera are the most important group of insects from the
viewpoint of applied biological control. Hence, most of the following
discussion involves this order. Presently the Hymenoptera contain about
125,000 nominal species, but is in actuality substantially larger, based on
the large number of species awaiting description (Gordh et al. 1999). Ecologically
the Hymenoptera are exceeding diverse. Features distinguishing Hymenoptera include mandibulate
mouthparts in larva and adult, adult with four membranous wings, forewing
largest and connected to the hindwing with hook-like hamuli which are engaged
only during flight, and females display an appendicular ovipositor. The order
includes the suborders Symphyta (Chalastogastra = sawflies, woodwasps) and
Apocrita (Clistogastra = bees, wasps, ants). In biological control the Symphyta assume a minor position
because nearly all species are phytophagous. Parasitism is restricted to one
family, the Orussidae, which is cosmopolitan in distribution and contains
about 70 species which apparently develop as external parasitoids of
Xylophagous Coleoptera. One species of Orussus has been used with some
effectiveness in applied biological control. The Apocrita are numerically more abundant and
impact to a significant extent the populations of other insects.
Anatomically, the Apocrita are characterized by adult without closed anal
cells in the wings, the first abdominal segment (propodeum) has become
functionally incorporated into the thoracic region and separated from the
remainder of the abdomen by a constricted abdominal second segment (the
petiole). Larval Apocrita sometimes undergo hypermetamorphosis, the head
capsule and antennae are present or absent, the body is apodous, the midgut
and hindgut typically are not connected during the feeding period, and
excretion is confined to the prepupal or late larval stage. The Apocrita are
sometimes subdivided into two infraorders, the Parasitica and Aculeata. Several aspects of adult anatomy have contributed
significantly to the evolutionary success of apocritous Hymenoptera. Most
important are the appendicular ovipositor, the constricted waist (petiole),
elaboration of accessory gland secretions, and provisioning for larval
progeny. Collectively these features and attributes have made parasitism a
highly successful lifestyle and consequently focused attention on parasitic
Hymenoptera as an important group in applied biological control (Gordh et al.
1999). The importance
of each attribute is as follows: 1. Appendicular Ovipositor.--The Symphyta and Parasitica are among the few Holometabola
with a lepismatid-like ovipositor. The functional significance of this
tubular egg laying structure as an adaptation for parasitism cannot be
overemphasized. This elongated egg-laying tube enables precise placement of
the egg in habitats or places that other insects cannot reach without
elaborate anatomical modifications involving other regions of the body. 2. Accessory Gland Secretions.--Secretions associated with the reproductive system are
common within the Insecta, and they serve many purposes, including
lubrication for the egg, a substrate for fungal growth, induce gall
formation, and venoms for the subduction of prey and hosts. The modification
of glandular secretions for use against potential hosts must be interpreted
as a cardinal landmark in the evolution of parasitism by Hymenoptera. 3. Constricted Waist
(Petiolate Abdomen).--The
Aculeata and Parasitica display a constriction between the thorax and
abdomen. The constriction takes the form of a small, ring-like second
abdominal segment, termed the petiole. This constriction permits abdominal
flexibility which enables the adult to sting hosts and prey into paralysis
and also permits the egg to be deposited in confined spaces. 4. Progeny Provisioning.--Ancestral
Hymenoptera presumably displayed a phytophagous larval stage. This is seen
today in Symphytan females which place their egg in plant tissue. The
behavioral transition from placing an egg in plant tissue to the present
condition in which an apocritan female places an egg in or on a host must
have evolved early in the evolution of parasitic habits. Taxonomic Groups
Important to Biological Control Ichneumonoidea.--This
superfamily contains about 28,000 nominal species, assigned to six or eight
families. Anatomically, Ichneumonoidea are distinguished from other groups by
a long antenna with more than 13 segments, the antenna is not geniculate, a
trochantellus (second trochanter) is attached to the femur, and the
ovipositor originates anterior of gastral apex. Principal families include
the Ichneumonidae and Braconidae. The Ichneumonidae is the largest family of parasitic Hymenoptera, containing
about 25 subfamilies, 1,250 genera and 20,000 nominal species. It has a
fossil record extending into the Cretaceous (Taimyrian amber), which demonstrates
that the family is among the oldest among the Parasitica. The host spectrum
of Ichneumonidae is broad, but the focus is clearly upon Holometabola.
