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INTRODUCTION
 Abstract
 Materials
and Methods
Results
Discussion
Acknowledgements
References
The long-horned beetle Dectes texanus LeConte
(Coleoptera: Cerambycidae) is an indigenous, univoltine species that
has emerged as a serious pest of soybeans throughout the eastern,
southern, and central United States over the past 40 years (Patrick, 1973, Hatchett et al., 1975,
Campbell et al., 1977, Laster et al., 1981, Rogers, 1985). In soybean, yield losses due to stem boring by
a single D. texanus larvae have been estimated
at ca. 10% (Richardson, 1975), although greater losses can result
from the lodging of mature plants. Pre-diapause larvae girdle the
lower stalk from the interior in preparation of an overwintering
chamber, causing plants to snap off at the slightest pressure. Cultivated
sunflowers can also lodge because of D. texanus damage
(Rogers, 1985), although larvae are usually unable to fully girdle
larger stalks (J.P. Michaud, personal observation).
The wild host plants of D. texanus are
all from the family Compositae and include cocklebur, Xanthium pensylvanicum Wallr.,
giant ragweed, Ambrosia trifida L.,
and wild sunflower, Helianthus annuus L.
(Hatchett et al., 1975, Rogers, 1977). It is thus of considerable biological
interest that soybean, an exotic, leguminous crop plant, should be
attacked by this insect. The association between D.
texanus and native Helianthus spp.
is likely ancient as both the insect and plant genera are indigenous
to North America. This beetle has been studied as a pest of cultivated
sunflowers (Rogers, 1985) although it can be notably difficult to
collect from wild H. annuus. Dissection of > 1000 wild sunflower stalks over several years in western Kansas has yielded only one overwintering D. texanus larva (A.K. Grant, unpublished observations), whereas a sample of 70 plants collected in the Texas panhandle in 2001 yielded 5 larva (L.D. Charlet, personal communication). In contrast, larvae of another cerambycid, Ataxia hubbardi Fisher, are frequently found infesting wild sunflower in western Kansas. Similarly, Rogers (1977) reported collecting the cerambycid Mecas
inornata Say from many wild Helianthus spp.,
including H. annuus, H.
tuberosus, H. maximiliani, H.
mollis, and H. salicifolius in
the rolling plains of Texas, but did not report finding larvae of D.
texanus in any of these plants, even though it was one of
the most common species he collected from cultivated H.
annuus in the region. Although some wild hosts may be available
for D. texanus in western Kansas (e.g.
cocklebur), soybean and cultivated sunflower appear to comprise the
primary host plants utilized in the region and it is not uncommon to find
large fields of either crop with virtually 100% of plants infested.
Both sunflower and soybean are planted as summer crops in the High
Plains region with similar planting dates and maturity schedules,
rendering them similar in seasonal availability for the beetles.
Although commercial farming of soybeans in the continental United
States began in the 1920’s, the crop did not become widely grown
until the 1940’s (Hymowitz, 1970) and the first reports of infestations
by D. texanus are from North Carolina
in the late 1960’s (Falter, 1969). Consequently, the association between D.
texanus and soybean is a novel one that likely evolved over
the past 50-60 years within a similar number of insect generations.
It is also notable that D. texanus has
emerged as a serious soybean pest over a broad geographic region
spanning North Carolina, Tennessee, Arkansas, Illinois, Missouri,
Texas, Kansas and Nebraska during this short period. Since it is
implausible that gene flow could have spread a single mutation across
such a vast region in 60 generations or less, the observed host range
expansion would appear to comprise a series of independent events
that occurred in parallel in different localities, i.e. through convergent
evolution in separate subpopulations. It also seems likely that the
ancestral D. texanus population fortuitously
contained substantial and widespread biological pre-adaptation to
utilize soybean as a host before it ever came in contact with the
plant. To be satisfactory, an evolutionary hypothesis for the D.
texanus host transition to soybean must explain how the transition
occurred in such a short evolutionary period over such a broad geographic
range.
In 2003 and 2004, we undertook a series of laboratory and field
experiments to compare the life history of D.
texanus on cultivated suflower and soybean plants and address
a series of questions relating to its patterns of host plant use
in the agroecosystems of western Kansas. Do the insects infesting
soybean and sunflower still constitute a single species? Do adult
females of D. texanus express a preference
for ovipositing in their larval host plant (the so-called ‘Hopkins
host selection principle’)? Does the population consist entirely
of polyphagous individuals, or a combination of specialists and generalists?
Do females express phenotypic plasticity with respect to host plant
acceptance, i.e. do adult experiences influence subsequent host selection
behavior?
MATERIALS AND METHODS
Abstract
Introduction
Results
Discussion
Acknowledgements
References
Experiments in 2003
Between 22, March and 9, April a total of 98 overwintering D.
texanus larvae were collected from stalks of cultivated
sunflower in Hays, Kansas, and a total of 110 larvae from infested
soybean stubble in Garden City, Kansas, about 200 miles to the
southwest. There is virtually no sunflower cultivation in the vicinity
of Garden City, but both crops are commonly grown around Hays.
