Biologia 63/3: 418—426, 2008
Section Zoology
DOI: 10.2478/s11756-008-0055-6
Contrast adaptation to time constraints on development of two
pre-dispersal predators of dandelion (Taraxacum officinale) seed
Zdenka Martinková & Alois Honěk
Research Institute of Crop Production, Drnovská 507, CZ-16106 Praha 6 – Ruzyně, Czech Republic; e-mail:
[email protected], [email protected]
Abstract: Pre-dispersal seed predators of quickly maturing inflorescences of Asteraceae are constrained by shortage of
development time. At seed dispersal, they should pupate or, if still immature, relocate into another inflorescence. To
investigate how dominant coleopteran predators of dandelion seed, Glocianus punctiger (Curculionidae) and Olibrus bicolor
(Phalacridae), cope with time limitation we combined observation (development and temperature of dandelion capitulum,
thermal constants of predator development, age structure of larval populations at seed dispersal) and analogy (“rate
isomorphy” in predator development, comparing “model” coleopteran species with similar temperature requirements).
Development of a dandelion capitulum takes 21 days. The time available to G. punctiger (140–190 day degrees, development
threshold 6.3 ◦C) is sufficient to complete development and pupate after seed dispersal. By contrast, only 30–50 day degrees
are available to O. bicolor (threshold 13.5 ◦C) and this is not enough to complete development and consequently immature
larvae should move to other capitula to continue feeding until pupation. These contrast strategies which are determined
by this thermal adaptation, are accompanied by differences in larval morphology. The “cold adapted” G. punctiger has an
apodous larva not capable of migrating between capitula while the “warm adapted” O. bicolor has a mobile campodeiform
larva capable of migration.
Key words: Curculionidae; Phalacridae; Coleoptera; lower development threshold; temperature; larva; morphology
Introduction
Phytophagan insect species living on temporary plant
structures such as buds, young foliage, flowers or fruits
must complete the addicted life stage before the hostplant organ declines. Their life span is limited to the
period granted by the plant and the time needed to
complete a life stage is a function of temperature. If
host-plant and phytophagan physiological time is heterochronous, the coexistence may become difficult. Consequently, any adaptation facilitating the concurrence
of host-plant and consumer development is an important life history trait.
An important group of animals living in a time constrained environment is the guild of pre-dispersal seed
predators, species eating maturing seed before its dispersal from mother plant. This guild includes enormous
number of species mainly belonging to Coleoptera, Lepidoptera, Diptera and Hymenoptera (Crawley 1997).
This diversity issues from taxonomic richness of flowering plants and their long co-evolution with insects.
For predators, seed complements are a potent lure since
they provide a copious offer of quality food. However, the seed is defended in many ways including
quick maturation and early dispersal which may prevent the predators from keeping pace with plant development. The quick development of inflorescence and a
rapid maturation of seed is typical for several species
of Asteraceae which produce infructescences of otherc 2008 Institute of Zoology, Slovak Academy of Sciences
wise weakly protected achenes. However, many seed
predators coped with hostplant temporality successfully (Fenner et al. 2002). Predators have evolved different strategies of living on ephemeral resource including
minimalization of development time or migration between several host infructescences.
Dandelion, Taraxacum officinale Weber ex Wiggers, is a plant whose inflorescences grow, flower and
mature quickly (Stewart-Wade et al. 2002). Each inflorescence (capitulum) is an isolated short-lived structure supported by an erect stalk inserted singly in the
leaf rosette. The ripening inflorescences of dandelion
are populated by several insect species among which
dominate the seed predators Glocianus punctiger (Gyllenhal, 1837) (Coleoptera: Curculionidae) and Olibrus
bicolor (F., 1792) (Coleoptera: Phalacridae) (Honěk et
al. 2005). The eggs of G. punctiger are laid in the hollows of dandelion stalks, at the beginning of stalk extension. The apodous larva (Fig. 1) moves to the underside of the thalamus, tunnelling through the receptacle
to feed on the maturing seeds. Olibrus bicolor lay eggs
under the leaves of involucrum, not earlier than at the
end of stalk extension. The mobile campodeiform larva
(Fig. 1) hatches after flowering and feeds on maturing
seed. Although both species are well known seed predators (Heyer, in Reitter 1912; Radde 1974; McAvoy et al.
