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THE
ROLE OF PARASITOIDS, PREDATORS
AND PATHOGENS IN NATURAL
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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 pesticides or other experimental means excludes natural
enemies. 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. Parasitoids and
predators attack the mealybugs; one gall midge has 12 species of parasitoids.
Coyote brush has 54 species of primary plant feeders that 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 African 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 that 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 that 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 prodigious 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 that 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): [Please see <koiidio.htm>
for greater detail ]. 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 that 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. The interactions
between an organism with its natural enemies creates a balance, which
guarantees the survival of all in accordance with available resources of food
and space, is a process which is termed "Regulation." 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 natural enemy holds a host population within
narrow density limits, 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. Different natural enemies in
different areas, climates and seasons; may also regulate a host 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 animal populations at very
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