Larvae were isolated individually in plastic Petri dishes (5.5
cm x 1.0 cm) with a circle of filter paper that was moistened once
every three days with a few drops of distilled water. Larvae are
highly aggressive toward conspecifics and isolation is essential
to prevent mortality resulting from larval combat. The Petri dishes
were individually numbered, placed on trays, and held in a climate-controlled
growth chamber at 24 ± 5° C and 16:8 day length under Philips
‘coolwhite’ fluorescent lighting. Larvae were examined daily and
their date of pupation recorded along with their pupal weight.
Sex was determined on the day of pupation according to the characters
described by Hatchett et al. (1975).
Adults were held in their respective labeled Petri dishes following
emergence under the same environmental conditions as larvae and pupae
and fed sections of greenhouse-grown sunflower stalks replaced every
two days. Males and females were brought together as pairs for mating
in larger Petri dishes (9.5 cm x 1.0 cm) at ages ranging from 10-12
days. Mating occurred when a male contacted a receptive female’s
elytra with his antennae and copula lasted anywhere from 30 minutes
to several hours, often with repeated couplings. The mating behavior
of D. texanus has been described in detail
by Crook et al. (2004). A total of 12 crosses were performed for
each of the four permutations of males and females from sunflower
and soybean (sunflower male x sunflower female, soybean male x soybean
female, sunflower male x soybean female, and soybean male x sunflower
female). This yielded a total of 48 mated females that were used
in oviposition experiments at 18-23 days of age.
Plants for oviposition experiments were grown from seed in plastic
pots (soybean: 4 L pots, sunflower: 8 L pots) in a greenhouse. Sunflowers
were an oilseed variety, Triumph 665, and soybeans were a Round–up®
ready variety, Asgrow 3003. Plants were used in experiments at the
6-10 leaf stage. Cylindrical wire-frame, fabric mesh cages (30 cm
diameter) were used to confine female beetles on plants ( www.lucina.freeserve.co.uk/index.html
). The height of the cage was adjustable from 30 – 100 cm, according
to the height of the plant, by altering the numbers of slotted frame
members. An elastic loop secured the bottom of the cage around the
pot and a large, zippered opening permitted access for introduction
and removal of insects.
Between 12, June and 18, July, 2003 a total of 48 mated females
were caged individually for 48 hours on one plant, followed by 48
hours on the alternate plant, half the females receiving sunflower
first, the other half receiving soybean first. Following insect exposure,
plants were examined for feeding damage and oviposition punctures
(hereafter ‘ovipunctures’) and then held for 7-10 days to permit
eggs to hatch. All plants with ovipunctures were then dissected to
detect the presence of larvae. Larvae recovered from plants were
held in Petri dishes in a growth chamber under the same environmental
conditions as the overwintered larvae and reared out on greenhouse-grown
sunflower stalks replaced every 2-3 days. A paired t-test was used
to analyze paired data from individual females, whereas data for
female treatment groups (larval host plant, sequence of plant presentation)
were compared by one-way ANOVA.
Experiments in 2004
Having demonstrated reproductive compatibility between D.
texanus populations collected from sunflower and soybean
in 2003, 326 overwintering larvae were collected from sunflower
stubble in Hays in 2004 since this host plant tended to yield larger
and healthier individuals. Following extraction from stalks, the
insects were weighed and then held under the same environmental
conditions as in 2003. Each insect was weighed again at pupation
and upon emergence as an adult.
Adult beetles of both sexes were divided randomly into two treatments
as they emerged, one group fed on petioles of sunflower, the other
on tender green stalks of soybean. The plant food was replaced every
second day. Adults were mated (as described for 2003) and mated females
were used in field trials when they were 21 days of age, or slightly
earlier if ovipunctures were observed in their food stalks.
As the quality of the greenhouse-grown plants used in 2003 was not
satisfactory, oviposition trials were conducted with field grown
plants in 2004. In particular, we suspected that the stalks of greenhouse-grown
soybeans were too frail to be suitable for oviposition, despite the
fact that females did ovipuncture in them. The same plant varieties
were used as in 2003, but they were planted in the field in a small
research plot fenced with chicken wire to exclude rabbits. Both sunflower
and soybean plants were fully grown and in early reproductive stages
when they were presented to insects, corresponding to the growth
stages normally attacked by adult beetles in the field. Each field
plant was given a careful visual examination prior to use in the
experiment to ensure it had no pre-existing insect damage that might
confound results, or possibly affect the responses of the experimental
female. A sequential presentation of plants was used, rather than
a simultaneous choice presentation, given the logistical difficulties
of growing soybeans immediately adjacent to sunflowers (due to shading
of the former by the latter) and obtaining adjacent pairs of plants
that would be both in suitable stages of growth.
Field trials were conducted by caging mated females on plants using
the same cages as in 2003, except that the lower edge of the fabric
was buried in the soil around the base of the plant in the field.