1983; Campagna & Rapparini 2002), a study demonstrating their strategy for adapting to an ephemeral life
in the dandelion capitula is lacking.
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Development of dandelion seed predators
Fig. 1. Mature larva of G. punctiger (A) and O. bicolor (B).
Scales 1 mm.
In this paper we studied the life history of both
seed predator species in populations of dandelion which
belong to the Section Ruderalia which, in the Czech
Republic, comprises c. 250 apomictic microspecies
(Kirschner et al. 2002). Their differences do not concern
seed predators because variation in seed quality among
species is small (Tweney & Mogie 1999). Here we show
how thermal requirements determine the concurrence
between development of dandelion capitula and that of
predator species. Observation and analogy were combined to document difference between both predator
species in their strategy of adaptation to the temporary
environment of dandelion capitula. (a) Development of
dandelion capitula and their temperatures were determined under natural conditions. (b) Lower development
threshold for predator species was established. (c) Thermal time available in the open for each species was calculated. (d) Data on “model” species of phytophagan
Coleoptera were used to determine whether this time is
sufficient to complete predator development. (e) Development strategy (completing development within one
capitulum or dispersing between them) was predicted
and the prediction tested using age structure of larval populations at seed dispersal. (f) Finally, the correspondence between larval morphology and development
strategy was established.
Material and methods
Development and temperature of capitula
In 2001, the development of capitula was established on
145 randomly selected dandelion plants, at Praha-Ruzyně
(50◦ 06 N, 14◦ 15 E, altitude 350 m a.s.l.). On each plant,
one capitulum sessile in the leaf rosette was selected and
labelled with a loose wire ring. The rising capitulum passed
through the ring which then surrounded the base of the
419
stalk. The position of each plant was indicated with wooden
label. The capitula were labelled on a south inclined dry plot
(ca. 100 m2 area), on April 11 (27 capitula), April 14 (37)
and April 18 (13), and on a tree-shaded plot (ca. 250 m2
area) on April 30 (68). The capitula were inspected in two
day intervals and their development classified into four categories: (1) stalk extension (from marking until flowering),
(2) flowering, (3) seed maturation (from flowering until exposure of mature seed) and (4) seed dispersal (until ceasing
of the last seed).
Temperature of dandelion capitula was measured to
select its best correlate among the eight temperature measurements provided by an automatic meteorology station
(350 m and 100 m from dry and shaded plot, respectively).
Using distance thermometre Raytek model RAYMX4PG
(0.1 ◦C precision), temperature of capitula was recorded on
10 days between July 12 – August 8, 2001 selected for contrast weather (air temperatures 11.7–28.8 ◦C). The temperatures were recorded three or four times per day, between
07:00–21:00 h, on each occasion on 10 randomly selected
capitula. Best correlated with average capitulum temperatures was air temperature at 5 cm above the ground surface
(R2 = 0.859, slope: 1.088 ± 0.079, maximum thermal excess
±3.5 ◦C). The regression was not significantly different from
1 (t = 1.13, n = 35, P > 0.05).
Thermal constants for predator development
As experimentation on predator development using whole
plants at constant temperatures was difficult, temperature
effects were studied in pupae. Mature dandelion capitula
were dissected and large larvae of both predator species including those just ready for pupation put individually into
glass tubes (55 mm long, 15 mm diameter) closed by plastic
lids. Cohorts of 30 larvae of each species were placed at each
of constant temperatures of 19 ◦C (G. punctiger only), 21 ◦C,
22 ◦C and 28 ◦C, maintained in climatised boxes with ±0.3 ◦C
fluctuations. The flat bottom of each tube was covered with
1mm thick layer of pressed cellulose moistened with few
drops of water. The tubes were held in vertical position so
that pressed cellulose substituted for soil and satisfied the
tendency of larvae to penetrate into the ground. The larvae
drilled through the cellulose layer and made a cell where
they could be seen through the tube bottom. Pupation and
adult ecdysis were inspected twice a day (08:00 and 20:00).
