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HYMENOPTERA, Encyrtidae (Walker 1846) - (Chalcidoidea) -- <Images-1> & <Images-2 & <Juveniles> Please refer also to the following links
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1 Description
& Statistics Encyrtidae. -- This is a large and worldwide group, with more than 372 North
American species known. They average 1.1-2.5 mm in length and are
distinguished by a broad convex mesopleura, whereas in most of the chalcids
the mesopleura have a groove for the femora, but this groove is absent in the
encyrtids. The encyrtids differ from
the eupelmids by having a convex mesonotum convex and lacking parapsidal
furrows or have them but incomplete. Most species are parasitoids of aphids,
scale insects, and whiteflies, but there are also species that attack insects
in other orders. Polyembryony occurs
in some of the species.
Members of this family regularly attack the Homoptera family Coccidae,
especially the Lecaniinae and Dactylopiinae, although other families such as
Aphididae and Cercopidae may also serve as hosts. In the hemipterous family Pentatomidae and in closely related
forms, only the egg stage is attacked.
Many Lepidoptera are parasitized, some by species that develop in the
eggs and others in the larvae.
Several genera are in the latter group that are capable of
polyembryonic reproduction, it being possible that several thousand
individuals emerge from a single host.
Among Coleoptera, the larval and pupal stages of Coccinellidae and
Chrysomelidae are frequent hosts.
Dipterous pupae, in particular those of the Syrphidae and
Cecidomyiidae, are often parasitized.
Several species are recorded from neuropterous cocoons, principally of
the genus Chrysopa. On occasion instances are known of attack
on other orders and families such as Ooencyrtus
submetallicus Howard attacking the
chloropid dipteran, Hippelates pusio Loew. Some encyrtids are internal parasitoids of the nymphs of ticks
(Ixodidae), represented by the genera Huntrellus
and Ixodiphagus.
Regarding secondary parasitism, some representatives of the family
develop in Coccidae and Aphididae and in lepidopterous eggs, the primary
hosts being the immature stages of other Chalcidoidea, etc. Some genera are known to parasitize the
immature stages of the Dryinidae in their cocoons. A large number
of species of Encyrtidae have been utilized in the biological control of crop
pests, in particular of scale insects.
Four species which have adequately controlled their hosts in one or
more geographic areas are Anagyrus dactylopii How. (on Pseudococcus filamentosus Ckll.); Blastothrix
sericea Dalm. (on Eulecanium coryli L.); Habrolepis dalmanni Westw. (on Asterolecanium variolosum Ratz.); and Pseudaphycus
utilis Timb. (on Pseudococcus nipae Mas.) (Clausen 1940/1962).
There are many other cases where an appreciable reduction in the host
population occurred, although not sufficient to eliminate entirely the need
for other controls Key
references are Trjapitzin & Gordh (1978a, 1978b), who keyed the females
and males, respectively, of the genera of North America; Trjapitzin (1971,
1989) keyed the Palearctic genera; Noyes (1980, 1988) keyed the Neotropical
genera and the New Zealand genera and species, respectively; Noyes & Hayat
(1984) keyed the genera from the Indo-Pacific region; and Prinsloo &
Annecke (1979) keyed the genera from the Ethiopian region. Trjapitzin (1973a, 1973b) discussed
subfamily and tribe classification, and Trjapitzin (1977) gave a
comprehensive analysis of known morphological diversity within the
family. Tachikawa (1963) monographed
the family for Japan, and Tachikawa (1981) provided a list of the known hosts
for encyrtid genera. Biology & Behavior
Encyrtidae usually develop as
internal parasitoids, the only exceptions being the occasional species of Microterys which are predaceous on the
eggs of Coccidae. This habit was
observed by Silvestri (1919b) in the case of M. sylvius Dalm. in
relation to Eulecanium coryli L. in Italy. DeBach (1939) found M. titiani Gir. to have
the same habit. The hyperparasitic species are
usually direct in their relationship, though Syrphophagus aphidivorus
Mayr is an indirect secondary parasitoid of Macrosiphum cornelli
Patch through Aphelinus juncundus Gahan (Griswold 1929). Adult Habits.--Adult females generally contain fully developed eggs at the
time of emergence, and they are consequently able to oviposit
immediately. Among certain of the
multibrooded species parasitic in single brooded Coccidae, there is a period
of diapause at the beginning of adult life of the females of the summer brood
that may be of advantage to the parasitoid during the period when the host is
not in a suitable stage of development for parasitization. Silvestri (1919a) found that the second
brood of adults of Blastothrix sericea refused to oviposit in young
host scales, and an examination of their ovaries showed them to be much
reduced during the summer and early autumn.
