AN ABSTRACT OF THE THESIS OF
Robert John Mader for the degree of Master of Science
in Entomology presented on June 3, 1982 Aspects of the Field and Developmental Biology of Apanteles Title: yakutatensis, a Parasitoid of Autographa californica.
Abstract approved: Redacted for Privacy Jeffrey tr. Miller
Behavioral and ecological aspects of the field and developmental biology of Apanteles yakutatensis (Ashm.),a primary larval parasite of
the alfalfa looper, Autographa californica (Speyer), were investigated in 1980 and 1981. Populations of A. yakutatensis were found incom- mercial peppermint, alfalfa and crimson clover fields involvingtwo areas (Willamette Valley, Great Basin) with very different climatic regimes. Second instar host larvae appeared to be the most commonly attacked stage in the field. There was no relationship between the numbers of host larvae collected in any one sample and theproportion of hosts parasitized in that sample. Thus, in peppermint fields, A. yakutatensis did not appear to respond in a dependentmanner to changes in host density.
Requirements for larval development and adult longevitywere investigated in the laboratory. When fed a thirty percent honey water solution, A. yakutatensis females lived anaverage of 18 days and males lived an average 16.5 days. When provided with water only, males and females lived an average of 2.5 days. The larvae of A. yakutatensis required 162 degree days above 10.5°Cto complete develop- ment, and pupae required 85 degree days above 9.4°C. Larvae of A. yakutatensis required 10.5 days to complete development at 26°C and passed through three instars. The first instar was mandibulate, and
the other two were hymenopteriform.The age of host attacked hadno
significant effect on the time required for developmentof A. yakutatensis at 26°C, but did affect the timerequired for the host
to reach the prepupal stage. The number of A. yakutatensis larvaeper host did not affect the percentage of larvae successfullyemerging from individual hosts, but therewas a negative relationship between the number of larvae per host and themean weight of adults produced by individual hosts. Aspects of the Field and Developmental Biology of Apanteles yakutatensis, a Parasitoid of Autographa californica.
by
Robert John Madar
A THESIS
submitted to
Oregon State University
in partial fulfillment of the requirements for the degree of
Master of Science
Completed June 3, 1982
Commencement June 1983 APPROVED:
Redacted for Privacy
AssieYantiltrofissor of-Efitomology in charge of major
Redacted for Privacy
Chairman, Entomology Department 67
Redacted for Privacy
Dean of Gradu t school (7
Date thesis is presented June 3, 1982
Typed by Robert John Madar. ACKNOWLEDGEMENT
Numerous people helped me to conduct the research reported in this thesis. In particular I wish to thank my major professor,
Dr. Jeff Miller, for his support (both moral and financial) during the last two and one-half years. I consider him to be a valuable adviser and friend. Ben Simko helped identify suitable peppermint fields in 1980, and Paul Hanson, Jim McIver, and Jan Cronhardt assisted in the sampling. I also wish to thank my wife Wendy Hadar for illustrating the larval instars and head capsule. Her drawings have made this thesis far more successful than it would have been without them. TABLE OF CONTENTS
I. Introduction 1 Statement of Problem 4
II. Literature Review 6
III. Parasitism of Autosrapha californica by Apanteles yakutatensis on peppermint in Oregon. 10 Abstract 11 Introduction 12 Methods and Materials 13 Results and Discussion 14 Endnotes 23
IV. Developmental Biology of Apanteles yakutatensis, a primary parasite of Autographa californica. 24 Abstract 25 Introduction 26 Methods and Materials 26 Results and Discussion 29 Endnotes 47
V. Conclusion 48
VI. References Cited 51 LIST OF FIGURES
Figure Page
1. Percent of Autographa californica in a sample parasitized by Apanteles yakutatensis as a function of the number of host larvae 19
2. Time required for parasite emergence from various instar hosts post collection 20
3. Larval stages of Apanteles yakutatensis 33
4. Schematic drawing of third instar head capsule of Apanteles yakutatensis 34
5. Relationship between temperature and developmental rate for larvae and pupae of Apanteles yakutatensis 37
6. Affect of parasitization on the length of development of Autographa californica 40
7. Affect of host load on the number of Apanteles yakutatensis successfully emerging from the host 44
8. Affect of host load on mean weight of adult Apanteles yakutatensis 45 LIST OF TABLES
Table Page
1. Number of Autographa californica collected and parasitized by Apanteles yakutatensis 18
2. Developmental times of larvae and pupae of Apanteles yakutatensis at five constant temperatures 36
3. Duration of Autographa californica larval development when parasitized as second, third, or fourth instar larvae 38
4. Head capsule sizes of parasitized Autographa californica larvae 41
5. Time to emergence of Apanteles yakutatensis when host was parasitized as second, third or fourth instar larvae 42
6. Affect of superparasitism on the numbers of Apanteles yakutatensis larvae successfully exiting the host and on mean adult weight 46 ASPECTS OF THE FIELD AND DEVELOPMENTAL BIOLOGY OF APANTELES YAKUTATENSIS, A PARASITOID OF AUTOGRAPHA CALIFORNICA
INTRODUCTION
The term biological control has different meandings depending
on the context in which it is used. When considered from an ecological
viewpoint, biological control can be defined as the action of parasites
predators, and pathogens in maintaining another organism's population
at lower levels than if these agents were absent (DeBach, 1964). This
definition is not adequate when speaking from an applied perspective,
as it does not consider the necessity of maintaining pest insect
populations below specified economic levels. Thus, the field of
biological control of insect pests ultimately concerns the suppression
of pest populations below economic levels by the manipulation of
natural enemies.
The field of biological pest control is quite diverse, and in a broad sense, can involve the use of microbial pesticides, host plant resistance, and cultural methods in addition to mammalian, avian,
and arthropod predators and parasites.However, much of the work which has been done in biological control involves the manipulation of enotmophagous insects (DeBach, 1964; Wilson and Huffaker, 1976).
Classical biological control involves the importation and release of exotic natural enemies, typically against non-native pests, and on occasion against native pest species. Recently, there has been more emphasis placed on the conservation and augmentation of indigenous natural enemies to suppress pest populations (Ridgeway and Vinson,
1976). This approach may involve: 1) manipulation of the habitat to 2
aid in the preservation of certain kinds of natural enemies (Doutt and
Nakata, 1973); 2) innoculative releases of a natural enemy whose pop-
ulations have been reduced by a previous pesticide application (Hart,
1972), or 3) innundative releases of large numbers of natural enemies
(Parker and Pinnell, 1972; Weseloh and Anderson, 1975).