Ichneumonids do not attack Mecoptera, Siphonaptera or Strepsiptera. They
prefer larvae, pupae, and cocoons, and the adults are often associated with
moist habitats and extensive groundcover. The Braconidae are related to Ichneumonidae. Numerically the braconids
are also a large family, including about 20 subfamilies and 8,000 nominal
species. All species are primary parasitoids, but host associations have not
been established for most species. Based on current information, braconids
display an exceptionally broad host range, mostly Holometabola, but do not
attack Trichoptera, Mecoptera or Siphonaptera. One subfamily, the Aphidiinae,
contains 32 genera and about 300 species, all of which are primary, internal
parasitoids of aphids. Aphidiids are generally regarded as important natural
enemies of aphids, but little objective data demonstrates their effectiveness.
Aphidiids are sometimes a distinct family considered near the Euphorinae. Ceraphronoidea.--This
superfamily consists of two extant families, Ceraphronidae and Megaspilidae,
which early classifications placed in the Proctotrupoidea. Adults are curious
in that they display two tibial spurs on the foreleg. Ceraphronidae
are very small to small sized, dark bodied, nonmetallic wasps. Details of
their biology are very poorly studied, but species apparently develop as
endoparasitoids of larval Diptera such as Cecidomyiidae. Pupation occurs
inside the mature larval integument. Some species attack thrips, Lepidoptera
(larva & pupa), Chrysopidae and Coniopterygidae. Megaspilidae are
anatomically similar, but develop as ectoparasitoids of diverse taxa. They are
hyperparasitoids of aphidiids on Aphididae, or primary parasitoids of
Coccidae, Mecoptera, Neuroptera and Diptera. Some myrmecophiles probably
attack Diptera. Evanioidea.--This
superfamily is also one of questionable development and composition. Included
families have been placed among the Ichneumonoidea and Proctotrupoidea in
some classifications. Anatomically they are characterized by a gastral
petiole attached high on the propodeum and functional spiracles on the
gastral tergum VIII. Three included families are the Evaniidae, Aulacidae
and Gasteruptiidae. The Evaniidae consist of about 400 widespread, predominantly tropical
species which under domestic conditions are typically encountered around
drains and on windows. All species apparently are endoparasitoids of
cockroach oothecae. As such, evaniids are potentially important in biological
control of cockroach pests, particularly of stored products. The Aulacidae are also
cosmopolitan with about 15 described species. Species are solitary egg-larva
endoparasitoids of wood boring Coleoptera and Hymenoptera. The female
oviposits in the host egg but parasitoid development is arrested until the
host completes larval development. Then the aulacid larva consumes the mature
host larva, emerges from the host, spins a cocoon and pupates. The Gasteruptiidae
are widespread and contain about 500 species. Adults visit flowers and
rotting logs in search of hosts which include aculeate Hymenoptera (bees and
wasps). The family is interesting because it demonstrates transitional
behavior between cleptoparasitism and ectoparasitism. In one condition adults
lay eggs in the host's cell where the parasitoid larva attacks the host
larva. In another condition adults lay eggs in the host cell and the
parasitoid larva consumes the host and contents of the host cell. Third
instar larvae void their excrement and spin week cocoons . Mature larvae
overwinter, with pupation occurring the following year. Trigonaloidea.--This
represents an ancestral lineage near the hypothetical base of the Parasitic
and Apocrita. Trigonalids have been placed in many superfamilies. Included
are one extant family, the cosmopolitan Trigonalidae and one fossil
family, the Ichneumonidae. The Trigonalidae are cosmopolitan and contain about 70
nominal species. They have been placed in Ichneumonidae, Proctotrupoidea and
among the Aculeata. Most species are hyperparasitoids of larval Hymenoptera
and Tachinidae; some develop as primary endoparasitoids on Symphyta in
Australia. Adult females lay eggs on vegetation, frequently several thousand
during one ovipositional episode. The trigonalid eggs are consumed by larval
Symphyta or Lepidoptera, the egg hatches and the parasitoid larva penetrates
the host's haemocoel. Chalcidoidea.--One
of the largest and most important superfamilies of parasitic Hymenoptera, the
Chalcidoidea is cosmopolitan in distribution and contains more than 17,000
described species. The group is ancient, with a fossil record extending into
the Cretaceous (Canadian & Taimyrian amber). Interestingly, the
Proctotrupoidea are more abundant in the oldest amber deposits. Biologically
they are the most diverse of Apocrita. Species feed as primary, secondary
parasitoids, inquilines, gall formers and develop as endoparasitoids,
ectoparasitoids, solitary or gregarious. Chalcidoids attack all stages except
the adult and the host spectrum extends from spiders and ticks to Aculeate
Hymenoptera. They are among the most important group for applied biological
control. Aphelinidae
are a moderately large, cosmopolitan family of 45 genera and 1,00 nominal
species. Typically very small (0.5 - 1.5 mm long) with body variable in
coloration but very rarely metallic. Biologically they are diverse, primary
and secondary ectoparasitoids and endoparasitoids. Some males are adelphoparasitoids.