Reproductive activity is thought to revive during the autumn, for 1st
instar larvae were found in 2nd instar hosts in November. Homoptera attacking species derive
their food mostly from the honeydew secretions of their hosts, although a
number feed directly on the host body fluids. Several species of Ooencyrtus
feed at punctures made in the host egg in which their progeny are to develop. Species attacking Homoptera obtain
their food mostly from the honeydew secretions of their hosts, though quite a
few feed directly on host body fluids.
Several species of Ooencyrtus
feed at punctures made in the host egg in which their progeny will develop. In Tachinaephagus zealandicus
Johnston & Tiegs (1921) suggested that mating occurred both inside and
outside the host puparium. They
isolated emerging females with hosts, and the resulting progeny contained
females, thus demonstrating pre-emergence mating. However, when Olton & Legner (1974) selected females at
emergence from Musca domestica puparia, only male progeny
were produced indicating that they were unmated. However, mating was repeatedly observed immediately after
emergence from the puparium. Males
and females usually issued through the same aperture cut in the host puparium
and tended to remain close to the host for several seconds while
grooming. Once the females moved away
from the host, males pursued rapidly from the posterior and moved sideways
with the female. Females were quite
active and males were often buffed in mounting. Mating proceeded rapidly, lasting only ca. 15-20 sec. after
mounting. Mating was observed in
light and darkness; however, activity of both sexes was reduced in darkness. Female parasitoid host examination,
feeding and oviposition are well exemplified in Microterys clauseni
Comp. parasitic in Ceroplastes floridensis Comst. in Japan. The preliminary activities are sharply
distinguished from insertion of the ovipositor for oviposition. The female first examines the host scale
carefully with the antennae, after which she mounts upon its dorsum. After a further examination in that
position, she inserts the ovipositor perpendicularly into the body. This insertion and the probing that
follows are not for oviposition but may serve two purposes: to determine whether the host is in a
suitable physical condition and whether it is already parasitized. Sometimes feeding takes place on fluids
that exude from the wound. When
examination is complete and the host is judged satisfactory. the female
dismounts from the scale dorsum, approaches the caudal end of the body, and
inserts the ovipositor by a backward thrust between the anal plates. The egg is deposited in the intestines and
lies with the anterior portion of the stalk extruded between the plates
(Clausen 1940/1962). Egg placement is
constant and has been recorded also for Eusemion
corniger Wlk. (Martelli 1910) and Diversinervus elegans Silv. (Compere 1931). The unusual habit of inserting the
ovipositor beneath the margin of the body of the half-grown Saissetia female and piercing the body wall from beneath is shown by Metaphycus lounsburyi How. Normally
the species attacking Coccidae insert the ovipositor through the dorsum. The oviposition habit of hyperparasitic Syrphophagus aphidivorus is distinctive in that the female stands upon the
dorsum of the living aphid, inserts the ovipositor perpendicularly, and
probes around until the young Aphelinus
larva is located. Then the body is
pierced and the egg deposited.
Surprisingly the aphid host appears not to be inconvenienced or to
suffer any discomfort during this act, although it may be already sluggish as
a result of the activities of the Aphelinus
larva within its body. Adult females feeding on host body
fluids usually does not result in serious host injury. In several other families it is known that
certain species which oviposit in the host egg or whose larvae are egg
predators completely consume the contents of the eggs on which they feed, and
this habit is probably of greater importance in reducing the host population
than is the parasitic or predaceous habit of the larvae. Observations on Ooencyrtus johnsoni
How. indicate that its stinging of the eggs of Murgantia histrionica
Hahn incident to feeding may similarly result in heavy mortality (Maple
1937). It was found that a very large
number of eggs that had been punctured with the ovipositor failed to hatch,
even though oviposition did not take place.
The death of the embryo is due not to the abstraction of appreciable
quantities of fluids from the egg but most likely either to mechanical injury
or to the injection of some toxic agent at the time of stinging (Clausen
1940/1962). Little is known about the
reproductive potentials of the monoembryonic Encyrtidae. The maximum recorded is ca. 250 for Microterys speciosus Ishii, and the majority of species do not seem to deposit
greatly in excess of 100-150 eggs.
Ishii found an average of 172 mature eggs in the ovaries of gravid
females of Aphycus timberlakei Ishii. Crossman (1925) found that virgin females
of Ooencyrtus kuvanae How. deposit a smaller number of eggs than do those which
are mated. Maple found that mating
had no influence on the oviposition activities of the females of O. johnsoni. In fact, one unmated individual produced
224 male progeny, a number in excess of that secured from the mated
females. The oviposition period of
this species covers ca. three weeks (Clausen 1940/1962). Studying oviposition and fecundity,
Olton & Legner (1974) found that females walked or flew when approaching
prospective M. domestica host larvae.
