THE ROLE OF PARASITOIDS, PREDATORS
AND PATHOGENS IN NATURAL CONTROL
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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.
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.
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.
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.
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 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 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 low densities when they possess no apparent natural enemies?
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