They attack predominantly sternorrhynchous Homoptera. Several species are
important in biological control of scale insects and whiteflies. Chalcididae
are a moderate sized, cosmopolitan family of 40 genera and 1,500 species. The
body is relatively large (to 10 mm), and robust, often sculptured, and non
metallic. All species are parasitic, primary and hyperparasitoids of
Holometabola, particularly Lepidoptera and to a lesser extent Diptera,
Coleoptera and other Hymenoptera. They are hyperparasitic on Tachinidae and
parasitic Hymenoptera. Development is typically as solitary endoparasitoids
of last instar larvae and pupae. The genus Brachymeria os of some use
in biological control. Elasmidae are a moderately
small cosmopolitan family of 1-2 genera and 200 nominal species which are
sometimes placed in the Eulophidae. They are typically small bodied (1.5-3.0
mm), never metallic. Most species are primary, gregarious parasitoids of
Lepidoptera; a few hyperparasitic species attack Braconidae and Ichneumonidae
in cocoons and Vespidae that provision cells with Lepidoptera. Females
paralyze the host with venom. The number of eggs deposited on a host is
influenced by host size. First instar larvae are hymenoptriform and
segmented, with thoracic pseudopodia (locomotory). There are four pairs of
spiracles on the first instar; the last instar has nine pairs of spiracles. Encyrtidae
are a cosmopolitan, large family (ca. 500 genera, 3,000 nominal species)
family. The body is robust, typically 0.75 - 5.0 mm long, often metallic or
dark colored. All species are endoparasitic and some hyperparasitic. The host
spectrum is broad, but most species are associated with Homoptera.
Polyembryony is known in some species. They are believed to be related to
Tanaostigmatidae and Eupelmidae. They are important in the biological control
of mealybugs, scale insects and synanthropic Diptera (genus Tachinaephagus). Euchartidae
are a cosmopolitan, moderately small (ca. 45 genera, 350 species) family.
Species are moderately large bodied (to 10 mm long) and frequently metallic
colored. They are typified by a complex biology with heteromorphosis. Larvae
develop as ectoparasitoids or endoparasitoids of ant larvae. Males sometimes
swarm over the crown of ant nests. Adult females are proovigenic, sometimes
with several thousand eggs per female. They lay eggs on vegetation, which
hatch into planidial first instar larvae. The planidium has 12 body segments
and a caudal sucker, which are transported to ant nests by workers. The ant
prepupa serves as host and pupation is inside a cocoon or exposed in the
brood chamber. Eulophidae
are a large cosmopolitan family (ca. 325 genera and 3,100 nominal species).
Characteristically they are small to very small (1-6 mm), often weakly
sclerotized. The coloration is variable, usually dark or metallic. They are
predominantly primary parasitoids with some hyperparasitoids and a few
phytophagous species. They are solitary or gregarious in development as
endoparasitoids or ectoparasitoids. There is a broad host spectrum including
all immature stages attacked. They frequently attack concealed Lepidoptera
and Diptera. Some larvae behave as predators. They are important in some
biological control programs involving sawflies on pine, and leaf miners. Eupelmidae
ar a cosmopolitan, moderately sized family (ca. 60 genera, 750 species). The
female body is elongate, frequently metallic and often "U"-shaped
in dried specimens. The family is predominantly parasitic with some
facultatively hyperparasitic species. Development is typically solitary with
larvae feeding ectoparasitically or endoparasitically. There is a broad host
spectrum with all progenitive strategies demonstrated, and some larvae feed
as predators of eggs and larvae. They are related to Encyrtidae and Tanaostigmatidae. Eurytomidae
are a moderately large, cosmopolitan family (ca. 75 genera, 1,100 species).