The host was usually mounted postero-dorsally and inspected with the
antennae and tip of the ovipositor.
If the host was accepted by the parasitoid, the ovipositor was
inserted inter- or intrasegmentally just beneath the integument. The eggs were deposited in 20-45 sec. Chemical stimuli present in the breeding
medium apparently were important in releasing the ovipositional response, as
females were induced to oviposit in 10 host integuments that were washed in
distilled water and re-contaminated with medium, while no oviposition was obtained
with 10 clean integuments. Multiple
ovipositions were common under laboratory conditions, where an individual
female that had just deposited a cluster of 3-6 eggs would return to deposit
another cluster. Under unusually high
parasitoid/host densities (>50 parasitoids/host) different females usually
attacked an individual host simultaneously. Newman & Andrewartha (1930)
stated that T. zealandicus preferred to oviposit in fully developed blow fly
maggots, but if this stage were unavailable they readily parasitized earlier
instars or pupae. This also was true
with M. domestica except that only white to light tan puparia were
accepted for oviposition. T. zealandicus
could not pierce a hardened puparium.
Olton & Legner (1974) compared the number of viable eggs deposited
and total number of larvae parasitized per female at three host
densities. Females generally
deposited most of their eggs during the first 12 h., and there was
considerable variation between consecutive periods of oviposition within and
among treatments. However, egg number
ranged from 11 to 148 (Olton & Legner 1974). Female T. zealandicus
longevity was significantly different between high and low host densities;
they lived an average of 50 h at a host density of 5 and 67.2 h at a host
density of 30 (Olton & Legner 1974).
To determine whether this variation in longevity occurred in the adult
life span, the reproductive behavior was divided into prereproductive,
reproductive and nonreproductive periods.
Six-hour intervals in these categories were totaled, multiplied by 6,
and divided by the number of females observed to give the average time per
category. There was an apparent trend
towards a longer prereproductive period at the low host density. The prereproductive period at the low host
density comprised a considerable part of the average longevity. Reproductive periods were not
significantly different among all three host densities, the greatest
variation occurring among nonreproductive periods which were considerably
longer than at the highest host density. Olton & Legner (1974) studying
the extent of parasitization and distribution of viable eggs at three host
densities found no significant difference in the average number of hosts
parasitized nor the average number of viable eggs laid per female among
treatments. But there was a
significant difference in the average number of viable eggs laid per host
between the high and low density. A
tendency towards multiple oviposition or more eggs per insertion of the
ovipositor was shown at the low density.
Averages of 4.58 eggs/host at a density of 30 hosts and 6.14 eggs/host
at a density of five hosts were well below levels resulting in
superparasitization. It was concluded
that T. zealandicus is a short-lived species capable of depositing a
relatively fixed number of eggs during a short reproductive period,
regardless of host density. The
probability of an increased number of eggs per host was a function of host
density. Under constant conditions cultures
of parasitic Hymenoptera may display a periodicity and time-spread in adult
emergence (Beck 1968, Legner 1969).
In T. zealandicus peak adult eclosion usually occurred during the early
morning hours. Emergence seemed
independent of a transition from darkness to light as shown by 0400 and 0800
h peaks in all light regimes, suggesting that adult eclosion showed a
circadian rhythm (ca. a 24-h period) with a free-running period that was
similar in all treatments. Analyzing
the 12:12 LD treatment to determine if the numbers and sex of parasitioids
that emerged per host changed during a 3+ day period, Legner & Olton
(1974) regressed the average number of parasitoids emerging per host (Y) on
time of emergence (X) and found a highly significant coefficient of -0.859. This indicated that the higher the average
density of parasitoids per host (within limits) the shorter the developmental
period. Host contents were consumed
sooner at the higher parasitoid/host densities. There was no obvious change in the proportion of emerged
females and males during periods of peak eclosion (early morning), and
females predominated 2:1. Parasitoids
issued from a single exit host within ca. 3 min. after breakthrough. Both males and females initiated
emergence; therefore, there was no differential rate of development between
sexes at various densities as found by Legner (1969) for pupal parasitoids. A high rate of multiple oviposition
was thought to occur with high parasitoid:host ratios in T. zealandicus (Olton
& Legner 1974). Results of reproductive
potential tests indicated that females deposited 4-6 eggs per host during
their life span. There was enough
food present in a single standardized host to sustain development of progeny
resulting from at least 3-4 average egg depositions; however, the progeny
usually were small and stunted at the upper limit. Regarding development of eggs and
larvae, in many cases it has been observed that a marked increase in size
takes place among the stalked eggs during the course of incubation. The dimensions given by Clancy for the egg
of Cheilophagus compressicornis Ashm. are 0.16 X 0.06
mm, for the egg body at the time of deposition and 0.73 X 0.27 mm on the
fourth day immediately before hatching.