Biological control has a number of advantages over the use of
pesticides in insect pest control. In many cropping systems, the use
of broad spectrum synthetic chemicals can decimate existing natural
enemy populations to such a degree that the pest populations are able
to resurge to much higher levels than they would be able to in the
presence of their natural enemies thereby requiring additional insect-
icide treatments. The use of these chemicals may also foster the
development of secondary outbreaks of potential pests that had
previously been under natural control. Secondary pest outbreaks may
the require additional applications of pesticidds which can cause
further disruptions, leading to still more insecticide treatments,
etc. (DeBach, 1974). This overuse of pesticides, which has been termed
the pesticide syndrome (Doutt and Smith, 1971) can result in excessive
environmental contamination and accelerated development of resistance
to insecticides in pest populations. Since biological control does not
rely on broad spectrum biocides, it offers a method of pest management which can avoid some of these problems.
One of the criticisms of biological control is that it has not yet become a predictive science, and partly because of this, it has not
enjoyed a high rate of success (Turnbull, 1967; Beirne, 1975). Often,
the limited availability of time and funds constrains the scope of 3
investigations dealing in the importation of exotic pests. Workers
are thus restricted to collecting what look to be suitable natural
enemies and sending them back to their home countriesas quickly as
possible. Numerous questions make this choice uncertain at best.
Should single or multiple species be introduced?Which species in an
assembleage of natural enemies should be selected? In the case of the winter moth, Operopthtera brumata (Linneaus),a tachinid, Cyzenis albicans (Fall.), did not appear to be contributing significantlyto winter moth mortality in its native England. However, this parasitoid was subjected to a large degree of winter mortality in England due to predation. When C. albicans was released in Nova Scotia against the winter moth, it was removed from this predationpressure and substan- tially reduced winter moth populations. This example illustrates potential difficulties which may be encountered when selectinga natural enemy for importation (Hassell, 1978).
What is needed to answer these and other questions about designing biological control programs is an adequate data base drawn from studies of parasitoid/host associations (Coppel and Mertins, 1977). Examinations of native associations, especially those in which the host appears to be under considerable natural control, can significantly contribute to this data base. For example, Miller (1977) reported results on the parasites of Spodoptera praefica (Grote) which tended to support multiple species introductions in biological control,a practice which has been the subject of debate among biological control workers
(Huffaker et al., 1971).
The thesis reported herein was inspired by the concerns mentioned 4 above, and prssenta the results of an investigation into a panasitoid/ host interaction that is native to western North America. The alfalfa looper, Autographa californica (Speyer) is a polyphagous noctuid moth that is native to the western half of North America (Eichlin, 1975).
It can reach economically damaging levels in a variety of truck crops
(Childs, 1938), and is an occasional pest in Oregon peppermint fields
(Berry, 1977). However, A. californica is generally under a considerable degree of natural control (Puttarudruiah, 1953)
Clancy (1969) reported that A. californica is attacked by a number of parasites in Southern California alfalfa fields, and one of the most common species was Apanteles yakutatensis (Ashm.), a braconid endoparasite. This parasite is distributed throughout the western United States, and has been recorded to complete development in larvae of Amanthes c-nigrum (Linneaus), Autographa californica and
Autoplusia egena (Guenee) (Krombein et al., 1979). Preliminary work carried out in 1979 by Miller (unpublished data) indicated that
A. yakutatensis is a common parasite of A. californica in Oregon peppermint fields.
Oregon is major producer of mint oil in the United States, and a large acreage is devoted to mint production. This, coupled with the fact that mint is easily sampled with a standard sweep net makes this system a convienent one for studying a parasitoid/host association in in what is essentially an annual crop.
The information reported in this thesis is the result of a two year investigation of the behavior and ecology of A. yakutatensis.
Also included are results of an examination on the distribution and abundance of A. yakutatensis in two of Oregons major mint producing 5 areas, the Willamette Valley and the area around Madras. In addition, a determination of seasonal trends in abundance of A. yakutatensis in a number of mint fields in both locations was made. In the lab, investigations were conducted on: 1) heat unit requirements for development of A. yakutatensis; 2) parasitoid/host developmental interactions; 3) superparasitism; 4) host load relationships and
5) larval morphology. 6
LITERATURE REVIEW
There is little information in the literature concerningthe
biology of either Autographa californicaor Apanteles yakutatensis
other than that mentioned in the introduction. Much of the work that
has been done on A. californica is concerned with the cultureand
manipulation of viral and bacterial pathogens which have beenisolated
from larvae of this species (Lee and Miller, 1978;Vail et al.,
1970,1973).
Many of the studies involving the determination ofpercent parasitism of host organisms in the field have involved sampling the host population, rearing the samples in the laboratory, and thenre- cording the number of parasites which emerge from the sample. Percent parasitism is then determined by dividing the number of parasites present by the total number of hosts in the sample (Barry, 1970;
Burleigh, 1971, 1972; Clancy, 1969; Herzog, 1977; Lentz and Pedigo,
1975; Smith et al., 1976). This method can serve as a rough approxi- mation, but it may give erroneous results. One source of error which can be very troublesome when working with parasites of lepidopterous larvae arises when estimates of percentage parasitism are based on a broad range of host stages, but the parasite only attacks one or two stages of the host (Marston, 1980). If the parasite attacks an early larval stage and emerges from the penultimate or last stage, the sampling on a weekly basis may overestimate the degree of parasitism because members of a given generationmay be counted twice. This source of bias can be eliminated by determining the percent parasitism of an intermediate instar whichoccurs after 7
parasite oviposition in the field, and prior to when the parasite
emerges.
The rate of development of poikliothermic organisms suchas
insects is strongly influenced by temperature (Belehradrek, 1926;
Davidson, 1944; Howe, 1967; Sanderson, 1910), and analyses of this
relationship have been used to predict various phenological events in
insects. In pest management programs, physiological time has been used
to predict population trends of pest insects so as to optimally time
control tactics (Ali Niazee, 1975; Bailey, 1976; Butler and Scott,
1976: Sterling and Hartsack, 1979).
The ability of an insect parasite to regulate or supress its host
is partly due to the turnover rate of successive parasite generations, and the rate of turnover is largely dependent upon temperature effects on parasite behavior and development (Campbell and Mackauer,
1975; Ables et al., 1976). In addition, knowledge of the temperature requirements for the development of a host and its parasites yields
information on their degree of synchrony (Campbell et al., 1974
Obrycki and Tauber, 1978).