While O. bicolor pupated, G. punctiger pupated reluctantly
because the larvae are strictly committed to enter soil where
they pupate quickly. Only three larvae pupated so that the
time of pupation could be recorded, each one being placed
in each of 19 ◦C, 21 ◦C and 28 ◦C temperatures. For precise
determination of development length, adult ecdysis of these
pupae was checked more frequently, in ca. 3 h intervals.
Using arithmetical means of pupal development length
at particular temperatures we calculated lower development
threshold LDT (a temperature below which the development ceases) and sum of effective temperatures SET (number of day degrees [dd ] needed to complete a development
stage). The linear model R = aT + b was used, where R is
development rate (a reciprocal of development length), T is
temperature, and a and b regression parameters. From here
LDT = −b/a and SET = 1/a. The model was used because
at sub-optimum temperatures it enables precise predicting
of thermal time required for the completion of development
stage (Trudgill et al. 2005).
Thermal time for predator development
Thermal time available in dandelion capitula for development of seed predator species was calculated from hourly
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Z. Martinková & A. Honěk
420
measurements of air temperature at 5 cm above soil surface
(available at: http://www.vurv.cz/meteo/). Average daily
thermal time for a species (Tdi ) was calculated using temperatures of the main period of development of dandelion
inflorescences (April 15 – May 31) as:
Tdi =
(Ta − LDTi )/(h · d)
for (Ta − LDTi ) > 0
where Ta is air temperature at 5 cm, LDTi is lower development threshold of a species i, h is number of temperature
measurements per day (24) and d is length of the period (46
days). Thermal time available for development of a species
Ti was then calculated as:
Table 1. Duration of development stages of dandelion capitula
(n = 145) in the open (April – May, 2001).
Duration (days)
Development stage
Stalk extension
Flowering
Seed maturation
Seed dispersal
Mean ± SE
Median
±
±
±
±
1.59
0.97
1.49
0.88
9
3
10
2
23.2 ± 1.56
23
9.2
2.8
9.6
1.7
Total
Ti = Tdi · n
where n is the duration (calendar days) of the period available for development of a species in a capitulum. Data for
calculating Tdi were available for 1993–2005. Tdi differed
between years because of different weather. The years were
ranked according to average thermal time as “cold” (1994,
1997, 1999, 2004), “medium” (1995, 1996, 1998, 2001, 2005)
and “warm” (1993, 2000, 2002, 2003).
Predator populations at seed dispersal
In 2000, age structure of larval populations of both species
was established at the time of seed dispersal. Mature capitula were collected, put by one into small inflated polyethylene bags, closed and stored on a shaded place at 25 ±
1 ◦C for 24 h. Capitula that opened spontaneously during
this storage period were considered “mature”. The capitula
were collected on April 26 (54 mature capitula), April 27
(17), May 2 (53) and May 9 (52). The bags of mature capitula were opened and larvae dispersed from a capitulum
assorted into three size (age) classes: “small” (G. punctiger
<1 mm, O. bicolor <1.5 mm), “medium” (G. punctiger 1–4
mm, O. bicolor 1.5–5.5 mm) and “large” (G. punctiger >4
mm, O. bicolor >6 mm). The differences in age distribution
of larvae of both species were tested by chi-square test.
Thermal requirements of pre-pupal development
Because SET of predator egg and larval development was
not known, taxonomically and trophically similar “model
species” were selected whose SET may be similar to that of
the seed predators. Data (Appendix) on temperature effects
on development length of Coleoptera feeding plant tissues
except wood and dry stored seed were retrieved. Thermal
constants were then recalculated using data of temperatures
≤28 ◦C (Honěk & Kocourek 1990; Honěk 1996) and the linear model (see above). The constants were established for
each batch of individuals of particular origin and (if distinguished) sex, kept under the same food, humidity and photoperiod conditions. In each of these “populations”, thermal
constants were calculated separately for eggs, for larvae and,
if available, also for both stages together.