This is exceeded in Tetracnemus
pretiosus Timb., the egg of which
increases in length from 0.03 or 0.04 mm to 0.25 mm. In Chrysopophagus,
the trophic membrane is seen, completely enveloping the embryo, one to two
days after deposition. Through this
membrane food materials are derived from the body fluids of the host. It envelops the body of the 1st instar
larva throughout the stage, allowing the head and tail to protrude. The distinctive longitudinal rib or
plate on the encyrtiform egg of Microterys
and many other genera has received considerable attention. It was generally assumed that the egg
stalk, which protrudes through the integument of the host, serves as a tube
through which the larva draws its air supply from the outside. Timberlake (1913) stated that the larva
"maintains, without the least doubt an intimate and vital connection
with the egg stalk, and the latter might properly be called a living part of
the organism." However, this
explanation ignores the relationships of the rib to this function (Clausen
1940/1962). Silvestri (1919) made the first
observations relating to the manner of respiration of the larva through an
egg of this type, in which the distinctive rib was described in detail and
considered from the point of view of its function. This was done on a series of species parasitic in lecaniine
Coccidae in Italy. It was noted that
the interstices of the cells of the rib were filled with air and hence
designated the structure as the "aeroscopic plate" but concluded
that actual respiration of the larva was through the lumen of the tube
itself. The plug at the outer end of
the stalk was thought permeable to gases, and exchange was thought to be by
diffusion. Maple (1937) studied the
structure and manner of functioning of this plate in O. johnsoni. He observed that the single pair of caudal
spiracles of the larva are always in direct contact with the plate of the egg
body and that the location of this point of attachment has no relation to the
egg stalk. No aperture could be found
in the external plug of the egg by means of which air can pass through the
lumen of the stalk. Stained oil tests
showed ready penetration of the interstices of the place and thence into the
larva's tracheal system. No penetration
into the stalk lumen was found.
Maple's work showed that the aeroscopic plate, rather than the stalk
lumen, provided the channel through which the outside air reached spiracles
of the parasitoid larva within the host's body. Unclear is how the air supply
contained in the rib interstices reaches the larval spiracles. The rib is external whereas the posterior
end of the larva, bearing the spiracles, remains within the cup-like egg
shell. Either the chorion beneath the
plate is permeable, or perforations are made somehow by the larva so that an
air supply in the plate becomes accessible (Clausen 1940/1962). It was generally assumed that all
eggs of this type which project through the host integument and to which the
larvae are affixed possessed the aeroscopic plate until Clancy found that the
egg of Isodromus iceryae How. lacks the plate and that
the shell and stalk have no function other than to hold the young larva in
position. Silvestri previously
mentioned that the 1st instar larva of Aphycus
melanostomatus Timb. (A. punctipes
Dalm.) lacked the caudal spiracles even though arising from an encyrtiform
egg but he still thought that the air supply was derived through the egg
stalk. All accounts of development of
encyrtiform eggs and larvae pointed out that the posterior end of the larva
is encased in the eggshell, but nothing is mentioned regarding the manner in
which that position was attained. The
stalk is at the anterior end of the egg, and the head of the embryo would
thus be formed near the base of the stalk and the posterior end of the body,
bearing the spiracles, at the opposite end.
In Maple's illustration of the mature embryo of O. johnsoni within the
egg, the opposite orientation was shown, with the posterior end of the body
at the anterior end of the egg and the spiracles in contact with the
aeroscopic plat at the base of the stalk.
His illustration of the newly hatched larva of Anagyrus yuccae Coq.
indicates a normal orientation prior to hatching (Clausen 1940/1962). It appears that the position of the
young larva with respect to the eggshell is brought about either by a
rotation of the developing embryo within the egg or by a reversal of position
of the larva immediately after hatching.