After 48 hours on one plant, the female was recovered and caged on
a plant of the other type for another 48 hours. One half the females
were presented with sunflower first, the other half with soybean
first. Following insect exposure, each plant was uprooted and taken
into the laboratory where it was trimmed of leaves. All stems and
petioles were then carefully examined under a low power dissecting
microscope. Each stem and leaf petiole was assessed for feeding damage
on a four point scale and feeding scores were then summed for the
whole plant. Unlike sunflower plants, soybean plants varied considerably
in architectural complexity by virtue of dichotomous branching. Therefore,
a proportional index of plant damage was also calculated for soybean
plants that weighted numbers of damaged petioles/branches by the
total number available for purposes of regressional analysis. All
ovipunctures were counted and each was carefully dissected with a
scalpel to determine the presence or absence of an egg. A paired
t-test was used to analyze paired data from all females considered
together and data for females grouped by treatment (adult food plant,
sequence of plant presentation) were compared by one-way ANOVA. When
effects were significant for dependent variables, a two-way ANOVA
was performed to analyze interactions between independent variables.
Only five of the mated females fed soybean laid one or more eggs
in the soybean stalks that were provided as food in the Petri dishes,
but oviposition behavior was common among females provided with sunflower
stalks. Therefore, the ovipuncturing and egg-laying behavior of 20
females held for their entire adult life in Petri dishes was observed
and recorded with sunflower stalk segments provided fresh every two
days. Upon removal, all stalks were examined for ovipuntures and
dissected to determine the numbers of eggs laid. These observations
provided estimates of lifetime fecundity (under laboratory conditions)
and permitted regressional analyses of reproductive behavior on other
life history attributes such as longevity and adult weight.
RESULTS
Abstract
Introduction
Materials
and Methods
Discussion
Acknowledgements
References
2003 Experiments
Seventy-two adults were obtained from sunflower (36 females, 36
males) and 79 adults from soybean (42 females, 37 males) for survival
rates of 73.5% and 71.8%, respectively. Female pupae weighed, on
average, 13.7% heavier than male pupae regardless of plant source
(F = 5.331; 1,170; P = 0.022). However, plant source influenced pupal
weight for both males [mean ± SEM = 34.2 ± 1.4 mg (sunflower)
vs. 21.0 ± 0.8 mg (soybean); F = 77.553; df = 1,84; P < 0.001]
and females [mean ± SEM = 39.0 ± 1.6 mg (sunflower)
vs. 23.2 ± 1.0 mg (soybean), F = 72.812; df = 1,84; P < 0.001].
Plant source had no effect on time to adult emergence calculated
from the first day of spring (F = 0.027; df = 1,162; P = 0.871) and
neither did sex (F = 1.850; df = 1,162; P = 0.176). Therefore, the
pattern of adult emergence is depicted for all insects pooled in
Fig. 1. The frequency of elytral deformities was higher among individuals
maturing in soybean compared to sunflower (F = 6.277; df = 1,151;
P = 0.013).
Of the 48 females tested in the greenhouse oviposition experiment,
40 made at least one ovipuncture on a plant and the remaining eight
were excluded from all subsequent analyses. A total of three viable
larvae were recovered from plants exposed to sunflower-collected
females mated to soybean-collected males and four viable larvae from
plants exposed to soybean-collected females mated to sunflower-collected
males. This compared to four viable larvae each recovered from plants
exposed to sunflower-sunflower and soybean-soybean crosses. All larvae
were recovered from sunflower plants. These larvae gave rise to 10
pupae and 9 adult beetles that emerged between 16 December 2003 and
9 April 2004. Three of these beetles were the progeny of sunflower
females crossed with soybean males and two were the progeny of soybean
females mated with sunflower males. Given the small numbers of larvae recovered,
only numbers of ovipunctures were subjected to analysis.
Larval host plant had no effect on the number of ovipunctures females
made on plants of either type as adults (sunflower; F = 3.373; df
= 1,38; P = 0.073; soybean: F = 0.303; df = 1,38; P = 0.585). However,
females made more ovipunctures on a plant type when it was offered
first (sunflower: F = 4.806; df = 1,38; P = 0.035; soybean: F = 5.390;
df = 1,38; P = 0.026). Overall, significantly more ovipunctures were
made on sunflower than on soybean (mean ± SEM = 4.43 ± 0.6
vs. 0.18 ± 0.06, t = 6.338, df = 39, P < 0.001).
2004 Experiments
Development. A total of 242 adult beetles emerged
from 326 overwintered larvae, 116 males and 126 females for a survival
rate of 74.2 % and a sex ratio of 0.52. Female pupae averaged 60.5 ± 1.43
mg compared to 52.3 ± 52.3 mg for male pupae, 12.9 % heavier
(F = 16.529; df = 1,240; P < 0.001). The mean pupation time was
similar for males and females (13.6 d and 13.7 d, respectively).
Male larvae lost an average of 37.6 % of their weight from time of
collection to emergence as an adult; female larvae lost an average
of 37.0 %.