The body is 3-15 mm long, robust, dark, non-metallic. The head and thorax are
frequently coarsely punctate. Development is typically solitary, rarely
gregarious, as ectoparasitoids which demonstrate larval combat. Some species
are endoparasitic on cecidogenic insects. Some eggs are spinose, with
micropylar projections. The first instar larva is hymenopteriform, often with
five pairs of spiracles. The host spectrum and feeding strategies are
diverse. They attack Coleoptera, Hymenoptera, Diptera, Lepidoptera. Some are
phytophagous in galls, forming the galls themselves. Some are egg predators
and parasitoids of phytophages in seeds, stems and galls. Leucospidae
are small and widespread, consisting of about 150 species. The family is
predominantly tropical and subtropical. They are apparently related to the
Chalcididae. They are primary parasitoids of solitary wasps and bees. Mymaridae are a cosmopolitan,
moderately large family (ca. 95 genera, 1,200 nominal species), whose members
are small to minute, nonmetallic colored. Mymarids display an extensive
fossil record in the Cretaceous (90-110 MYBP), which suggests they are an
ancient group which radiated early in the history of Apocrita. All species
develop as endoparasitoids of insect eggs. Typically mymarids are solitary,
rarely gregarious. Ecologically they prefer host eggs in concealed habitats
such as in plant tissue, under bark and in soil. They are not host specific
but seem to prefer Auchenorrhyncha (Homoptera). Some species have aquatic
females which parasitize submerged Dytiscidae eggs. Pupation occurs inside
the host egg. Some species have been successful agents in biological control
programs. Mymarommatidae
are a very small, widespread family (1 genus, ca. 20 species). The body is
minute, nonmetallic with exodont mandibles. Biology of this family is
unknown. A few species have been recovered from Cretaceous amber, thereby
establishing the lineage as ancient. The family is sometimes placed in a
separate superfamily and is regarded as the sister group of the Chalcidoidea. Ormyridae are cosmopolitan
with only three genera and 60 species. They are sometimes placed in Torymidae
or Pteromalidae. The body is 1-7 mm long, robust, metallic, strongly
sclerotized and sculptured. Species parasitize gall-forming Diptera,
Cynipidae and Eurytomidae in seeds. Perilampidae
are small, cosmopolitan (ca. 25 genera, 200 species). Fossils are from the
Lower Oligocene. Their classification is problematical; they are near
Eucharitidae or Chrysolampinae, a subfamily of Pteromalidae. The body is
robust, moderately large, metallic. Their biology is poorly understood;
apparently primary and secondary parasitic habits, primary parasitoids
attacking xylophagous beetles. Hyperparasitoids attack braconids,
ichneumonids, tachinids on Symphyta and Lepidoptera larvae. Pteromalidae
are among the largest families of chalcidoids (ca. 600 genera, 3,100
species). The body is 1-7 mm long and usually metallic. Biological diverse,
solitary or gregarious, typically ectoparasitoids. The egg shape and size is
highly variable, there being reports of up to 700 eggs/female; sometimes
spiculate. First instar larvae are hymenopteriform with 13 segments. The head
and mandibles are sometimes large. Ectoparasitic forms have an open
respiratory system, while endoparasitic forms have a closed system. Their
feeding spectrum is very diverse: predominantly parasitic of Holometabola,
attacking concealed host larvae and pupae in stems, leaf mines, galls,
organic wastes and similar habitats. Some are larval-pupal parasitoids and
some are predatory on cecidomyiid larvae and coccoid and delphacid eggs. Gall
formers occur where they also feed on gall tissue. Signiphoridae
are a small (ca. 80 species) cosmopolitan family of parasitic Hymenoptera.
Adults are small to minute in size, with a dorsoventrally compressed body.
They are primary and secondary parasitoids of whiteflies, scale insects,
Diptera puparia and the primary parasitoids which attack these insects. Tanaostigmatidae
is a small, widespread family of about 80 species. All are apparently gall
formers on Fabacae, Myrtaceae, Rhamnaceae, Polygonaceae and allied families.