The former is obvious in O. johnsoni, and observations on Microterys clauseni indicate a similar movement prior to hatching (Clausen
1940/1962). Encyrtiform larvae
usually maintain their connection with the egg stalk until the final larval
stage, utilizing it for respiration during this entire period. The successive exuviae are forced back
over the body and become a part of the sheath enveloping the posterior end of
the body. The number of exuviae is
directly related to the larval instar. Encyrtiform larvae of M. clauseni,
which occurs in the hind intestines of Ceroplastes,
seems to limit its feeding to the contents of the digestive tube, and only
after the 2nd molt is the intestinal wall broken and direct feeding on the
viscera and body fluids occurs. The
host usually dies 10-12 days after parasitoid oviposition. In species that have stalked eggs,
a varying proportion of individuals may also retain the egg shell and the
cast skins as an envelope about the caudal end of the body (Clausen
1940/1962). This habit is associated
with larvae of both the hymenopteriform and caudate types, which are free
living in the host body, and serves no apparent purpose. In C.
compressicornis, the successive
exuviae cover a considerable portion of the body, and the mandibles of the
firs two can be easily distinguished on the mid-ventral area of the 3rd
instar larva. Biology
In Encyrtidae the number of larval
instars is variable, ranging from 2-5.
Anarhopus sydneyensis Timb. is the single
species known to have only two (Compere & Flanders 1934). Most species are thought to have three
instars, although several have four or five.
However, the great majority probably have five and the lesser number
recorded in many cases is due to having overlooked early exuviae. An exact number can be determined only b
clearing and staining the entire host contents, and in this way the mandibles
become recognizable and can be measured. Modifications in larval development
that are most striking relate to respiration of encyrtiform larvae during
later stages. At this time a
functional relationship is made by some species with the host's tracheal system. This phenomenon was demonstrated in Encyrtus infelix Embl. (Embleton 1904, Thorpe 1936). E.
infidus Rossi (Clausen 1932b), Aphycus melanostomatus Timb. (Imms 1918) and Carabunia myersi
Waterst. (Myers 1930). Carabunia is parasitic in the nymphs
of the froghopper, Clastoptera undulata Uhler, and the remaining
species attack lecaniine Coccidae.
All these, with the possible exception of A. melanostomatus,
pupate and emerge while the host is still alive. Clausen (1940/1962) stated the course of events as follows: "When approaching maturity, but
before the last molt, the parasite larva becomes invested with a membranous
sheath. At approximately the same
time, the tracheal branches of the host fuse with, or become attached to it,
in the immediate vicinity of each of the four parasite spiracles. At this time, the functional connection of
the larva with the egg stalk is broken.
The sheath, which surrounds the larva and later the pupa..., becomes
filled with air, and the oxygen supply of the parasite is derived
therefrom. Miss Embleton, who was
first to observe this remarkable adaptation, surmised that the sheath was
probably a cast larval skin, and this interpretation was followed by several
later authors. Imms concluded that it
arises as a chitinous proliferation of the host tracheae, whereas Thorpe,
after a detailed study, has recently stated that it is of host origin but
produced by phagocytic action, in the building up of which the find tracheal
branches play a part." Flanders (1938a) arrived at what seems
to be the correct conclusion as to the origin of this sheath. He found that the ileac and labial glands
of the larvae are apparently identical in function and that they produce a
viscid material which exudes from both ends of the body and spreads to form a
thin protective covering. The sheath
of Encyrtus is consequently a
cocoon, in film form rather than composed of strands, and is identical in
origin with the common spun cocoon.
The sheaths enveloping the larvae and pupae of other endoparasitic Chalcidoidea,
in particular the Encyrtidae and Aphelinidae, are developed in the same
manner. Although Thrope's
interpretation of the origin of the sheath of E. infelix is seemingly
not valid, yet his explanation of the manner in which the connections between
the sheath and the host tracheae are brought about is of interest. As the sheath develops, the adjacent
tracheal trunks of the host form a union with it in the immediate vicinity of
the larval spiracles. This is stated
to be the result of a physiological rather than a mechanical reaction. The tracheal epithelium is activated by a
sudden change in respiratory activity, such as a lowering of the oxygen
tension or an increase in carbon dioxide concentration incident to the
approach of the pupal stage and to the stoppage of an adequate air supply
through the egg stalk. Such a
stimulus would naturally be most strongly felt in the areas surrounding the
open spiracles. The sharp bending of
the tracheal branch, which is evident at the point of attachment, results in
most cases in a definite fracture of the tracheal lining (Clausen 1940/1962). Also of interest in the biology of Encyrtus is the habit of the mature
larva of reversing its position within the sheath prior to pupation. This occurs whether the parasitoid is
solitary in young scales, as E infelix in Saissetia hemisphaerica Targ., or gregarious, as
E. infidus in Lecanium kunoensis Kuw. In the latter, an average of 6.4 Encyrtus individuals reach maturity in
each full grown female scale. Without
a reversal in position, the pupae and the newly transformed adults would lie
with their heads directed downward toward the venter of the scale, and
emergence from the living host would be encumbered. However, the head of the pupa is directed outward near the point
of insertion of the egg, and the instincts of the adult to move directly