There are numerous methods by which the thermal requirements for insect development can be determined. Some workers have employed relatively sophisticated analytical techniques to design computer simulation models of the response of an insects development to temperature changes (Barfield et al., 1977; Logan et al., 1976;
Sharpe et al., 1977; Stinner et al., 1974). However, in many applica- tions these models do not offer a greatly improved level of precision over simple. models to justify the effort required for their development
(Stinner et al., 1975) 8
A less complicated method for describing the relationship
between temperature and the rate of development ofan insect is
the linear degree-day or heat unit model. This method involves
rearing samples of individual insects at various constant temperatures and then regressing the reciprocal of the mean development time against temperature (Arnold, 1959). By extrapolating the resulting regression line to the abcissa, an estimation of the developmental thresholdcan be made. The number of degree-days necessary to complete development can be determined by the following formula: DD = (T-th)Dt, where T = constant temperature, th = developmental threshold and Dt== development time in days (Bari and Lange, 1980). These types of models have been used to describe the thermal requirements of a variety of insect species (Butler and Hamilton, 1976; Butler and Scott, 1976; Chmiel and
Wilson, 1979; Eckenrode et al., 1975; Elsey, 1980).
A considerable amount of research has been conducted on the larval morphology and developmental stages of parasitic Hymenoptera, and several good reviews of earlier literature exists (Clausen, 1940;
DeBaah, 1964). Short (1978) provides keys and descriptions of the final larval instars of the subfamilies of the Ichneumonidae, in which there appears to be remarkable agreement between the classification system of the adults and a scheme based on the larval characters.
Short (1953) also demonstrated that larval characters indicate a grouping of species of the genus Apanteles that is very similar to a grouping based on adult characters.
Various aspects of host regulation by insect parasitoids have been reviewed by Vinson and Iwantsch (1980). It is apparent that the 9 effects of parasitism'on the host vary between different associations.
In some cases the larval period of the host may be lengthened after parasitism (Doudu and Davis, 1974; Jones et al., 1981), accelerated
(Varley and Butler, 1933), or it may remain unaffected (Vinson and
Barras, 1970; Iwantsch and Smilowitz, 1975). Parasitization of a host may also result in the induction of supernumary instars (Beckage and
Riddiford, 1978). Conversely, the life stage of host attacked can have affects on the developmental rate of the parasite as well. Corbet
(1968) reported that the first larval instar of Nemestris canescens
(Holmgren) lasted longer in young caterpillars of its host Ephestria kuehniella (Zell.) than in older larvae because the first instar parasite larvae feed and grow very slowly in young hosts, but are able to grow faster if transferred to older host caterpillars. Similar results have been reported by Jones and Lewis (1971) for Microplitis croceipes (Cresson), Sato (1980) for Apanteles glomeratus (Linneaus), and Vinson and Barras (1970) for Cardiochiles nigriceps Viereck. 10
Journal of Economic Entomology Correspondence to:
Jeffrey C. Miller Department of Entomology Oregon State University Corvallis, Oregon 97331
Parasitism of Autographa californical/ by Apanteles
yakutatensis2jon peppermint in OregonJj
Robert J. Madar
and
Jeffrey C. Miller
Department of Entomology, Oregon State University
Corvallis, OR 97331 11
ABSTRACT
Field studies indicated that Apanteles yakutatensis wasa relatively common parasite of Autographa californicaon peppermint.
Adult parasites were active throughout much of the growingseason
(June - September) and were present at all locations sampled. Para- sitism by A. yakutatensis within individual samples of field-collected third and fourth instar hosts ranged from 7 to 71% atseven different study sites. Larval A. yakutatensis develop as gregarious endoparasites in second to fifth instar hosts. An average of 29 parasites emerged per host with a highly variable sex ratio, generally 4 t:1ot. A hyper- parasitoid, Stichtopithus sp., was observed to be rare. 12
The alfalfa looper, Autographa californica (Speyer), is a polyphagous agricultural pest native to the western half of North
America (Eichlin, 1975) capable of reaching damaging levels in crops such as spinach, lettuce and alfalfa (Childs, 1938). In Oregon,
A. californica is a pest on peppermint, Mentha piperita Linneaus, and may require occasional insecticidal treatments (Berry, 1977).
Populations of the alfalfa looper are generally under a con- siderable degree of natural biological control. In Southern California alfalfa fields, A. californica populations have appeared to be sup- pressed by a number of natural enemies (Puttarudriah, 1953; Clancy,
1969). In Oregon peppermint fields, A. californica larvae are attacked by a number of insect parasites, with levels of parasitization capable of reaching 90+% (J.C.M., unpublished data).
One of the more common parasites of A. califurnica is the gregarious endoparasite, Apanteles yakutatensis (Ashur.). A. a yakutatensis is distributed throughout the western Unites States, with a host list consisting of three species: Amanthes c-nigrum Linneaus,
Autographa californica and Autoplusia egena (Guenee). Madar (1982) examined aspects of the developmental biology of A. yakutatensis in the laboratory.
In this paper, we report the results of field studies which evaluated the distribution and abundance of A. yakutatensis in two very different areas of Oregon where peppermint is grown. We monitored host density, host age class, and percent parasitism to determine trends in the abundance of A. yakutatensis throughout the growing season. We also report on the number of parasites emerging per host, parasite sex 13
ratio, and the incidence of hyperparasitism.
METHODS AND MATERIALS
Extensive sampling.-Two of the major peppermint growing areas
in Oregon are separated by the Cascade Mountains and are characteriaed by very different climatic conditions. The Willamette Valley is west of
the Cascades and has cool rainy winters (101 to 153 cm annually) and warm dry summers.Average temperatures range from max.-min. of 25.5 -
9.7°C and 8.9-0.17°C during summer and winter, respectively. East of the Cascades, in central Oregon, the climate is drier with a wider
range in temperatures. Annual precipitation is between 25.4 to 35.5 cm with summer and winter temperatures ranging from a max.-min. of 28.7 -
7.22°C and 7.1-3.7°C respectively. In the summers of 1980 and 1981,
two peppermint fields were selected in each region for extensive-
intensive sampling.
In addition to the eight primary study sites, seven secondary study sites were extablished for extensive sampling. Four peppermint
fields (40-75 ha.) were selected to be sampled at least twice (500 sweeps/sample date) during the growing season. Three of these were within 48km north of Corvallis and the fourth was located 128km north of Corvallis near Brookes. Also, in 1981, two fields of crimson clover (Trifolium incarnatum Linneaus) were sampled in may by taking
250 sweeps in each field. One of these fields was located near Corval- lis, and the other was 96km north near Amity, Oregon. On September
15, 1981 a small (ca. 2 ha.) field of alfalfa was sampled by taking
150 sweeps.