Galls are formed on most plant parts and are typically monothalamous. The
ovarian egg is encyrtiform, a character shared with the Encyrtidae. Tetracampidae
is an Old World family of about 15 genera and 40 nominal species. It is
probably related to Pteromalidae and Eulophidae. One species has been
introduced into the Nearctic. Their biology is poorly known, but seem to be
primary parasitoids of Coleoptera and Hymenoptera eggs and of Diptera larvae
mining leaves and twigs. Subfamilies include Mongolocampinae,
Platynocheilinae and Tetracampinae. Torymidae is a
cosmopolitan, moderately large (ca. 100 genera, 1,500 species) family of
moderate size (1-8 mm long), typically metallic blue-green. They possess a
diverse biology: phytophagy to hyperparasitism. Most larvae feed externally
as parasitoids. The egg shape is variable, typically sausage-like. Larvae are
hymenopteriform. Parasitic species often have spines; phytophagous species
are spineless. Developmental strategies include phytophagous gall formers,
phytophagous feeding on seed endosperm, primary ectoparasitoids of gall
formers or ectoparasitoids of gall formers then phytophagous. Some
ectoparasitoids of aculeate Hymenoptera and Coleoptera are known. Trichogrammatidae
is a moderate sized (ca. 75 genera, 600 nominal species), cosmopolitan family
characterized by a minute, weakly sclerotized body lacking metallic
coloration and without ornate, bold microsculpture. Biologically they are
primary, solitary or gregarious endoparasitoids of host eggs. They exhibit
hypermetamorphic larval development with first instars sacciform or
mymariform, and last instars are segmented, robust and without spines.
Trichogrammatids display a broad host spectrum to include principal orders of
Holometabola, Hemiptera and Thysanoptera. They are extensively used in biological
control programs. Unusual biological features include phoresy on Tetigoniidae
and Nymphalidae. The genera Prestwichia and Hydrophilita
parasitize submerged eggs, and representative taxa are among the smallest
insects (Megaphragma ca. 0.20 mm long). Proctotrupoidea.-- are moderately
sized and cosmopolitan with about 2,000 nominal species. They have a fossil
record datable to the Jurassic (two extant families). All species are primary
parasitoids and superficially resemble Chalcidoidea in that both groups have
small body size and reduced wing venation. Cynipoidea.--Fossil
Cynipoidea are found in Cretaceous amber (Taimyr and Canadian).
Morphologically and biologically they are near Diapriidae, and apparently
branched early from generalized parasitic Hymenoptera. Nordlander believes
Cynipoidea were primitively parasitic. Includes a group with mixed biology,
about 30% are phytophagous; other groups are predominantly parasitic. General Ecology Parasitic insects display a prodigous array of progenitive
strategies. Basically parasitic insects may develop internally
(endoparasitoids), externally (ectoparasitoids) or they may develop initially
as internal parasitoids and complete development externally. Beyond this
basic architecture for parasitism there are numerous variations on themes
which are influenced by ecological habitat, adult female morphology,
oviposition behavior, host taxa, host biology and numerous other factors, as
will be treated in some detail in coming sections. The term Idiobiont has been
proposed for protelean parasitoids which kill, permanently impair or paralyze
their hosts after oviposition and thereby prevent further development of the
hosts. Typically, idiobionts are ectoparasitoids which attack hosts in
concealed situations and which express a broad host spectrum (generalists). Koinobiont has been proposed for protelean
parasitoids which do not kill, permanently impair or paralyze their hosts
after oviposition and thereby do not prevent further development. They are
typically endoparasitic and attack hosts in exposed situations, thereby
demonstrating a limited host range (specialists). Price (1977) discussed
aspects of the evolutionary biology of parasitic insects. Reproductive Strategies Solitary
parasitism is a condition in which a parasitoid larva completes
development in a one to one relationship with its host. Supernumerary
parasitoid eggs or larvae are eliminated. In contrast, gregarious
parasitism involves the
development of many individuals on one host. Host
discrimination is the ability of a female parasitoid to determine whether
a potential host has been parasitized, and to reject or accept the host as a
site for oviposition based on that determination. The phenomenon is
widespread among parasitic Hymenoptera, and aspects of its analysis have been
discussed by van Lenteren et al. (1978). Multiple parasitism is the oviposition in or on a host by more than one species
of parasitoid. Facultative multiple parasitism is the periodic association of
more than one species of parasitoid on a host simultaneously. Obligatory
multiple parasitism is a very rarely encountered phenomenon, and one
whose functional significance is not clearly established. Superparasitism, a phenomenon common to parasitic Hymenoptera, has been
defined in several ways: (1) a female ovipositing more eggs on or in a host
than can hatch with successful development to maturity; (2) the oviposition
on or in a host which had previously been parasitized by a conspecific
female; (3) development on one host by more individual larvae than can
survive to maturity irrespective of conspecificity. Each definition views the
phenomenon in a different way, with disparate effects on the fitness of
ovipositing females. Aspects of superparasitism involving individual
reproductive effort versus superparasitism by Trichogramma evanescens
Westwood conspecifics have been considered by Dijken & Waage (1987). Definitions and impact of fitness notwithstanding, the
phenomenon is so widespread in the Parasitica that one must conclude that it
probably has been independently encountered in many lineages. Intimately
associated with the phenomenon of superparasitism is host discrimination,
or the ability of female parasitoids to distinguish between hosts which have
been parasitized and those which have not been parasitized. Aspects of host
discrimination and superparasitization have been considered by Bakker et al.