forward bring it quickly to the body wall of the host where emergence may
occur. Why E. infelix changes its
position is not so clear; for the solitary parasitoid is oriented along the
longitudinal axis of the host, and emergence of the adult would seem to be as
readily accomplished from one end or the other. Thorpe stated "That this turning movement is the result of
an innate instinct and is not dependent on some stimulus provided by the
tissues of the host is shown by the fact that even in those rare cases where
the egg has been deposited anteriorly the tendency to turn is still
manifest." Regarding pupal respiration, the
change in position has little effect, for in either case the two points of
fusion of the sheath and the host tracheae would overlie the two pairs of
functional spiracles of the pupa. The way of formation of the sheath
and the pupation habit of Carabunia
myersi are apparently identical
with those of Encyrtus, but it is
interesting that the early larval instars are of the caudate type rather than
encyrtiform. Tracheal attachment may
occur at several or all of the six larval spiracles. The sheath does not become filled with air
until sometime after pupation, while in Encyrtus
the connection is functional during the last larval stage and air bubbles
surround the pupa at its formation. Solitary encyrtid parasitoids of
mealybugs produce a pronounced inflation of the host body, causing it to become
circular in cross section, cylindrical, and smoothly rounded at both
ends. The interior of the shell is
smooth and often highly polished, as if by a secretion provided by the
parasitoid itself. These parasitized
mealybugs are usually referred to as "mummies" and bear a
superficial resemblance to certain dipterous puparia. The gregarious species, such as Acerophagus notativentris Gir., produce a similar inflated condition, and
each of the surface cells is distinctly outlined externally. In some hyperparasitic species, pupation
takes place within the larval skin of the primary host. This is shown by Quaylea whittieri Gir.,
a solitary internal parasitoid of the mature larvae of Scutellista, Metaphycus,
and other parasitoids and egg predators of Saissetia and related Coccidae.
The larval skin of the host parasitoids becomes very distended and
darkened, and also resemble dipterous puparia (Clausen 1940/1962). The effect of the stage of host
development at the time of attack on the cycle of the parasitoid is shown in
the case of Hunterellus hookeri How. (Ixodiphagus caucurtei
Buy.), which develops internally in many species of ticks in various parts of
the world. The eggs are deposited in
the nymphal instars of the host, and development of the larvae is delayed
until the host becomes engorged with blood.
This was called "latent parasitism," and under some
conditions a period of six months may elapse from the time of oviposition
until the host shows evidence of parasitization. The obligatory diapause in the early larval stage is imposed by
the host and is apparently due to the nutritional requirements of the
parasitoid larva not being met until the host is fully fed (Clausen
1940/1962; Cooley 1928, Cooley & Kohls 1933, Brumpt 1930). Regarding sex ratio and parthenogenesis, the majority of Encyrtidae reproduce
bisexually, and there is usually a slight preponderance of females among the
progeny, the extreme in this respect being a ratio of 5.3:1 in Zarhopalus sheldoni Gir. (Clausen 1924).
An exception to this rule may be in Tetracnemus pretiosus
in which the males are in excess in the ratio of 1.4:1 (Clancy 1934). This record is based on laboratory
rearings and may differ from the field ratio, which in Ooencyrtus johnsoni is
ca. 4:1. The sex ratios of the overwintering
and spring generations of Microterys
clauseni in Ceroplastes are markedly different. The first generation is solitary in young scales, and the
adults that emerge in the early spring are predominantly female, in the ratio
of 3:1. In the second generation,
which is gregarious in the mature scales, an average of 3.15 individuals
develop in each scale and the ratio is increased to 9:1. Parthenogenetic reproduction occurs in
male progeny only. The peculiar
aspect about the reproductive habits of this species is that the
"brood" in each scale consists of only one sex (Clausen
1940/1962). In a series of 73 Ceroplastes females isolated
individually for parasitoid emergence, not a single exception to this rule
was found. The explanation of this is
not clear, because the eggs are deposited singly, and the females show no
hesitation in ovipositing in hosts that already contain one or more
eggs. Therefore, the parasitoid
content of a scale is often the result of successive ovipositions by several
females over a period of days. Unisexual reproduction occurs in a number of species. Embleton secured only a single male among
1,000 adults of Encyrtus infelix, and only a single one has
been secured among the extensive rearings of the same species in Hawaii. Timberlake (1919) recorded the same
reproduction habit in Adelencyrtus odonaspidis Full., Blepyrus mexicanus How., Pauridia
peregrina Timb., and Saronotum americanum Perk. To this
list may be added Anagyrus subalbicornis Gir., Habrolepis dalmanni, and Comperiella
unifasciata. Occasional males have been reared in most
of these species, but they seem to play no part in normal reproduction. However, Ishii believed that virgin
females of Microterys speciosus produce only female progeny,
whereas those which are mated produce both sexes. Parker & Thompson (1928) mentioned that their rearings of
polyembryonic Copidosoma thompsonii Mercet have not yielded a
single male, though they do not state that reproduction is unisexual Polyembryony.--The Encyrtidae is the only family demonstrating polyembryonic
reproduction among Chalcidoidea. It
is mostly confined to a group of closely related genera comprising Ageniaspis, Copidosoma, Paralitomastix,
and Copidosoma. Most if not all species of these genera
probably reproduce by polyembryony.