Longevity and reproduction in the laboratory. Male
beetles lived an average of 23.3 ± 1.4 d on a diet of soybean
stalks, compared to an average of 75.6 ± 4.3 d on a diet of
sunflower petioles (F = 148.847; df = 1,113; P < 0.001). For females,
the averages were 23.2 ± 1.2 d and 52.4 ± 3.7 d, respectively
(F = 65.273; df = 1,98; P < 0.001). The twenty females followed
in the laboratory laid a mean (± SEM) of 33.05 ± 5.2
eggs over an average reproductive lifespan of mean (± SEM)
56.0 ± 4.5 days for an average reproductive rate of 0.57 eggs
per day of reproductive life. The mean (± SEM) pre-oviposition
period was 17.0 ± 0.7 days and 42.3 % of ovipunctures were
associated with eggs. Female weight was positively correlated with
total number of ovipunctures in linear regression (F = 5.02; df =
1,18; P = 0.038; r2 = 0.218), but the effect was not significant
for total number of eggs laid (F = 1.77; df = 1,18; P = 0.200). Female
longevity was strongly and positively correlated with total number
of ovipunctures (F = 11.05; df = 1,18; P = 0.005; r2 = 0.441), but
not with total number of eggs laid (F = 2.57; df = 1,18; P = 0.131).
Female longevity was negatively correlated with the proportion of
ovipunctures that resulted in eggs laid (F = 5.26; df = 1,18; P =
0.038; r2 = 0.273). Female fecundity was negatively correlated with
pre-oviposition interval (F = 5.34; df =1,18; P = 0.33; r2 = 0.229)
and positively correlated with daily rate of oviposition (F = 64.21;
df = 1,18; P < 0.001; r2 =0.781).
Field trials. A total of 81 mated females were
tested in the field trial, 52 fed sunflower and 29 fed soybean. These
unequal samples arose because many soybean-fed females died before
they were old enough to use in the experiment, some before mating
and some soon thereafter. In numerous dishes we observed little or
no evidence of feeding on the soybean stalks, suggesting that many
adults were reluctant to consume them. Of the tested females, 27
were either lost or died in the course of their field trial and were
therefore excluded from all analyses. Only data from the 54 females
recovered alive at the end of their trial were used for analyses
of feeding and reproductive behavior.
Feeding behavior in the field. Females fed sunflower
in the laboratory had higher feeding scores on sunflower than on
soybean plants in field trials (t = 2.109, df = 36, P = 0.021), whereas
soybean-fed females had higher feeding scores on soybean plants (t
= 1.994, df = 16, P = 0.032, Fig. 2). Comparing females by diet treatment,
those fed soybean in the laboratory did more feeding on soybean in
field trials than did those fed sunflower regardless of the sequence
of plant presentation (F = 8.233; df = 1,52; P = 0.006), whereas
both fed equally on sunflower (F = 0.593; df = 1,52; P = 0.445).
Sunflower plants sustained higher feeding scores from soybean-fed
females in the field trial when they were presented first than when
they were presented second (F = 5.810; df = 1,15; P = 0.029) but
there was no effect of plant presentation sequence on soybean feeding
scores (F = 0.005; df = 1,15; P = 0.945). Plant presentation sequence
had no effect on the feeding behavior of sunflower-fed females on
either sunflower (F = 1.007; df = 1,35; P = 0.323) or soybean (F
= 2.989; df = 1,35; P = 0.093). A two-way ANOVA revealed no significant
interactions between adult food plant and plant presentation sequence
for feeding scores on either sunflower (F = 0.285; df = 1,50; P =
0.596) or soybean (F = 0.302; df = 1,50; P = 0.585).
Oviposition behavior in the field. Significantly
more total ovipunctures were made (F = 10.190; df = 2,31; P < 0.001;
LSD, P < 0.01) and more eggs laid (F = 9.499; df = 3,31; P = 0.001;
LSD, P < 0.01) by females that accepted both plant types for oviposition
(means ± SEM = 19.00 ± 3.58 and 6.00 ± 0.98,
respectively) than by females that either laid only on sunflower
(means ± SEM = 8.00 ± 2.12 and 3.08 ± 0.82,
respectively) or only on soybean (Means ± SEM = 4.25 ± 1.10
and 1.5 ± 0.26, respectively). However, females laying eggs
only on sunflower also made the occasional ovipuncture on soybean
(mean ± SEM = 0.73 ± 0.30) and females laying eggs
only on soybean also made a few ovipunctures in sunflower (mean ± SEM
= 1.17 ± 0.98). Only data from the 34 females that laid one
or more eggs in their field trial were included in further analyses
of oviposition behavior.
On average, 32.3 and 33.2 percent of ovipunctures resulted in an
oviposition in sunflower and soybean, respectively, in the field
trial. The type of plant provided as adult food had no significant
effect on the total number of ovipunctures made (F = 0.661; df =
1,52; P = 0.420) or the total eggs laid (F = 1.238; df = 1,32; P
= 0.274). However, females fed soybean made twice as many ovipunctures
on soybean plants in the field as they did on sunflower plants (t
= 2.183, df = 16, P = 0.044, Fig. 3a), although the difference was
not significant for numbers of eggs laid (t = 0.537, df = 9, P =
0.604, Fig. 3b). Sunflower-fed females ovipunctured sunflower and
soybean plants to a similar extent (t = 1.513, df = 36, P = 0.139)
and laid similar numbers of eggs in each (t = 0.169, df = 23, P =
0.296).