Results
Development of dandelion capitula
Development of an inflorescence (Table 1) consisted of
long periods of stalk extension (40% of total inflorescence life) and seed maturation (41%), separated by
short flowering (12%) and followed by seed dispersal
(7%). There were small (< 2d) but significant differences between cohorts of inflorescences labelled on successive dates in duration of stalk extension (ANOVA:
Table 2. Average (± SE) development duration of O. bicolor and
G. punctiger pupae at constant temperatures.
O. bicolor
Temperature
◦C
n
days
19
21
22
28
24
19
25
12.7 ± 0.27
11.3 ± 0.19
6.6 ± 0.09
G. punctiger
n
days
1
1
13.0
9.9
1
7.5
F3.141 = 29.67, P < 0.001), flowering (F3.141 = 12.46,
P < 0.001) and seed maturation (F3.141 = 99.91, P <
0.001) because each cohort faced different weather conditions during its development. However, total duration
of inflorescence development (23.2 ± 1.6 d) was similar (F3.141 = 2.57, P > 0.05) in all cohorts. Over the
period of capitula development the effects of weather
fluctuations levelled and the calendar time available for
predator development was generally similar.
Thermal constants of pupal development
Duration of pupa development decreased with increasing temperature, less in G. punctiger than O. bicolor
(Table 2). Consequently, thermal requirements for development were contrast in both species. While G.
punctiger was a “cold adapted” species with low LDT
(6.3 ± 1.58 ◦C) and a high SET (160.5 dd ), O. bicolor
with its high LDT (13.5 ± 0.1 ◦C) and low SET (95.8
dd ) was a “warm adapted” species (Fig. 2). Assuming
rate isomorphy, pupal LDT was a “model” LDT substituted for egg and larval development of the predator
species.
Thermal time available for predator development
Thermal time available for each of predator species
was estimated using calendar time (number of days)
available in the developing capitulum. In G. punctiger
(oviposition at the beginning of stalk extension) development extended over the whole 21.6 calendar days of
capitulum development. In O. bicolor which oviposit
at flowering, earliest egg-laying was supposed to take
place 1.8 d before the flowering, and available time was
then 15.9 calendar days. Calendar time was converted
to thermal time (Table 3). For G. punctiger available
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Development of dandelion seed predators
421
Table 3. Thermal constants, lower development threshold (LDT, ◦C) and sum of effective temperatures (SET, day degrees dd), for egg,
larval and combined (egg + larval when available for the same population) development of phytophagan Coleoptera species. Data
presented for cold adapted species (LDT = 5.1–10.0 ◦C) and warm adapted species (LDT = 10.1–15.0 ◦C)
Egg
Larva
Egg+larva
Species
n
LDT
SET
n
Mean ± SE
Range
26
8.7 ± 0.26
124.8 ± 10.83
54.8–310.3
Mean ± SE
Range
24
11.9 ± 0.25
97.9 ± 13.16
31.1–266.7
LDT
Cold adapted
23
8.4 ± 0.25
Warm adapted
18
11.6 ± 0.31
SET
n
LDT
SET
262.0 ± 16.21
124.8–403.5
10
8.3 ± 0.29
365.8 ± 30.57
212.3–545.2
209.4 ± 18.43
107.9–425.8
8
12.1 ± 0.39
281.8 ± 22.10
184.2–363.8
Table 4. Calendar time (days) and thermal time (dd) available for development of G. punctiger and O. bicolor. Average thermal time
(± SE) calculated for cold, medium temperature and warm years using summation of hourly measurements of air temperatures 5 cm
above ground level, on April 15 – May 31 (see Material and Methods).
Calendar time
G. punctiger
O. bicolor
Thermal time
Mean ± SE
Median
Cold years
Medium years
Warm years
21.6 ± 0.19
15.9 ± 0.19
21
16
133.6 ± 8.1
29.4 ± 2.9
159.8 ± 5.1
43.1 ± 2.1
189.6 ± 8.1
52.7 ± 3.1
0.20
Development rate
G. punctiger
O. bicolor
0.15
0.10
0.05
LDT = 6.3 °C
0.00
0
5
LDT = 13.5 °C
10
15
20
25
30
Temperature (°C)
Fig. 2. Relationship between development rate of pupa and temperature (linear model) in G. punctiger (– – –) and O. bicolor
(—). Intersection point of the regression line with the abscissa
indicates lower development threshold (LDT) of each species.
thermal time was from 120–146 dd in cold years to 173–
207 dd in warm years. For O. bicolor available thermal
time was from 23–34 dd in cold years to 48–60 dd in
warm years. The difference between the time available
for species was caused by difference in their LDT while
annual variation was less important.