Hosts are exclusively Lepidoptera. Marchal (1898, 1904) first studied
polyembryony on A. fuscicollis Dalm. and A. testaceipes
Ratz. Other early investigations were
Silvestri (1906, 1908, 1914a) on L.
truncatellus Dalm., A. fuscicollis
praysincola Silv., C. buyssoni
Mayr., C. tortricis Waterst., and C.
nanellae Silv.; Martin (1914) on A. fuscicollis;
Patterson (1915, 1917, 1918, 1921a) on C.
gelechiae How. and L. floridanus
Ashm.; Leiby (1922) on C. gelechiae; and Ferriere (1926b) on L. kriechbaumeri
Mayr. Bugnion (1891) first observed
the presence of embryo "chains" of A. fuscicollis Dalm. in
the larvae of Hyponomeuta, but he
did not attribute them to polyembryonic development. It was not until the classic series of
papers by Marchal, the first of which appeared in 1898 and which dealt not
only with Ageniaspis but also with
several platygasterid genera of similar habit, that the true explanation of
their origin was revealed. There is much uniformity in habit
among the members of this group. All
lay the egg within the embryo of the host egg, and the host attains the
mature larval stage before it dies.
In some species a few host individuals may reach the pupal stage. At the time the parasitoid larvae attain
maturity, the body of the host becomes much distended, being often twice or
more the size of a healthy larva. It
is frequently considerably distorted, with a mummified appearance and the
uneven surface shows each of the outer parasitoid pupation cells
distinctly. In other species the
bodies are distended but not deformed.
The number of parasitoids that are able to complete development in a single
host is dependent on the size of the latter.
The species that are known to be of polyembryonic habit, with their
hosts and the number of individuals developing in each one, were listed by
Clausen (1940/1962). The genus Encyrtus, as now restricted, is limited in its host preferences
to nondiaspine Coccidae Clausen (1940/1962).
Ishii (1932a) recorded what he believed was an embryo chain of Syrphophagus sp. in the larva of a
syrphid fly. The parasitoid egg is
deposited within the embryo in the host egg and during the remainder of
incubation of the latter, and in the body of the developing caterpillar, it
multiplies into a varying number of cells, forming an elongate, asymmetrical
body, enveloped in a membrane of parasitoid origin, the whole mass being
generally referred to as an "embryo chain" (Clausen 1940/1962). This chain, which is free-floating in the
body of the caterpillar, finally breaks up into its component parts, each of
which becomes attached to a host organ and develops into an embryo and
finally into a larva. This latter stage
is attained only after the host larva has become mature. In hosts that produce a very large number
of parasitoid individuals, several of these embryo chains may be found, each
one of which has developed from a single egg. The sexual, or normal, larva is
hymenopteriform and presents no distinctive features. Among the larvae arising from an embryo
chain, there are a varying number that are characterized by the lack of the
reproductive, the respiratory, and possibly the circulatory system. These, which have been designated as
asexual larvae (Clausen 1940/1962) were first observed by Silvestri in Copidosoma truncatellus and have since been found among the broods of many
other species. They develop in
advance of the sexual larvae and are of greater size. They are unable to feed directly and begin
to disintegrate shortly after emergence from the embryonic envelope. Silvestri expressed the opinion that these
larvae serve a definite purpose in lacerating or breaking up the host tissues
for the feeding of the sexual larvae, but Parker & Thompson (1928)
considered them to be mere monstrosities and of no special significance. Silvestri also presented the hypothesis
that the asexual larva is an ancestral form, harking back to the time when
the normal larva was free-living and somewhat vermiform. The length of the life cycle of the
polyembryonic Encyrtidae is dependent on that of the host, insofar as larval
feeding is not completed until the host larva is in its final instar. Most of the species listed have only one
generation per year, though several have two or three. In the latter case, the cycle of the
summer broods, from egg to adult, is ca. 30 days. Hibernation is also host
influenced. C. gelechiae, parasitic
in Gnorismoschema salinaris, passes the winter in the
adult stage and oviposits in the spring as soon as host eggs become
available, while when parasitic in G.
gallaesolidaginis, this period is
passed as an egg in the host embryo.