Intensive sampling.- In 1980, four mint fields (41 - 72 hs.) 14 were selected for intensive sampling, two in the Willamette Valley near
Corvallis, and two east of the Cascades near Madras, Oregon. Three of these fields were sampled weekly with a standard (38 cm dia.) sweep net from late June until the mint was harvested in August. Sampling in the fourth field was discontinued after a pesticide application and the data from this field will not be included in this report.
Sampling was conducted in the following manner. Starting near the edge of the field, a series of fifty sweeps were taken along a transect approximately 50m long. The transect was then shifted laterally three meters and another 50 sweeps were taken. This process was repeated until a total of 500 sweeps were conducted per field. The larvae collected in each set of 50 sweeps constituted a subsample.
Subsamples were placed in plastic cups with a mint sprig and put into a cooler until they were returned to the lab. After recording species and instar collected, individual larvae were put in 1-oz. plastic cream cups and fed an artificial diet which was changed every two days. The date of emergence of parasite larvae from the host was recorded as was the date of parasite adult emergence.
A similar program was followed in 1981, but the same fields were not sampled due to a reduction in mint acreage between 1980 and 1981.
One of the fields sampled in 1981 (#7) had very low numbers of
A. californica and data from this field were not included in the presentation of seasonal trends and the abundance of A. yakutatensis.
RESULTS AND DISCUSSION
Extensive sampling.- Larvae of A. californica were commonly parasitized by A. yakutatensis throughout the summer and in the various 15 crops studied. All fields sampled possessed populations of A. yakutatensis. A total of 1,392 A. californica larvae were collected of which 13.1% were parasitized by A. yakutatensis. Within the respec- tive crops were 1) peppermint: 1,338 larvae, 12.9% parasitized by
A. yakutatensis; 2) alfalfa: 11 larvae, 45.5% parasitized, and 3) crimson clover: 43 larvae, 9.3% parasitized. The comparison to be made here is qualitative rather than quantitative. These data demonstate that A. yakutatensis was capable of colonizing hostsover a broad geographical region in different agroecosystems.
Intensive sampling.- Intensive sampling of peppermint demon- strated a marked reduction in the number of A. californica larvae present between 1980 and 1981. In 1980, a total of 1,002 (0.1 larva/ sweep) larvae were collected. In 1981, this total was reduced to 336
(.035 larva/sweep) which resulted in correspondingly fewerrecoveries of A. yakutatensis.
A standard procedure for evaluating parasiteoccurrence is needed before general comparisons of parasitism ratescan be conducted.
Studies of percent parasitism of host organisms in the field have generally-involved sampling the host population, rearing larvae in the laboratory, and then recording the number of parasites whichemerge from the sample. Percent parasitism is then determined by dividing the number of parasites present by the total number of hosts in the sample
(Barry, 1970; Herzog, 1977; Lentz and Pedigo, 1975; Smithet al., 1976).
This method can serve as a rough approximation but itcan also give erroneous results.
There are several factors which can confound estimations ofpercent 16
parasitism in the field (Marston, 1980). The exposure of hosts to
parasites may be curtailed when they are removed from the field. For
example, if the third instar of a lepidopterous pest is the stage most
commonly attacked by a parasite, then removing this or earlier instars
from the field will lessen the period of exposure to attack, and may
lead to an underestimation of percent parasitism. Percent parasitism
can also be underestimated by not deleting the numbers of hosts which
do not survive collection because it is difficult to determine which hosts would or would not have produced parasites had they survived.
Another source of error results when the frequency of sampling is
shorter that the time period for a parasitized host to complete its development in the field. For example, in the case of A. yakutatensis, adult females commonly oviposit into second instar larvae in the field
(see below), and the parasite larvae always emerge from fifth instar hosts. Thus, sampling on a weekly basis and determining percent parasitism from the total sample may overestimate the proportion of hosts parasitized because a given cohort may be sampled more than once. This source of error can be minimized by determining the percent parasitism of a particular instar.
In order to minimize these sources of error for the present parasitism of A. yakutatensis on A. californica only the numbers of parasites emerging from the total number of pooled third and fourth instar hosts surviving collection were used to determine the actual population reduction due to this parasite. These two stages were used because, on a weekly sampling program, the cohort would not be counted twice. Second instar host larvae were not included in this analysis 17
because of the possible interruption of theirexposure to the parasite.
Fifth instar hosts were not considered becausesome of them could have
either completed development and pupated or produced parasitesbetween
sampling dates.
The number of A. californica larvae collected andparasitized
by A. yakutatensis in peppermint is presented in Table1. Once the
standardizations were made it became apparent that calculationsof
precent parasitism based on all age classes tended to underestimate
parasitism of those life stages actually utilized by theparasite.
There appears to be no relationship between the number ofhost
larvae attacked by A. yakutatensis and host density. The relationship
between percent parasitism of pooled third and fourth instarhost larvae
and number of host larvae for all fields sampled in 1980is given in
Fig. 1. The 1980 results were pooled because therewere no apparent
differences between fields, and there wereno observable trends over the
season. The 1981 results were essentially thesame as the 1980 data
and are not presented here. It seems clear that in the peppermint
fields studied, A. yakutatensis appeared to respondindependent of host
density.
As previously discussed, information on the host lifestages attacked and occupied by respective parasites isnecessary for evaluat- ing rates of parasitism. The stage preferred for parasite oviposition can be empirically derived from field and laboratory data. The relationship between the mean length of time required for thedevelop- ment of A. yakutatensis larvae after the hostwas brought in from the field and the host instar collected is presented in Fig.2. The length Table 1. Number of Autographa californica (Ac) larvae collected and parasitized by Apanteles yakutatensis (Ay) in peppermint fields in Oregon, 1980-1981.
Ac Ay % Parasitism b/ Total 3+4 Total 3+4 Total 3+4
1980 1 386 148 64 36 16.5 24.3
2 348 106 23 36 6.6 34.0
3 115 30 18 5 15.7 16.7
1981 5 129 84 14 11 10.9 13.0
6 36 14 21 10 58.3 71.4
7 47 23 2 2 4.3 8.7
8 124 17 9 4 7.3 23.5
Overall 1,185 422 151 104 119.6 191.6
VFields1, 2, 5, 6 located near Madras, fields 3, 7,.8 located near Corvallis, field 4 omitted due to insecticide use.
1VNumbersonly consider host larvae collected as third or fourth instars. Fig. 1. Percent of Autographa californica ina sample parasitized by Apanteles yakutatensis as a function of the number of host larvae.