(1985). Apparent from many studies is the general aversion to
superparasitism expressed by female parasitoids ready to oviposit.
Conventional wisdom views avoidance of superparasitism to conserve parasitoid
eggs and promote increased efficiency in searching for hosts. From the
viewpoint of applied biological control, superparasitism is regarded as an
important consideration, and mathematical models have been developed to
address parasitoid distribution and the avoidance of superparasitism (Bakker
et al. 1972, Rogers 1975, Griffiths 1977, Narendran 1985). Hyperparasitism represents a progenitive strategy in which individuals of
one species behave as parasitoids in relation to individuals of another
species which is itself developing as a parasitoid of a free living organism.
The phenomenon has been reviewed by Gordh (1981) and Sullivan (1987).
Beddington & Hammond (1977) developed a mathematical model for a
host-parasitoid-hyperparasitoid system in such a way as to analyze the
implications of hyperparasitism for biological control. Within the Insecta hyperparasitism seems restricted to
Hymenoptera, Coleoptera and Diptera (Gordh 1981). Hyperparasitism seems
inconsequential in the Coleoptera (Cleridae, Rhipiphoridae) and Diptera
(Bombyliidae, Conopidae), but reaches elaborate development in the parasitic
Hymenoptera. The extensive literature on parasitism in the Hymenoptera
has shown that hyperparasitic development takes many forms of expression
including facultative
hyperparasitism, obligatory
hyperparasitism, adelphoparasitism and tertiary
hyperparasitism. Facultative hyperparasitism is a form in which the immature hyperparasitoid can
complete feeding and development as a primary parasitoid or use a primary
parasitoid as a host. Obligatory hyperparasitism is a form in which
the immature hyperparasitoid must complete feeding and development using a
primary parasitoid as host. Although details are incomplete regarding the
biology of many hyperparasitoids, it seems the phenomenon has been derived
independently several times because it is found in many distantly related
lineages. Adelphoparasitism appears
restricted to one family of parasitic Hymenoptera (Aphelinidae). In
adelphoparasitism the larval male develops as a hyperparasitoid of a
conspecific female larva which acts as an endoparasitoid of Homoptera.
Several genera of Aphelinidae demonstrate this form of development. Tertiary
hyperparasitism represents a form of hyperparasitism in which hyperparasitic
individuals attack one another. Conceptually tertiary hyperparasitism has
been divided into interspecific tertiary hyperparasitism (allohyperparasitism)
(Sullivan 1972, Matejko & Sullivan 1984) and intraspecific tertiary
hyperparasitism (autohyperparasitism) (Bennett & Sullivan 1978, Levine
& Sullivan 1983). Both have been studied in the laboratory on
hyperparasitoids of aphids. From a biological viewpoint, tertiary
hyperparasitism is a precarious form of development which has rarely been
documented in the field. It seems likely to arise from intensive competition,
and its significance may be restricted to the laboratory, or an unusual phenomenon
best exemplified in aphid parasitoids. Percent Parasitization Simmonds (1948) discussed the difficulties in determining
by means of field samples the true value of parasitic control. A percent parasitism
figure has little real value in population studies unless it is closely
associated with real host densities. For example, some of the highest levels
of parasitism of synanthropic Diptera are associated with relatively low host
densities (Legner 1971). Spatial density samples of hosts may be obtained by
sampling known quantities of habitat (Legner & Olton 1971, Legner et al. 1980). Some of these difficulties are illustrated in the appraisal
of the true role of parasitic insects in the natural control of synanthropic
Diptera (Legner 1983). Different species of synanthropic Diptera have different
favored habitats as exemplified by the oviposition preferences of the face
fly, Musca autumnalis DeGeer, and horn fly, Haematobia irritans
(L.) in field dung of cattle versus the barnyard accumulated excrement
habitat which is sought out by the common house fly, Musca domestica
L., stable fly, Stomoxys calcitrans (L.), and the poultry fly, Fannia
canicularis (L.). Because their breeding habitats are so different
(Snowball 1941), these two groups of Diptera are usually assigned to
different categories of synanthropy (Legner et al. 1974, Povolny 1971). For each category of host synanthropy, there are also
different groups of associated natural enemies (Legner et al. 1974). Predatory arthropods
appear to be of principal importance in the natural regulation of Diptera