Development strategy
We investigated whether thermal time is sufficient to
complete pre-pupal development of predator species
supposing analogy between requirements of “model”
species of phytophagan Coleoptera (Table 4) and thermal requirements of seed predators. In “cold adapted”
model species (LDT = 5.1–10.0 ◦C) probably similar to
G. punctiger, average SET for combined egg and larva
development was 366 dd (above the LDT = 8.3 ◦C), i.e.
more than available for G. punctiger. However, minimum combined SET [established in Oulema melanopus
(L., 1758), Chrysomelidae; Ali et al. 1977] was 212 dd
(Appendix), and the sum of minimum egg SET (55 dd )
and minimum larva SET (125 dd ) (i.e. minima each
of which was established for a different model species)
was only 180 dd. With similar minimum requirements
G. punctiger is able to complete development within
one capitulum. By contrast, in “warm adapted” model
species (LDT = 10.1–15.0 ◦C) probably similar to O.
bicolor, average SET for combined egg and larva development was 271 dd (above 12.1 ◦C) and a minimum
one [Cylas puncticollis (Boehman, 1851), Curculionidae; Nteletsana et al. 2001] was 184 dd (Appendix).
The sum of minimum egg SET (31 dd ) and minimum
larval SET (108 dd ) of different model species was 139
dd. All these values are far above the thermal time available (during its stay in one capitulum) to O. bicolor.
Consequently, O. bicolor cannot complete the pre-pupal
development within one capitulum and the larva should
migrate between the capitula.
To test the prediction that G. punctiger unlike O.
bicolor is able to complete pre-pupal development in
one capitulum age structure of larval populations at
seed dispersal was compared. The expectation was that
population of G. punctiger consist of mature larvae capable of pupation and that of O. bicolor consist of larvae of different age. Age structure of larval populations
of both species (Fig. 3) differed significantly (chi-square
= 43.1, P < 0.001). In fact, population of G. punctiger
consisted of 93 % of mature larvae ready to pupate
while population of O. bicolor contained a significant
proportion of medium sized (32%) and small (15%) larvae not capable of pupation.
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422
12
G. punctiger
O. bicolor
Frequency
0.8
0.6
0.4
0.2
Frequency (no. populations)
1.0
10
8
6
4
2
0
0.0
Large
Medium
Small
Larvae
1
2
3
4
5
6
7
8
9 10 11 12 13 14 15 16 17 18
Lower development threshold (°C)
Fig. 3. Age (size) structure of larval populations of G. punctiger
(n = 84) and O. bicolor (n = 313) in mature capitula before seed
dispersal. The larvae were classified into three size classes (see
Material and methods).
Fig. 4. Distribution of lower development threshold LDT for egg,
larval and pupal development of 27 populations of 14 species
of Curculionidae (LDT of each development stage scores separately). Literature data referred to in the Appendix 1.
Discussion
opment flexible compared to other stages (Honěk et al.
2002; Perdikis et al. 2003). However, the capitulum provides a relatively constant environment and food quality. Therefore, in dandelion seed predators rate isomorphy is likely to be expected, or, if violated, then to a
small extent causing insignificant difference in LDT.
An additional consideration is the analogy between
thermal times required for development of our seed
predator species and “model” species of phytophagan
Coleoptera. This analogy holds because thermal constants of development, LDT and SET, are correlated
(Honěk & Kocourek 1988; Trudgill 1995; Trudgill et al.
2005). Phytophagan Coleoptera were selected as “models” because taxonomic constraints and food specialization affect the LDT/SET relationship (Honěk 1999).
By contrast, effect of body size was not considered because its variation among “model” species was relatively small (Honěk 1999).