The sequence of plant presentation in the field affected the total
number of ovipunctures made by sunflower-fed females (F = 9.243;
df = 1,35; P = 0.004; Fig. 4a), although the effect was not significant
for soybean-fed females (F = 1.028; df = 1,15; P = 0.327). However,
the sequence of plant presentation in the field affected the total
number of eggs laid by soybean-fed females (F = 6.262, df = 1,8;
P = 0.037; Fig. 4b), with no significant effect for sunflower-fed
females (F = 2.534; df = 1,22; P = 0.126). A two-way ANOVA revealed
no significant interactions between food plant and plant presentation
sequence for any reproductive activity (ovipunctures in sunflower:
F = 1.128; df = 1,50; P = 0.293; ovipunctures in soybean: F = 0.400;
df = 1,50; P = 0.530; total ovipunctures F = 1.068; df = 1,50; P
= 0.306; eggs in sunflower: F = 0.231; df = 1,30; P = 0.634; eggs
in soybean: F = 0.001; df = 1,30; P = 0.983; total eggs: F = 0.144;
1,30 df; P = 0.707). Pooling insects from both diets, females made
more total ovipunctures (F = 9.573; df = 1,52; P = 0.003) and laid
more total eggs (F = 6.707; df = 1,32; P = 0.014) when the plant
sequence was sunflower-soybean than when it was soybean-sunflower.
Thus more reproductive activity was elicited from females when sunflower
was encountered first, regardless of their diet in the laboratory.
In terms of plant-specific activity, females ovipunctured more often
on sunflower (5.78 ± 1.2 vs. 1.63 ± 0.57; F = 9.910;
df = 1, 52; P = 0.003) and laid more eggs on sunflower (2.95 ± 0.63
vs. 0.67 ± 0.37; F = 8.391; df = 1, 32; P = 0.007) when it
was presented first than when it was presented after soybean. A similar
pattern was evident for ovipunctures on soybean, although the effect
was only marginally significant due to a smaller sample size and
large variation in female activity (4.67 ± 1.41 vs. 1.89 ± 0.57;
F = 3.334; df = 1,52; P = 0.074). There was no indication that sequence
of plant presentation affected the number of eggs laid in soybean
(F = 0.081; df = 1,32; P = 0.778), but both female sample size and
count data were even lower for eggs than for ovipunctures.
Correlations between feeding and oviposition. Feeding
scores on sunflower plants were linearly correlated with both numbers
of ovipunctures (F = 93.05; df = 52; P < 0.001; r2 = 0.642; Fig.
5a) and numbers of eggs (F = 39.56; df = 52; P < 0.001; r2 = 0.432;
Fig. 6a). Similar relationships were observed between soybean feeding
scores and ovipunctures (F = 44.16; df = 52; P < 0.001; r2 = 0.459;
Fig. 5b) and soybean feeding scores and oviposition (F = 21.46; df
= 52; P < 0.001; r2 = 0.292; Fig. 6b). The proportional index
of feeding damage provided a better fit to the oviposition data on
soybean than did the raw feeding scores (F = 37.63; df = 52; P < 0.001;
r2 = 0.42), but did not improve fit to the ovipuncture data (F =
38.09; df = 52; P < 0.001; r2 = 0.423).
DISCUSSION
Abstract
Introduction
Materials
and Methods
Results
Acknowledgements
References
Reproductive compatibility
The reciprocal crosses of D. texanus adults
reared from sunflower and soybean each produced several viable progeny,
indicating that the two populations comprise a single species according
to the Biological Species Concept (Mayr, 1942). The fact that progeny
were only recovered from sunflower plants may be of little significance.
The greenhouse environment altered plant architecture and physiology
considerably, especially in the case of soybeans, where leaf petioles
may have been too slender to contain a pith core and permit completed
oviposition. Hatchett et al. (1975) suggested that successful oviposition
depended on whether or not pith was present in the stem, and whether
or not the female could reach it with her ovipositor. Although we
were able to compare the frequency of ovipunctures among these plants,
we did not feel that any reliable conclusions could be drawn from
these data regarding the relative acceptability of the two host plants,
or their suitability for larval survival. Based on these observations,
we decided to perform all behavioral assays on field-grown plants
the following season.
Life history consequences of host plant
Development of D. texanus larvae in soybean
resulted in a 40% reduction in body weight compared to development
in sunflower, and a higher frequency of elytral deformities. This
reduction in adult weight could translate into significant reductions
in beetle fitness if body size is correlated with other life history
attributes that affect survival or reproductive performance in the
field. For example, adult body mass could be positively correlated
with ability to survive adverse physical conditions, with female
fecundity, or with male mating success. The laboratory observations
on reproductive females may not have had sufficient sample size to
detect effects of female weight on fecundity, but the number of ovipunctures
in sunflower stalks increased significantly with female weight suggesting
that larger females had greater repoductive vigor. The survival to
maturity of larvae from both plant sources was similar in the laboratory,
and comparable to the survival obtained by Hatchett et al. (1975)
in soybean, suggesting a relatively high degree of adaptation to
the novel host plant despite these apparent fitness costs.