breeding in isolated deposits of cattle dung in pastures (Hammer 1941, Legner
1978, Mohr 1943,
Poorbaugh et al. 1968), while both predatory and parasitic arthropods
interact to regulate populations of Diptera breeding in accumulated animal
wastes and garbage (Legner 1971; Legner & Olton 1970, 1971; Legner et
al. 1974, 1975). Although
some natural enemy species overlap into both the pasture and accumulated dung
habitats, there are many species which are mostly confined to either one or
the other habitat (Legner & Olton 1970, Poorbaugh et al. 1968). Parasitic
insects in particular, tend to confine their activities to the larger
accumulations of dung (Legner & Olton 1971, Legner et al. 1974). An important requirement for appraising the value of
parasitic insects in the natural control of synanthropic muscoid Diptera is
to extract samples from the natural, undisturbed habitat. The immature hosts
(larvae and puparia) must be removed directly from the habitat in which they
were naturally formed, admittedly entailing painstaking labor. Changing the
breeding situation to facilitate collection as, e.g., gathering dung
deposited in pastures into piles in an effort to concentrate pupation sites
of hornflies and face flies, attracts those parasitic species which range in
accumulated dung for their hosts. Consequently, as most parasitoids of
synanthropic Diptera are not host specific but habitat
specific, the pasture breeding hornflies and face flies then sustain
parasitism by species of parasitoids that would rarely if ever find these
hosts in nature. The host habitat is all important to parasitoid searching,
as will be discussed in a later section (Flanders 1937, Laing 1937, Salt
1935, Vinson 1976). Particular attention to habitat is required when an
accurate appraisal of parasitoid performance is desired. Simmonds (1948)
concluded that, "...to avoid misleading results care must be taken to
secure samples of host material in the field with due consideration to the
habits of both host and parasite." In this way, the "host-exposure
method" acclaimed by Bartlett and van den Bosch (1964) is not always as
well suited technique, either for the qualitative or the quantitative
evaluation of parasitoids. The artificial exposure of host puparia can, as in
the case of Hippelates eye gnats, attract parasitoids that would not
normally parasitize the host in nature (Bay et al. 1964, Legner & Bay 1965 ). A careful
study of the breeding situation can, however, result in the development of
techniques where by the host may be exposed in a relatively natural situation
(Legner & Bay 1964, Mullens et al. 1986). The exposure of muscoid Diptera puparia in containers
within the host habitat, often called the "sentinel pupae method,"
may provide misleading results. In California, such exposures have (1)
produced parasitism by Nasonia vitripennis (Walker), a
parasitoid of blowflies that is only infrequently secured from muscoid hosts
when these are extracted naturally from the habitat (Legner 1967a), (2) excluded the parasitoids Spalangia cameroni
Perkins, Spalangia endius Walker and Spalangia nigroaenea
Curtis, which are often destroyed through multiple parasitism by both N.
vitripennis and Muscidifurax species, both intrinsically
superior in competition to Spalangia (i.e., their larvae kill other
parasitoids that they encounter inside a host with almost 100% efficiency). Although
N. vitripennis is the strongest "intrinsic"
competitor by virtue of its faster rate of development and gregariousness,
and Muscidifurax spp. are intermediate in superiority, their
respective searching abilities in the breeding habitat are reversed. The Spalangia
spp. range most broadly in the habitat, the Muscidifurax spp.
intermediate, while N. vitripennis searches primarily at the
habitat surface and is not capable of penetrating much beyond a few
centimeters for host puparia (Ables & Shepard 1974; Legner 1977; McCoy 1965).
Therefore, since each parasitoid species has its own special preferred
portion of the breeding habitat, an evaluation of each one's performance
would require positioning the "sentinel pupae" at different habitat
depths for each species. For further arguments about the sentinel pupae
method of host exposure see Meyer & Petersen (1982). Parasitic species also respond differently to different
sizes of hosts (Legner 1969a) and densities (Legner 1967b , 1969b). A standardized size of host which is not adjusted to
seasonal changes in nature, could give biased results. Although clumping of
the host is frequently found in nature, its degree varies and a host exposure
would have to reflect this to realistically appraise parasitoid activity.