Other species are found during the winter in their early stages of
development within the partly grown host larvae, and still others are in the
mature larval stage within the host carcass.
In every species, there is a close synchronization with the cycle of
the host. The parasitoid brood that
emerges from a single host may all be of the same sex, or they may be
mixed. No males have been found in C. thompsoni
and in only one case in L. kriechbaumeri. These two species may reproduce
unisexually. In most of remaining
species the broods are of one sex only, with, in some species, occasional
broods containing a few individuals of the other sex also. Silvestri noted that the broods of L. truncatellus
in Phytomctra gramma are usually of one sex, but Leiby (1926) found that the
great majority of those from P. brassicae are mixed. L.
floridanus and Paralitomastix variicornis
usually produce mixed broods. The
brood may arise from a single parasitoid egg, or it may be the result of
several ovipositions. It was noted in
several species that several eggs are deposited at one insertion of the
ovipositor. Silvestri thought that
about 100 normal larvae are produced from each egg of L. truncatellus. The several thousand individuals in each
brood must thus be the result of a considerable number of ovipositions. Marchal and others considered that the
mixed broods are the result of oviposition by both mated and virgin females
in the same host individual, the former producing female progeny and the
latter male progeny only. But
Patterson and others do not accept this explanation. Parasitism Effects on Host Reproduction.--Many encyrtid parasitoids of Coccidae attack
the adult females, but, if oviposition is in the nymphs, host death does not
occur until after maturity is reached.
The host thus may be able to realize a portion of its reproductive
potential, and the value of the parasitoid is correspondingly reduced. Ishii thought that Microterys speciosus
exercised little repressive effect on the increase of Ceroplastes rubens
Mask., for death of the parasitized female seldom occurred until the full
quota of eggs had been laid. In
contrast, M. clauseni, in its spring generation upon adult C. floridensis
Comst., very largely inhibits oviposition after the parasitoid eggs are laid,
and the portion of the oviposition potential that is realized in the field is
small (Clausen 1940/1962). Imms (1918a) estimated that 71.9%
of the females of Eulecanium coryli L. parasitized by Blastothrix sericea deposit about their normal quota of eggs. Females of Lecanium kunoensis
parasitized by Encyrtus infidus in Korea were estimated to
deposit ca. 50% of the normal number, and it was noted that oviposition
frequently takes place even after the parasitoids within the body have
attained the pupal stage (Clausen 1940/1962). The effect of parasitism on the diaspine scales is more quickly
evident. Taylor (1935) stated that
the disintegration of the body of Aspidiotus
destructor Sign. begins immediately
after hatching of the eggs of Comperiella
unifasciata Ishii and Spaniopterus crucifer Gahan; therefore, oviposition ceases within five days
after attack by these parasitoids. Life Cycle.--Most species of Encyrtidae produce several generations each
year. This is especially true of
those whose hosts are in a proper stage for attack throughout the
season. Under optimum temperature,
the cycle from egg to adult is complete in 2-7 weeks. Ooencyrtus
malayensis Ferr., parasitic in the
eggs of Pentatomidae in Java, completes its cycle in 12-13 days. In many cases the duration of the life
cycle is strictly dependent on that of the host. This is especially true of the polyembryonic forms that
oviposit in the host egg and emerge from the mature larva or the
prepupa. A given species may have a
single annual generation on one host and several on another, depending upon
the habits of the hosts. In each
case, the cycles are closely synchronized (Clausen 1940/1962). Among those species that are
parasitic in scale insects, several generations per year is the rule though
notable exceptions occur. Microterys clauseni, which passes through its spring generation in Ceroplastes in ca. one month,
nevertheless has only two generations annually. These adult must persist in the field for several months until
the young scales are sufficiently developed for attack in autumn. Hibernation may be in any larval or even
in the pupal stage within the host.
Many of the species that parasitize insect eggs have a life cycle
entirely independent of that of the host.
Thus, Ooencyrtus kuvanae has six and a partial seventh
in the eggs of the gypsy moth, though the latter has an annual cycle, the
greater portion of the year being passed in the egg stage. The parasitoid itself hibernates as an
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Richerche sugli insetti entomofagi.
I. Specializzazione
entomoparassitica negli Encyrtidae:
studio morfologico, etologico e fisiologico del Leptomastix dactylopii
Howard. Bol. Lab. Ent. Agr.
"Filippo Silvestri" Portici 18:
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