Pupation times and emergence dates of adults in a 24° C chamber
were similar for insects collected from sunflower and soybean, suggesting
no effect of host plant on these life history parameters. The extended
period of adult emergence (Fig. 1), combined with a female longevity
of ca. two months, are probably the reasons why delayed planting
dates yield limited benefits in reducing infestations in all but
the most southern regions that have the largest planting window (Rogers, 1985). The fact that larvae recovered from experimental plants pupated
and produced viable adults in as short a period as six months at
24° C demonstrates that diapause is facultative in this species and
that a cold period is not obligatory for completion of larval development.
The observed reduction in adult longevity when soybean was the exclusive
adult food is consistent with soybean representing a host plant of
generally lower nutritional suitability than sunflower for both feeding
life stages. The significance of this effect in reducing adult longevity
in natural populations will depend on the degree to which adults
are limited to soybeans as a food source, or able to supplement their
diet with more nutritious plants. Note also that the soybean diet
did not reduce the reproductive performance of females in the field
trial relative to the sunflower diet.
Feeding behavior
Females in field trials fed more on the plant they had been provided
in the laboratory than on the alternative (Fig. 2), indicating that
adults became conditioned to feeding on a particular plant type.
When diet treatments were compared, soybean-fed females fed more
on soybean in the field trial than did sunflower-fed females, whereas
feeding on sunflower was equal. Thus, the soybean feeding experience
increased female acceptance of soybean as food, without reducing
the acceptability of sunflower. Encounters with whole plants in the
field appeared to influence female feeding behavior more than did
their laboratory experience of feeding on stalk segments. Thus, soybean-fed
females exhibited stronger feeding responses to sunflower plants
when they were the first whole plant encountered than when they were
the second. Apparently, a 48 hour encounter with a whole soybean
plant reduced the feeding response to sunflower more than did three
weeks of an exclusive diet of soybean stalks.
Oviposition behavior
The 2003 data did not provide any indication that the larval host
plant influenced an adult female’s tendency to ovipuncture plants
of one type or another, the so-called ‘Hopkins host selection principle’.
Collectively, the 2004 data are consistent with Barron’s (2001) inference
that adult experiences have a greater impact on oviposition behavior
than larval experiences in most phytophagous species. Approximately
one third of ovipunctures resulted in an egg being laid and this
was independent of host plant, suggesting that counts of ovipunctures
might be used to assess host plant acceptance in larger scale studies
without the need for time-consuming plant dissections to count eggs.
The fact that soybean-fed females made twice as many ovipunctures
on soybean plants as did sunflower-fed females (Fig. 3) suggests
that a female’s adult feeding experience affects her reproductive
response to a plant. The lower count data for eggs and the small
sample size of soybean-fed females reduced our ability to detect
such an effect on actual oviposition. Interestingly, a diet of sunflower
did not serve to reduce the acceptability of soybean for oviposition,
suggesting that no negative conditioning to soybean resulted from
the sunflower diet, although positive conditioning apparently did
result from the soybean diet.
It is remarkable that a female’s oviposition behavior appeared more
influenced by the first whole plant she encountered in the field
than by the type of plant she had been fed in sections for the previous
three weeks. A female’s total ovipositional activity was higher when
her initial encounter was with sunflower than when it was with soybean
(Fig. 4), suggesting that the ancestral host plant still triggered
a stronger reproductive response than the novel host plant, and one
with sufficient duration to affect behavior on a subsequent plant
of another species. However, the reverse effect could also be inferred,
i.e. an intial encounter with soybean reduced a female’s reproductive
activity, not only on the soybean plant, but also on a subsequent
sunflower plant. An effect of plant sequence was also noted in the
greenhouse trials in 2003 in that females (all fed on sunflower in
this case) made significantly more ovipunctures on the host that
was presented first as a whole plant.
The description of D. texanus female
oviposition behavior provided by Hatchett et al (1975) identifies
a clear link between feeding and oviposition: almost all ovipunctures
begin with a female chewing a hole through the tough, epidermal surface
of plant petiole before inserting her ovipositor. The significant
regressions of feeding damage on ovipunctures (Fig. 5) and eggs (Fig.
6) for both plant types support the inference of an important relationship
between adult feeding and oviposition behavior. In an agricultural
context, emergent adults encountering a large monoculture would be
likely to feed only on plants of that type, the females ultimately
accepting the same plants for oviposition. The link between adult
feeding and oviposition behavior could have been an important proximal
mechanism facilitating the host transition to soybean by D.
texanus. It also suggests that sunflower, on which D.
texanus has little if any yield impact (J.P. Michaud, unpublished
data), could function as a trap crop, or companion crop, to protect
soybeans. If sunflower is preferred over soybean as an adult food
plant, then sunflower plants could serve to attract and retain emerging
adults and subsequently serve as an oviposition sink for reproductive
females. The feeding preference should result in declining gradients
of infestation across soybean fields where ever they approach a border
with a sunflower field, the companion crop effect. However, even
better protection might be afforded the soybean crop if it were completely
surrounded by sunflowers planted as a trap crop so that immigrating
beetles encountered, and fed first, on the preferred host plant before
encountering the less preferred.
Why a transition to soybean?