50
40
30
20
1 0-0-
alit a 10 20 30 40 50I 60 70 80 NUMBER OF A CALI FORNICA PER SAMPLE 20
Fig, 2. Relationship between the number of days required fro parasite emergence from a host after collection and the instar of that host at the time of collection (25°1' 3°C), Oregon, 1980.
19 Ile
18
IT
16
15 Oa
14 9.19.9-3.3x
13
I2
110111111
10
1111101111
Ole
111111011011.1111110
OS*
2 3 4 5 HOST INSTAR COLLECTED 21 of time required for A. yakutatensis to develop after being field- collected was longer for those parasites collected inyounger host
instars that for those collected in older host instars. The amount of time required for parasite emergence for the various host instars was (X -± S.D.) 13.3± 2.5 days for second instars, 10.1± 1.8 days for third instars, 6.5± 2.8 days for fourth instars, and 3.71:1.8 days for fifth instar hosts. Given that the developmental time of A. yakutatensis larvae at 26°C was 10.5 days, and that development was not affected by the stage of host attacked (Hadar, 1982), these data suggest that A. yakutatensis generally attacked second instar host larvae in the field.
The numbers and sex ratio of A. yakutatensis emerging froman individual field-collected host were highly variable. Based on a randomly collected subsample of thirty-nine A. yakutatensis colonies reared from host larvae collected from peppermint fields in 1980,a mean of 29 (S.D. = 11.9, range 2-69) adult A. yakutatensis emerged per host. The mean sex ratio (female:male) was 4.1:1 (S.D. = 2.7:1, range
12.7-0.1:1).
A hyperparasite, Stictopithus AR., was reared from field collected A. clalfornica parasitized by A. yakutatensis. In 1980,
140 host larvae parasitized by A. yakutatensis were collected between
June and August of which two (1.43%) were hyperparasitized. In 1981, three (5.3%) of 58 A. yakutatensis colonies contained Stictopithus R.
Hyperparasitism was 100% within two of the primary parasite colonies and
60% in the third.
The results of the present study demonstated that A. yakutatensis 22 was geographically widespread, common throughout the growing season, a numerically dominant species in the guild of parasites, and capable of exploiting a large portion of the host population. This information along with additional investigations into the ecological relationship between A. yakutatensis and the other parasites of A. californica will contribute to a better understanding of interactions in parasite guilds and their composition. 23
Endnotes iLepidoptera: Noctuidae
2Hymenoptera: Braconidae
30regon. State University Agricultural Experiment Station Technical
Paper No. . Recieved for Publication 24
Annals of the Entomological Correspondence to: Society of America Robert J. Madar Department of Entomology Oregon State University Corvallis, OR 97331
Developmental Biology of Apanteles yakutatensiAL/,
a Primary Parasite of Autographa californicaY.
Robert J. Madar
Department of Entdmology, Oregon State University
Corvallis, OR 97331 25
ABSTRACT
The developmental biology of Apantelesyakutatensis (Ashm.),
a primary gregarious larval endoparasite of the alfalfalooper,
Autographa californica (Speyer) was investigated. When fed a thirty
percent honey water solution adult parasites livedan average of
18 and 16.5 days, females and males respectively. However, with
water only, adult parasites lived anaverage 2.5 days. Larvae of
A. yakutatensis required 10.5 days to developat 26°C and exhibited
three instars. The first instar was mandibulate, whilethe other two were hymenopteriform. The larvae required 162 degree-daysabove 10.5°C and pupae required 85 degree-days above 9.4°Cto complete development.
The age of the host when parasitized hadno significant effect on the time required for development of A. yakutatensisat 26°C. However, the age of the host when parasitized did affect the time required forthe host to reach the prepupal phase, thestage from which A. yakutatensis will emerge. Hosts parasitized as fourth instars requireda longer period of time to reach the prepupalstage than did those parasitized as younger instars. The number of A. yakutatensis larvaeper host did not affect the percentage of parasite larvae successfully emerging from an individual host, but there wasa negative relationship between the number of parasite larvae per host andthe mean weight of parasite adults. 26
A gregarious endoparasite, Apanteles yakutatensis (Ashm.), is native to western North America and has been reported to parasitize larvae of Amathes c-nigrum (Linneaus), Autographa californica (Speyer) and Autoplusia egena (Guen.) (Krombein et al., 1979). The femalewasp will oviposit into younger host instars. Larvae emerge from host prepupae and spin a common silk mass within which they construct individual pupal cells. In Oregon, A. yakutatensis appears to produce several generations per year (Madar, 1982).
The alfalfa looper, A. californica, appears to be a suitable, if not favored, host for A. yakutatensis. Clancy (1969) reported that
A. yakutatensis was a common parasite of A. californica on alfalfa in
Southern California and Madar (1982) found it to be one of the most common members of'the parasite guild associated with A. californica on peppermint in Oregon. Information on the life history of A. yakutatensis is lacking. Thus the developmental biology of A. yakutatensis was studied using A. californica as a host resource.
METHODS AND MATERIALS
The following studies were conducted in the laboratory in 1980 and 1981:1) a determination of the effect of food on the longevity of adult A. yakutatensis; 2) description of the larval stages of A. yakutatensis; 3) determination of the developmental threshold and heat unit requirements of A. yakutatensis; 4) the effects of host age on the developmental rate of A. yakutatensis; and 5) the effects of host load and superparasitism on the numbers of A. yakutatensis successfully completing development.
In all of the experiments, the parasites and hosts were handled in the following manner: All experimental adult parasites were 27
reared directly from field-collected A. californica larvae on pepper-
mint near Corvallis, Oregon. Experimental host larvae were taken from
a laboratory population of A. californica which had been reared at
26°C, 12L:12Don an artificial diet (Bio-Sery #773-4) for three
generations. Adult wasps were held in sleeve cages in the laboratory
and fed a 30% honey solution. Hosts were offered to a female wasp by
putting a larva on a piece of gauze covering the mouth of a pint jar,
placing glass tubing containing the wasp over the larva, and the
forcing the wasp down onto the larva by blowing through a plastic hose
attached to the tube. In all experiments, except the developmental
threshold analysis, parasitized larvae were held at 26°C, 85% R.H.,
12L:12D and fed the artificial diet mentioned above. The diet was
changed every two days.
Adult Longevity.- Six males and six females were randomly
selected from each of four different colonies of A. yakutatensis.
Based on .a completely randomized design, one female and one male were
assigned to each of 24 quart jars. Twelve of the jars received a
thirty percent solution of honey in distilled water, the other twelve
jars received distilled water. Wasps were then observed twice daily
to determine the time of death.