Clumping intensity can be expected to vary seasonally, and accurate sampling
would be necessary to judge its pattern. With such sampling necessary anyway,
there is no logical reason to avoid it in the first place. Population Regulation Population theory is replete with definitions, so it is
often difficult to communicate upon various aspects without getting into
heated arguments. With the purpose of avoiding communication gaps, the
following terms may aid to separate the various forces involved in population
density determination. Competition.--is the interference between two or more organisms
seeking the same requisite. There are two kinds: interspecific and intraspecific. Regulative Factor.--a factor whose
action is governed by the density of a population in such a way that a
greater percentage of that population is destroyed as its density increases,
and vice versa. In other words, a regulative factor must be responsive to the
population which it regulates or that population would tend to increase or
decrease in large fluctuations. Examples are natural enemies (e.g., Cryptochaetum
iceryae, Coccophagoides utilis) which maintain their
hosts' densities at low levels. When environmental conditions favoring the
host would cause it to soar in numbers, the regulative factor increases
its rate of attack, to keep the host at a low level. Conversely, when the
density of the host reaches a critically low level, the action of the
regulative factor must ease off proportionally, or it might cause the
extinction of the host. It is important to realize that regulation is a
population phenomenon, and when a natural enemy species regulates its host it
does so with its entire population playing various roles in dynamics. Thus,
although individual members of the species may not be responsible to the
density of their host, the average action of the entire population of
individuals follows this pattern, or it would not be regulative. When a host
population is held within narrow density limits by a natural enemy, this reciprocal
relationship can be judged mathematically. Limiting Factor.--one whose input into a given ecosystem is independent of
a given population. It sets the maximum density at which that population can
exist (e.g., nesting sites, protective niches, available food, etc.). Control.--the manipulation by humans of certain population-determining
factors to maintain a given pest population at noneconomic levels. The above terms are used interchangeably and with different
meanings in the literature. These proposed definitions are a reflection of a
larger consensus of authors as of 1990, but may change in succeeding years. Many cases of scientific proof of the decisive role of
natural enemies in population regulation exist. Skeptics on the proven
examples may be either lacking in expertise, have minimal field experience,
or be just plain foolish. Certain methods of proof have individual
shortcomings, and whenever possible, two or more methods ought to be
employed. It should be realized that a host may be regulated at
different levels by the same natural enemy species in different climates or
seasons. A host may also be regulated by different natural enemies in
different areas, climates and seasons; and a host may be regulated by one or
more natural enemies in one geographic area and by no natural enemies
in another area. Intriguing subjects with many unknown are Matsucoccus
acallyptus and Matsucoccus spp. on pine trees, and Phryganidia
californica above 36E N. Lat. vs below
this latitude. Percent parasitization may be extremely low and still be
partly responsible for the observed population density (Rabb 1971). For
example, the tachinid, Winthemia manducae Sabrosky &
DeLoach, which attacks last instar tobacco hornworms, parasitizes at the rate
of 3-12%. But this rather modest parasitism occurs after all other mortality
factors and is, therefore, quire significant on the hornworm population. Also
parasitization of synanthropic flies is an example of irreplaceable
mortality and can have a significant effect on the adult fly population density
even when occurring at low percentages. The role of parasitism on alternate
hosts in determining the pest population levels on crops is poorly
understood, particularly when the mobility of the pest is high. A greater
effect of parasitism may occur on alternate host plants where the bulk of the
pest population may reside (e.g., egg parasitoids of the tobacco hornworm,
and the spotted bollworm in northeastern Australia). Important natural enemies probably often go unnoticed
because they are so effective (e.g., vedalia beetle, Chrysolina spp.
on Klamath weed, flatworm mosquito predators in rice fields, herbivorous fish
in irrigation canals, drainages and lakes). Effective natural enemies
regulate their own populations at very low densities and are seasonally most
abundant when they are not host regulative. Some predators are nocturnal and
many of the diurnal ones are highly mobile and difficult to observe.
Sometimes the act of predation is so quick that it is difficult to observe;
other times the balance has resulted in such a lowering of the pest density
that the natural enemy is difficult to find in sizeable numbers. Prominent ecologists with adequate field experience do not
dispute the often important role of parasitoids and predators in natural
control. Rather, they are active studying the complicated mechanisms involved
in natural control in order to enhance our understanding of the population
phenomena involved, as well as to further our ability to properly manage our
environment. Exercise 7.1--Discuss the examples of stability in nature using natural
biomes as illustrations. Exercise 7.2--How may the impact of natural control factors be
measured? Exercise 7.3--Discuss the value of a percent parasitization figure. Exercise 7.4--What is a natural balance? Homeostasis? Exercise 7.5--How do you account for the long term existence of some
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