Given the significant fitness costs associated with exploitation
of soybean relative to sunflower (and presumably other ancestral
host plants), the potential compensatory payoffs for D.
texanus females that decide to accept soybean for both feeding
and oviposition must be examined and weighed. Various hypotheses
can be considered, none mutually exclusive, and some potentially
additive in effect. However, in order to be sufficient, an explanation
of the selective advantage for exploiting soybean must function equally
well in all the various geographic regions where host expansion has
occurred.
1) The host availability hypothesis. Michaud (1990)
described a series of ecological conditions that could theoretically
serve to maintain, or select for, polyphagous habits in phytophagous
insects. The model focused primarily on conditions that generated
spatial or temporal uncertainty in the quality or availability of
the preferred host plant and these were further elaborated in Michaud
(1992). Soybean may have been initially accepted for feeding, and
subsequently for oviposition, simply because it was readily available
and abundant in circumstances where alternative host plants were
not. This hypothesis seems plausible for the arid High Plains region
where soybean circles under center-pivot irrigation frequently constitute
‘green islands’ in a virtual desert of parched summer vegetation. D.
texanus ecology also conforms to the first category of cerambycids
described by Hanks (1999), i.e. species that attack healthy host
plants, both larvae and adults feeding on the same plant, and the
adults having low dispersal tendency. Collectively, these traits
are conducive to scenarios in which female beetles arrive in soybean
monocultures by chance, eventually begin feeding, and finally oviposit
on the plants rather than opting for dispersal. The observed link
between adult feeding and oviposition also supports this scenario.
However, the host availability hypothesis may function less well
in regions where soybean is grown on smaller scales and without irrigation.
More information on the availability of wild host pants relative
to soybean in other regions of the D. texanus range
would be useful for assessing the general applicability of the host
availability hypothesis.
2) The natural enemy hypothesis. Soybean may represent
a host plant that, although inferior as food for both adults and
larvae, provides an effective refuge from predators, parasitoids
and/or diseases that normally inflict mortality on the population
in ancestral host plants. For example, Gratton & Welter (1999)
showed that larvae of the agromyzid leafminer, Lyriomyza
helianthi, subjected to an artificial host shift from H.
annuus to other composite plants experienced a 22% reduction
in rates of parasitism, consistent with the novel host plants providing
‘enemy free space’. Little information exists on sources of mortality
for D. texanus larvae in its various ancestral
hosts, although the protected location of the larvae within the plant
suggests little vulnerability to predation. Hatchett et al. (1975)
reported one ichneumonid, two braconid, and three pteromalid parasitoids
attacking D. texanus taken from Ambrosia spp.
in Missouri, but none from soybean. Although moribund larvae can
be found in winter stalks, we have yet to detect a single parasitoid
or predator of D. texanus larvae in samples
collected from either soybean or cultivated sunflower in western
Kansas and none have been reported in the literature to our knowledge.
Similarly, collections of D. texanus larvae
from cultivated sunflowers across the High Plains made by the USDA,
ARS Sunflower Insect Research Laboratory in Fargo, ND over a period
of more than 20 years have yet to yield any parasitized individuals
(L.D. Charlet, personal communication). Consequently, there is little
evidence that natural enemies exert any significant mortality on D.
texanus in any host plant, or in any portion of its range.
3) The interspecific competition hypothesis. Soybean
might represent a refuge host plant for D. texanus where
it can escape aggressive, superior competitors that inflict considerable
larval mortality, directly or indirectly, in ancestral host plants.
A great diversity of insects feeds within the stalks of sunflowers
– too many to list here, but no insects have yet been reported to
feed within the stalks of soybeans in the continental United States.
Interspecific competition among phytophagous insects has long been
thought to be a weak or insignificant evolutionary force because
herbivores typically consume such a small proportion of the available
primary production (Lawton et al., 1981). Whereas this may be
true for many foliage feeding species, it is not necessarily true
for insects that compete for more limited, high-value resources such
as fruits and seeds, or in the case of D. texanus,
for the base of the stalk, the only suitable over wintering site.
There is also anecdotal evidence to indicate that A.
hubbardi engages in ‘interference competition’ (Miller, 1967)
with D. texanus within sunflower stalks
in western Kansas. Larvae of the former species average three times
the size of D. texanus and are highly
aggressive toward both conspecifics and D. texanus larvae. Ataxia
hubbardi occurs in both wild and cultivated H.
annuus in the High Plains, but does not attack soybean. A
preliminary laboratory trial indicated that A.
hubbardi larvae mutilated and killed larvae of D.
texanus in 16 of 20 replications when two larvae of equal
weight were introduced into opposing ends of the same sunflower stalk
(AKG, unpublished data). Rogers (1977) reported that “there appears
to be considerable competition between larvae of A.
hubbardi and M. (Mecas) inornata”
(another cerambycid that bores sunflower stalks) and that “larvae
of A. hubbardi appear to have the advantage”.