The strategy adopted by each of the seed predators
is specific and correlated with their morphology and behaviour after seed dispersal. In G. punctiger there is a
good match between the requirements of the predator
and the thermal time available during development of
capitulum. Glocianus punctiger thermal requirements
are probably near the feasible minimum. The available
data (Honěk & Kocourek 1990; Honěk 1996) revealed
that the LDT of G. punctiger is within the range of
values established for other species of the family Curculionidae (Fig. 4), though at its lower limit. Thermal
time available in dandelion capitula determine that G.
punctiger SET also should be near the lower limits of
possible values. With these minimal requirements the
thermal time available for G. punctiger in dandelion
capitula is just sufficient to complete the development
until the stage of “wandering larva”. Completing development is facilitated because its final part takes place
in the soil after seed dispersal, where the larvae prepare for pupation. Completing development in one capitulum, and the associated thermal adaptations are
This is probably the first study that quantified thermal time required for development of seed predators in
rapidly maturing Asteraceae capitula. Both seed predator species adopted contrast strategies to cope with
temporal environment of dandelion capitula. Glocianus
punctiger is a “cold adapted” species which complete its
pre-pupal development in one capitulum thanks to its
low development threshold. Olibrus bicolor is a “warm
adapted” species destined by its thermal requirements
to migration between capitula. Direct proof of this migration by observing O. bicolor larvae climbing stalks of
dandelion inflorescences is not made as yet. Movement
of larvae on the ground could be probably established
by pitfall trapping, however, this does not demonstrate
vertical migration. The evidence for existing contrast
strategies is based on both observation (development
and temperature of dandelion capitula, age structure
of larval populations) and analogy of thermal requirements (between development stages of predators, and
between related “model” species and predators) which
should be discussed first.
Fundamental analogy is that of LDT for egg, larval and pupal development which are expected to be
identical. This is true under condition of “rate isomorphy” (Jarošík et al. 2002) or “constant rate allocation”
(Perdikis et al. 2003) which assumes that under different temperatures each developmental stage takes a
constant proportion of the total development time. In
fact, “rate isomorphy” holds between larval instars and
frequently also between development stages. It hold for
57% of the total of 426 insect and mite populations and
was only slightly violated in the most of the rest of the
cases ((Jarošík et al. 2002). An important cause of violation of “rate isomorphy” is variation in conditions
of larval development, particularly food quality. Consequently variation in physiological and behavioural aspects of food processing make duration of larval devel-
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Development of dandelion seed predators
enforced by larval morphology that prevents migration
between capitula. The apodous larva is unable to climb
dandelion stalks and re-enter the capitula (A. Honěk &
Z. Martinková, in litt.).
In contrast to G. punctiger, the time granted by a
capitulum to “warm adapted” O. bicolor is short. Although the thermal time necessary to complete development of warm adapted species is generally shorter
than that for cold adapted species (Honěk & Kocourek
1990; Trudgill 1995; Trudgill et al. 2005) the larvae may
have available no more than a half of the time necessary to complete pre-pupal development. No “model”
species with similar low SET has been established. The
difference in thermal requirements of both seed predator species is probably a consequence of a taxonomic
constraint on thermal adaptation which may preclude
changing thermal requirements beyond the limits set
by family or even higher taxonomic affiliation (Dixon
et al. 2005). There are no data on thermal requirements
for Phalacridae, but other species of Cucujoidea (Coccinellidae, Cucujidae, Cybocephalidae, Nitidulidae, Silvanidae) are mostly “warm adapted” (Honěk & Kocourek 1990; Honěk 1996).
The time shortage is compensated for by the supposed ability of O. bicolor larvae to leave declining inflorescence and move to fresh developing one. The campodeiform larva, with its well developed legs (Fig. 1),
is capable of relatively quick movement. In preliminary
experiments larvae put on the ground crawled towards
and climbed dandelion stalks artificially erected in an
experimental arena (A. Honěk & Z. Martinková, in
litt.). In the open, surface migration of larva is probably
very risky. Migration success obviously increases if there
is a dense “population” of dandelion with many flowering capitula, and few other plant species are present.
Low “spatial complexity” of plant stands and limiting development to the period of the highest flowering
intensity is in fact typical for O. bicolor populations
(Honěk & Martinková 2005; Honěk et al. 2005).
There exist direct and indirect evidence that both
species of dandelion seed predators adopted contrasting strategies to cope with time constraint on their development in dandelion capitula. The “cold adapted”
G. punctiger increases the available thermal time by
having a low LTD and succeeds in development in a
single capitulum. By contrast, the “warm adapted” O.
bicolor requires more time to develop than granted by
one capitulum and before pupation necessarily migrates
to another capitulum. The life strategies are correlated
with larval morphology. While the apodous larva of G.
punctiger is unable to move between capitulum, the mobile campodeiform larva of O. bicolor is capable of migration between capitula.