Larval Parasite Morphology.-In 1980, 100 third instar larvae of
A. californica were parasitized by A. yakutatensis and placed in the
26° chamber. At 24 hour intervals, ten host larvae were removed, boiled in water for 3 min. and preserved in 80% EtOH for later dis-
section. Upon dissection, the eggs and younger parasite larvae were mounted on glass microscope slides in Hoyers solution. Older parasite larvae were boiled in a 10% solution of KOH, rinsed in diStilled water, 28
stained with a 10% crystal violet solution forone to two minutes
and mounted on glass microscope slides in Hoyers solution (seeNagy,
1978). Egg and larval dimensions were measured using a calibrated
ocular micrometer in a binocular dissecting microscope and mandibular
dimensions were measured using an ocular micrometer in a compound
microscope.
Developmental Threshold and Heat Unit Requirements.- Twenty
parasitized third instar host larvae were placed inone of five
constant temperature cabinets set at either 11, 16, 21, 26, or 31°C.
Temperature assignments were based on a completely randomized design.
Observations were conducted twice daily until adult parasiteemergence.
The occurence of parasite larvae exiting the host and pupatingwas
noted, as was the emergence of adults from thecoccoon. The
theoretical threshold for development (t) was estimated by regressing
the reciprocal of the developmental time in days againsttemperature
and then extrapolating the resulting regression line to the abcissa
(Campbell et al., 1974). The thermal constant (K) was calculated
from the equation K Y(d - t), where y is the mean developmental time
in days, d is the temperature (0C), and t is the theoretical threshold
for development (Andrewartha and Birch, 1954).
Host Age: Parasite Development.- A total of three hundred A. californica eggs were separated from the stock laboratory culture, placed in the 26°C cabinet and observed every eight hours to accurately monitor host age. Each of the five host instars were tested relative to the effects, if any, that age of the host might have on the rate of development of the parasite at 26°C.Twenty-five host larvae which 29
had molted within the preceeding four hours (exceptfirst instar host
larvae which were one day old) were subjectedto parasitization by
A. yakutatensis. Fifty non-parasitized host larvaeserved as a check
treatment. All larvae were observed at twelve hourintervals, with
the duration of each instar and the time ofparasite emergence being
recorded.
Host Load and Superparasitism.- Fourty third instar host larvae which had molted within the previous eight hourswere parasitized by mated female A. yakutatensis and placed in the 26°Cchamber. The
larvae were checked daily for parasiteemergence, after which the host remains were held an additional two days and thenboiled in water for three minutes and preserved in 80% EtOH for laterdissection. Twenty third instar host larvae were parasitized by A. yakutatensis,held at
26°C for one hour and then parasitized byan additional twenty
A. yakutatensis females. These larvae were then returned to the 26°C cabinet and treated in the same way as the previous sample. All adult parasites which emerged in both experimentswere killed by freezing and then dried at 35°C for four weeks in orderto obtain dry weights.
RESULTS AND DISCUSSION
Adult Longevity.- The longevity of A. yakutatensis adultswas significantly increased when they were provided witha sugar food source (P4;0.05, n = 12). Female wasps lived an average of 18±1.0 days when provided with a thirty percent solution of honeywater, and
2.51.0.5 days when given distilledwater only. Males lived an average of 16.5±1.0 days when given the honey water and only 2.3±.5 dayswhen provided with distilled water. 30
Larval Stages.-Dissection of third instar host larvae two days after parasite oviposition demonstrated that theeggs of A. yakutatensis were unattached and floating within the host haemolymph, and occured in aggregations in the region of abdominal segments eight and nine. Two days after ovipostion, the parasite egg was elongate, translucent, and slightly clavate in appearance (Fig 3a). The mean length and width was 0.229+0.03mm and 0.0348±0.0001mm respectively
(n = 10). The developing larvae were clearly visible inside the chorion by three days after oviposition. At this point in development, the egg was 0.347±0.003mm long and 0.075±0.002mm wide (Fig. 3b).
The first instar larvae had eclosed by the fourth day after oviposition. All of the hosts examined contained first stage
(mandibulate) larvae which were aggregated into a large clump in the same area as were the eggs. The body was translucent with a slight taper toward the caudal end (Fig. 3c). Young first instar larvae did not show a well defined segmentation, but by the second day after eclosion, segmentation was more obvious, exhibiting three thoracic and seven abdominal segments. The young larvae were
0.487-0.02mm long and 0.103-0.002mm wide (n = 12). The mandibles were relatively large in camparison to the head capsule, and were supported by thickened rodlike areas of cuticle. First instar mandibles were 0.041±0.001mm long and 0.002±0.0002mm wide. The anal vesicle was not well developed in young first stage larvae, but by the second day after eclosion, it had increased in size and appeared to be well developed. The first instar developed over a period of four days at 26°C. 31
The second instar larva was hymenopteriform (see Hagen, 1964) with thirteen well defined segments, and measured 3.5-0.10mm long by
0.57- 0.01mm wide (n = 12) (Fig. 3d). The anal vesicle was prominent and well defined. The cephalic structures were weakly sclerotized and difficult to see, but posessed a pair of mandibles which measured
0.061±0.001mm long and 0.005±0.002mmwide. The midgut was not connected to the hindgut and occupied the central portion of the body cavity. The cuticle was smooth and appeared to lack setae except in the region of the anal vesicle. The tracheal system was well developed with two longitudinal trunks which were connected in the last abdominal segment, and from this point a common trunk extended toward the anal vesicle. No spiricles could be seen in this instar. This stage developed over a period of one day at 26°C.
The third instar larva was clearly visible through the cuticle of the second instar by the ninth day after oviposition. It appears that the cuticle of the second instar completely enveloped the third instar larva until the parasite was ready to emerge from the host.
This makes it difficult to determine when the second stage ends, but in the case of A. yakutatensis the third instar larva was well formed
48 hours after the molt to the second instar. This appears to be a common pattern among the Microgasterinae (Allen, 1958; Clausen, 1940).
Cardona and Oatman (1971) found that the second instar of Apanteles dignus Mues. lasted for one day, but they did not report the develop- ment of the third instar within the cuticle of the second.
The third instar larva was creamy white in color with thirteen well defined segment. The cuticle was not smooth as for the second 32
instar, but was ornamented with many small conical projections and
appeared to be lightly sclerotized or pigmented:.___ The anal vesicle was
still present, but it decreased in size as the larva matured. By the
time the larva exited the host, the anal vesiclewas absent. Young
third stage larvae were 4.25±0.05mm long and 0.785- 0.02mm wide (n= 12)
and tapered toward both ends. The tracheal system was well developed
and similar to the second instar except that eight pairs of spiracles
were present: one pair on the second thoracic segment and one pair on
each of the first seven abdominal segments. Third instar larvae
developed over a period of three days at 26°C (Fig. 3e).