Adults of A. hubbardi emerge earlier in
spring than either D. texanus or M.
inornata (Rogers, 1977) and the larvae typically predominate
over D. texanus in stalks of early-planted
sunflowers in our region (JPM, unpublished data). Complete information
is not available on the degree to which host ranges and geographic
ranges overlap for these two species, but it seems unlikely that A.
hubbardi could represent a serious mortality factor for D.
texanus in all its composite hosts throughout its entire geographic
range, although it may contribute some selective pressure for soybean
utilization by D. texanus in our particular
area.
4) The intraspecific competition hypothesis. Ward
(1992) put forward a model for the evolution of polyphagy in phytophagous
insects that included intraspecific competition as a potential force
reducing the suitability of the preferred host plant and driving
the evolution of a host range expansion. Dectes
texanus infestation rates in soybean and sunflower fields
often exceed 80 or 90% of available plants. In summer, plants can
be found to contain two, or even three of four larvae that are ultimately
reduced through larval combat to a final victor, although occasionally
two overwintering chambers may be formed. Hatchet et al. (1975) noted
that “Most infested plants contained several larvae” and described
larval competition occurring in two stages, the first between neonate
larvae within petioles, the second between third instar and older
larvae within the main stem. The unique stalk-girdling behavior of
the pre-diapausing larva can also be interpreted as a defensive tactic
that has evolved to foil any conspecific competitors that are late
in descending to the base of the plant. In the early stages of the
host transition, any viable offspring of females ovipositing in soybean
would escape competition from conspecifics, although the benefits
would diminish as the behavior increased in frequency in the population.
There is not only strong evidence for intraspecific competition in D.
texanus populations, but the initial benefits of reduced competition
in soybean, although frequency-dependent, are quite compatible with
an evolutionary scenario of multiple independent host shift events
from various ancestral host plants wherever soybean has been grown.
Thus, we favor intraspecific competition as the most likely force
driving the host shift of D. texanus throughout
its range, although the transition was likely re-inforced by other
selective advantages for soybean exploitation that varied among localities.
Implications for the evolution of D. texanus.
If the D. texanus population was uniformly
polyphagous with respect to utilization of sunflower and soybean,
all females would be expected to accept both host plants. However,
females fell into three discrete categories of host plant acceptance
with approximately equal frequency, laying eggs either only in sunflower,
only in soybean, or in both plants equally. This observation is consistent
with some genetic basis for host plant fidelity, and is superficially
suggestive of disruptive selection if the ‘both plants’ category
could be construed to represent heterozygotes occurring at less-than-expected
frequency and the ‘only one’ categories, homozygotes. However, such
an interpretation lacks supporting evidence as yet. An alternative,
and equally plausible, hypothesis is that multiple alleles affect
host plant acceptance and that the observed distribution of female
‘types’ in the experiment simply reflects the ‘net’ responses of
a broad range of genotypes present in the population. Whether the
basis for host plant fidelity is monogenic or polygenic, the data
suggest that genes for soybean acceptance presently occur with a
frequency equal to those for sunflower acceptance, at least in this
particular population.
The final question is whether evolution can be expected to proceed
toward specialization within subpopulations, or general polyphagy.
Although the studied population contained individuals with apparent
behavioral specialization, this specialization was not absolute,
as evidenced by some ovipuncturing on the alternative host, and the
fitness costs of feeding on soybean, for adults and larvae, remain
considerable for the population as a whole. Thus it seems unlikely
that disruptive selection would favor assortative mating according
to host plant that would ultimately result in sympatric speciation,
although this is the theoretical outcome if fitness on one host is
negatively correlated with fitness on the other. An alternative evolutionary
scenario, more likely in our view, is one in which particular alleles
increase in the population that provide increments to fitness on
soybean without corresponding decrements to fitness
on sunflower. This scenario assumes that phenotypic plasticity
for host plant acceptance yields higher average fitness for individuals
over time than traits associated with specialization on either plant.
Sunflower will remain the preferred host plant, but soybean will
also be utilized whenever it is available, to a lesser extent when
sunflower is available, and to a greater extent when it is not. The
supporting rationale for this outcome encompasses both temporal and
spatial components of host plant availability in the agroecosystem
that now supports the vast majority of the beetle population. Agricultural
crop rotations generate temporal variation in the availability of
host plants, resulting in a capricious environment for the beetle
population; whatever crop was present in a field in one year is the
least likely to be present in the same field in a subsequent year,
thus favoring genotypes adapted to utilize both host plants. In the
High Plains, both crops are sometimes present in adjacent fields
and in other cases irrigated circles are split between sunflowers
and soybeans. Under these conditions, polyphagous females can ‘spread
risk’ by placing some offspring in both host plants, and achieve
potential fitness gains whenever larval mortality factors vary as
a function of host plant. The D. texanus -soybean-sunflower
system warrants continued study for many years to come as it represents
a unique opportunity to test assumptions and theories of insect host
range evolution in agroecosystems that are artificially simplified
by monocultural practices.
ACKNOWLEDGEMENTS
Abstract
Introduction
Materials
and Methods
Results
Discussion
References
The authors are thankful to the National Sunflower Association for
partial support of this research and S. Kambhampati for reviewing
the manuscript. Contribution No. 05-220-J from the Kansas Agricultural
Experiment Station.
REFERENCES
Abstract
Introduction
Materials
and Methods
Results
Discussion
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