Acknowledgements
We thank Ing. J. Lukáš, PhD. for kindly providing photographs of larvae and Mrs H. Uhlířová for excellent technical assistance. The work was supported by grants Nos
423
1R55010 (ZM) and 0002700603 (AH) of the Czech Ministry
of Agriculture.
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Received February 21, 2007
Accepted January 16, 2008
Appendix 1. Thermal constants, lower development threshold (LDT, ◦C) and sum of effective temperatures (SET, day degrees dd) of
phytophagan Coleoptera used as “model” species. According to lower development threshold the populations are classified as “cold
adapted” (LDT = 5.1–10.0 ◦C) or “warm adapted” (LDT = 10.1–15.0 ◦C). Different populations of the same species with contrast
thermal requirements may be classified as “cold” and “worm” adapted.
Egg
Larva
Species
Cold adapted
Baris lepidii Germar, 1824
Crioceris asparagi (L., 1758)
Epilachna varivestis Mulsant, 1850
Hypera brunneipennis (Boehman, 1843)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Leptinotarsa decemlineata (Say, 1824)
Listronotus oregonensis (LeConte, 1868)
Oulema melanopus (L., 1758)
Oulema melanopus (L., 1758)
Anoplophora malasiaca (Thomson, 1868)
Cetonia aurata (L., 1758)
Costelytra zealandica (White, 1835)
Costelytra zealandica (White, 1835)
Cylas formicarius elongatulus (Summers, 1902)
Hypera brunneipennis (Boehman, 1843)
Hypera meles (F., 1792)
Leptinotarsa decemlineata (Say, 1824)
Leptinotarsa decemlineata (Say, 1824)
Leptinotarsa decemlineata (Say, 1824)
Melolontha melolontha (L., 1758)
Neochetina eichhorniae Warner 1970
Otiorhynchus sulcatus (F., 1775)
Perapion antiquum (Gyllenhal, 1839)
Sitona humeralis Stephens, 1831
Trichosirocalus horridus (Panzer, 1795)
Chrysomela populi L., 1758
Diabrotica barberi Smith and Lawrence, 1824
Diabrotica barberi Smith and Lawrence, 1824
Diabrotica virgifera LeConte, 1868
Galeruca sardoa (Gené, 1831)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Hypera postica (Gyllenhal, 1813)
Phloetribus scarabeoides (Bern, 1856)
Phyllotreta vittata (F., 1775)
Warm adapted
Carpophilus humeralis (F., 1775)
Cassida rubiginosa Müller, 1776
Cylas puncticollis (Boehman, 1843)
Leptinotarsa decemlinaeta (Say, 1824)
Leptinotarsa decemlinaeta (Say, 1824)
Leptinotarsa decemlineata (Say, 1824)
Listronotus texanus (Stockton, 1925)
Pyrrhalta luteola (Müller, 1776)
Reference
LDT
SET
LDT
SET
9.8
8.1
8.6
7.1
9.9
8.6
9.8
8.2
7.9
10.0
9.6
9.9
5.7
7.9
9.0
9.3
9.7
9.3
10.0
8.4
9.2
9.8
6.2
9.2
10.0
5.3
141.7
63.0
98.2
110.0
117.6
123.8
75.2
119.4
84.6
87.5
148.2
167.7
241.6
158.4
88.4
133.3
115.1
54.8
70.6
88.0
310.3
153.3
167.9
63.8
130.0
131.2
7.6
6.6
7.6
6.8
8.9
8.3
9.0
5.9
7.9
8.8
403.5
235.6
278.0
261.3
297.9
239.5
285.8
361.2
149.4
124.8
8.0
9.8
9.5
9.9
9.2
5.8
8.1
8.6
8.7
9.7
9.8
9.4
9.1
202.9
359.7
382.2
277.6
358.5
247.2
208.9
195.7
188.7
233.0
160.1