The cephalic structures were well developed and are described
according to the terminology of Short (1952,1953). The mandibles
were sclerotized, bluntly pointed, and appeared to be crossed at the
tips when not extended. Third instar mandibles measured 0.07±0.003mm
long and 0.005-.0004mm wide. The mandibles articulate with. the
pleurostoma, which showed a marked differentiation between anterior
and posterior processes. The hypostoma formed a semicircle which
partially surrounded the stipital sclerite, and appeared to be
connected to the pleurostoma. The labial sclerite was U shaped, with
the stipital sclerites extending laterally from it toward the hypo-
stoma. The labial sclerite enclosed the prelabrum, the paired
papillose labial palpi and the silk press and orifice. The papillose
maxillary palps were smaller than the labial palpi and were situated ventral to the pleurostoma but close to the dorsal end of the labial
sclerite (Fig. 4)
Heat Unit Requirements.- The mean developmental rates of A. 33
Fig. 3. A, egg of A. yakutatensis 48 hours after oviposition; B, egg of A. yakutatensis 72 hours after oviposition; C, first instar larva of A. yakutatensis (av, anal vesicle; 1p, labial process; md, mandible); D, second instar larva of A. yakutatensis (av, anal vesicle); E, third instar larva of A. yakutatensis.
-----av 34
Fig. 4. Schematic drawing of mature third instar Apanteles yakutatensis head capsule ( pls, pleurostoma; hst, hypostoma; hsp, sclerotic spur of hypostoma; mplp, maxillary palp; 1plp, labial palp; lbs, labial sclerite; prlb, prelabium; slo, silk orifice; sp, silk press;ss, stipital sclerite; lm, labrum; md, mandible).
md Im
SS
prlb 35 yakutatensis larvae and pupae under various constant temperatures are presented in Table 2. These results are also presented in Fig. 5 to illustrate regression lines fitted to the data. Larvae of A. yakutatensis required 162 degree-days above 10.5°C to complete develop- ment, and pupae required 85 degree-days above 9.4°C. The predicted larval developmental threshold of 10.5°C agreed well with the result obtained from the sample reared at 11°C, which did not exit the host after a period of five months. Dissection of the host larvae at the end of this period showed that all larval instars of A. yakutatensis were present in the host. Thus, 110C was close to the developmental threshold. Dissections of host remains of the sample reared at
31 °C also revealed the presence of all three larval instars, indicating that 31°C is approaching a high temperature threshold for this species.
Host Age:Parasite Development.-Apanteles yakutatensis was capable of parasitizing second, third, and fourth instar larvae of
A. californica in the laboratory. All first instar larvae died within 24 hours after being parasitized (n = 25). All fifth instar host larvae completed normal development and pupated following oviposition by A. yakutatensis (n = 25).
Parasitization can have dramatic effects on the development of the host (Vinson and Iwantsch, 1980), and A. yakutatensis exhibited a strong influence on the developmental rate of its host at 26°C. Data are presented in Table 3 on the time required for A. californica to develop from the second instar to the beginning of the prepupal stage
(cessation of host feeding) for host larvae that were not parasitized 36
Table 2. Developmental times (days) of larvae and pupae of A. yakutatensis reared at five constant temperatures.
Temperatures) N Life Stages
oc Larva Pupa
11 17 150x *
16 15 46.0*11.5 18.4'0.6
21 19 13.0-+1.0 6.4±1.4
26 20 10.51'0.64 5.0-+ 0.38
31 16 8.8±0.57 4.5-+ 0.31 aComplete development at 11°C did not occur within 150 days. Fig, 5. Relationship between temperature and developmental rate for Apantelesyakutatensis, A pupae, B larvae.
.12 A .21B
.22
.10 .20
.09 .10
.16
.14
.12
.10-
.04 .00 ..11111- AIM
.05 .06
.02 .04
.01 .02
1 1 16 21 26 31 11 16 21 26 31 II 1( MPERA1URE (*C TEMPERATURE( *c I Table 3. Duration in days of Autographa californica development when parasitized as second, third, or fourth instars.
Instar Instar Parasitized N 2 3 4 4A/ 5 Total
Control 20 1.8± 0.31 1.9± 0.8 2.1± 0.2 2.4± 0.2 8.3± 0.3
Second 14 1.5± 0.1 2.4± 0.2 2.2± 0.3 2.5± 0.3 8.6± 0.2
Third 16 1.8± 0.3 2.7± 0.3 2.7± 0.6 3.4± 0.6 10.6± 0.5
Fourth 19 1.8± 0.3 1.9± 0.8 3.1± 0.5 2.6± 0.6 2.5± 0.6 12.4± 0.5
A/ Supernumary instar. 39 vs. those parasitized as second, third, or fourth instar larvae. A strong relationship existed between the length of time required for the host to attain the prepupal stage and the time at which the host was parasitized (Fig. 6). The later the host was parasitized, the longer it took to complete development. In addition, all host larvae which were parasitized immediately after the third molt
(fourth instar larvae) produced a supernumary instar with a head capsule width that was intermediate between the size of fourth and fifth instar head capsules (Table 4). This supernumary instar was not observed in any of the other treatments. Lengthening of the larval period of the host and the induction of supernumary instars after paraSitization have been documented in other parasite-host associations (Beckage and Riddiford, 1978; Duodu and Davis, 1974;
Miles and King, 1975; Smilowitz and Iwantsch, 1973).
A number of studies have shown that the stage of the host attacked has a strong effect on the developmental rate of the parasite (Corbet,
1968; Jones and Lewis, 1971; Sato, 1980; Vinson and Barras, 1970). It appeared that the instar of host parasitized did not have any sig- nificant effect on the developmental rate of A. yakutatensis at
26°C (Table 5).
Host Load and Superparasitism.- The number of parasite larvae emerging from a host has been used as an index of the effect of host load on successful parasite development for other gregarious parasites
(Beckage and Riddiford, 1978; Thurston and Fox, 1972).When the number of A. yakutatensis larvae actually emerging from the host were plotted against the total number of larvae emerging from the host Fig. 6. Time required (in days) for development from the beginning of the first instar to beginning of the prepupal phase for Autographs californica larvae that were unparasitized or parasitized in the second, third or fourth instar.
12.5
12.0
II .5 U) >- 04 I 1.0 10.5
10.0 9.5 9.0 8.5 8.0 1 NOT 2 3 4 PARASITIZED 41
Table 4. Head capsule sizes (mm) of Autographa californica parasitized as third or fourth instar larvae.
Instar Instar Parasitized N 3 4 4 5
3 15 1.2 ± 0.02 1.5 ± 0.03 1.8 ± 0.07
4 20 1.4 ± 0.04 1.6 ± 0.02 1.9 ± 0.06
Supernumary instar 42
Table 5. Time to emergence (days) of Apanteles yakutatnesis larvae when Autographa californica were parasitized as second, third, or fourth instars.
Host Instar Days to a/ Parasitized N Emergence
2 14 9.9
3 16 10.4
4 19 10.2
WValuesnot significantly different, one way analysis of variance. 43
(Fig. 7), there was no apparent relationship between host load and
successful emergence in the laboratory (r2 = .0128).
The mean weight of adult A. yakutatensis plotted against the
total number of larvae in the host is presented in Fig. 8. Regression
analysis of these data indicated that high numbers of parasite larvae
in the host had a weak negative effect on the weight of the adults
(r2= .2692). When host larvae were superparasitized, the overall
effect of host load on the number of larvae emerging was not
significant. However, there was a significant (P4:0.05) decrease in
adultweight (Table 6).
The results demonstrated that certain aspects of the developmental biology of A. yakutatensis are similar to those of other gregarious and solitary Apanteles which have been studied (Beckage and Riddiford,
1978; Cardona and Oatman, 1971). Salt (1933) stated that the penalties resulting from superparasitism may not be as severe for gregarious parasites as they are for solitary species, and the results obtained from A. yakutatensis tended to support this statement. The develop- mental relationships between A. yakutatensis and its host show some similarities to results obtained by other investigators (Beckage and
Riddiford, 1978; Jones et al., 1981), but differ from the results obtained by others (Sato, 1980), indicating that these relationships are complex and variable in nature. Fig. 7. Effects of the number of Apanteles yakutatensis larvae per host on the percentage of larvae successfully emerging from that host.
100 90 80 70
60-
50-
40-
30--
20--
10--
1 1 1 1 30 40 50 60 70 80 90 100 110 NUMBER OF LARVAE PER HOST yakutatensis larvae per host on the meanweight Fig. 8. Effects of the number of Apanteles of resulting adults.
4.5 4.0
3.5 Y. .0004-i.36tio-6x 3.0
2.5-- 2.0 1.5 1.0
.50
I I I 90 I 50 60 70 80 10 20 30 40 NUMBER OF LARVAE PER HOST 46
Table 6. Number of larvae successfully completing development and mean adult weight of Apanteles yakutatensis from super- parasitized and non-superparasitized hosts.
total larvae larvae mean
N per host in host - adult wt. Control 12 601 26.24 7.01: 5.5 3.03* 0.86mg
Super- parasitized 14 118.2± 32.0 20.6- 10.5 2.40± 0.10mga) a) significant at the .05% level, t test. 47
Endnotes
1 Lepidoptera: Noctuidae
2Hymenoptera: Braconidae 48
CONCLUSION
The results given in this thesisare a contribution to further
understanding the nature of parasite-host associations,and add to
the data base necessary for the developmentof biological control.
It has been suggested that parasitoid femalesmay first be
attracted not to the host itself, but to the habitattype in which the
host occurs (Matthews, 1974; Vinson, 1976). The results of the field studies tend to confirm this for Apanteles yakutatensis. All of the crops in which A. yakutatensis was found are similar in that theyare either annual or perennial herbs, andare harvested on an annual or semi-annual basis. Thus, it appears that A. yakutatensismay commonly search habitats of rather low durational stabilityfor its host.
Some parasitic wasps are restricted in their climaticadaptations, or their ability to suppress host populations is adversely affected by unsuitable climatic conditions (DeBach, 1965). In the case of
A. yakutatensis, it appears that this parasite hasa rather wide climatic tolerance. It was found on both sides of the Cascade
Mountains in areas which are very different climatically. However, peppermint is grown under irrigated conditions inOregon, and it may be that the microclimate within the peppermint canopy moderates the climatological differences between the two areas examined in this study.
The differences in percent parasitism between fields should support the caution that biological control workers avoid sampling from only one location when looking fora suitable natural enemy for an introduction program. Field number six had unusually high levels 49 of A. yakutatensis. If this field was taken to be representative of the abundance of A. yakutatensis, thenone might assume that it exerted more regulatory pressure on A. californica than is actually thecase.
In order to get a more accurate estimation of its contributionto the mortality of A. californica, a number of fields should be sampled, preferably over a wide geographical range.
A more important consideration, than staticmeasures of abundance, is the trajectory of changes in a parasites population size inresponse to changes in host density. It seems clear that within peppermint fields A. yakutatensis parasitizes a variable proportion of availiable hosts over time. It may be that the mint habitat is not of a sufr ficiently lengthy duration to allow A. yakutatensis to manifesta density dependent response. Alternatively, A. yakutatensis may be an inferior competitor with respect to other members of the guild of parasites exploiting A. californica, and thus be unable to exhibit its true regulatory potential. In any case, additional studies in a variety of other habitats and in the absence of potential competitors would be necessary to determine the true regulatory potential of
A. yakutatensis.
Another aspect of the biology of A. yakutatensis which may have a bearing on its suitability as a biological control agent is the result obtained from the superparasitism study. Superparasitism seems to have less of a negative impact on a gregarious species such as
A. yakutatensis than would be the case for a solitary parasite. A host cannot support more than one solitary parasite larva, and any additional larvae in the host are not able to complete development. 50
Gregarious parasites, on the other hand, do not experiencesuch extreme
consequences from superparasitism (Salt, 1934). In the case of A.
yakutatensis superparasitism may result in a slight depression of
adult weight, but there appears to beno significant reduction in the
number of larvae completing development. Although no choice
experiments were performed, A. yakutatensis females didnot show any
reluctance to oviposit into host larvae whichwere already parasitized.
Thus, it may be that they do not discriminate between parasitizedand
non-parasitized hosts. This would have the effect of reducing the
number of hosts parasitized, especially at high host densities,over
what it would be if A. yakutatensis could discrimminate between
parasitized and non-parasitized hosts.
Considering the above, one might conclude that A. yakutatensis would not be a suitable candidate for a biological control introduction
against Autographa californica. However, additional experiments must
be performed to determine the effects of competitorson its population
dynamics, its abilities to regulate its host in habitats of longer
duration, and the possible negative effects of insecticide applications on populations of A. yakutatensis. 51
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