364.4
209.9
Sherrod et al. (1982)
Taylor & Harcourt (1978)
Fan et al. (1992)
Butler & Ritchie (1967)
Litsinger & Apple (1973)
Guppy & Mukerji (1974)
Tauber et al. (1988)
Simonet & Davenport (1981)
Guppy & Harcourt (1978)
Ali et al. (1977)
Adachi (1994)
Hurpin (1962)
Wightman (1973)
Wightman (1973)
Mullen (1981)
Madubunyi & Koehler (1974)
Chan et al. (1990)
Ferro et al. (1985)
Logan et al. (1985)
Tauber et al. (1988)
Hurpin (1956)
DeLoach & Cordo (1976)
Stenseth (1979)
Julien & Bourne (1983)
Kwong (1980)
McAvoy & Kok (1985)
Loi & Belcari (1983)
Woodson & Jackson (1996)
Woodson & Jackson (1996)
Jackson & Elliott (1988)
Uscidda & Crovetti (1983)
Schroder & Steinhauer (1976)
Schroder & Steinhauer (1976)
Schroder & Steinhauer (1976)
Schroder & Steinhauer (1976)
Hsieh et al. (1974)
Schroder & Steinhauer (1976)
BenAzouri (1990)
Satomura (1950)
11.4
11
14.9
11.3
12.7
10.5
13.5
11.4
292.3
236.7
148.3
159.7
146.1
229.9
284.8
257.0
James & Voegele (2000)
Ward & Pienkowski (1978)
Nteletsana et al. (2001)
Lactin & Holliday (1992)
Lactin & Holliday (1992)
Walgenbach & Wyman (1984)
Woodson & Edelson (1988)
King et al. (1985)
13.1
11.7
13.7
12.0
11.8
11.6
11.5
11.9
34.8
89
35.9
64.5
62.5
62.7
79.0
71.3
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Z. Martinková & A. Honěk
426
Appendix 1. (continued)
Egg
Larva
Species
Anthonomus grandis (Boehman, 1843)
Aphtona abdominalis (Duftschmid, 1825)
Artipus floridanus Horn 1910
Carpophilus hemipterus (L., 1758)
Chrysomela populi L., 1758
Diabrotica barberi Smith and Lawrence, 1824
Diabrotica virgifera LeConte, 1868
Epilachna varivestis Mulsant, 1850
Listronotus oregonensis (LeConte, 1868)
Neochetina bruchi Hustache 1884
Pachnaeus opalus (Olivier, 1792)
Pantomorus cervinus (Boehman, 1843)
Phloetribus scarabeoides (Bern, 1883)
Rhinocyllus concinus (Froelich, 1792)
Sitona humeralis Stephens, 1831
Anthonomus grandis Boehman, 1843
Diabrotica virgifera LeConte, 1868
Hypera brunneipennis (Boehman, 1843)
Hypera meles (F., 1775)
Hypera postica (Gyllenhal, 1813)
Leptinotarsa decemlineata (Say, 1824)
Leptinotarsa decemlineata (Say, 1824)
Leptinotarsa decemlineata (Say, 1824)
Perapion antiquum (Gyllenhal, 1839)
Reference
LDT
SET
12.1
12.3
11.1
10.6
10.9
11.0
10.8
10.4
13.9
10.6
12.9
10.8
14.7
11.1
11.0
43.1
113.1
151.5
31.1
58.9
224.2
253.6
88.8
59.0
145.6
94.3
266.7
79.5
59.2
108.0
LDT
10.9
10.7
11.4
10.8
10.7
10.5
11.2
10.5
11.3
SET
120.3
236.0
176.4
425.8
237.6
130.0
138.4
269.1
173.0
Bacheler at al. (1975)
Fornasari (1995)
Tarrant & McCoy (1989)
James & Voegele (2000)
Loi & Belcari (1983)
Woodson et al. (1996)
Schaafsma et al. (1991)
Mellors & Allegro (1984)
Martel et al. (1976)
DeLoach & Cordo (1976)
Tarrant & McCoy (1989)
Tarrant & McCoy (1989)
BenAzouri (1990)
Smith & Kok (1985)
Sue et al. (1980)
Bacheler et al. (1975)
Jackson & Elliott (1988)
Madubunyi & Koehler (1974)
Chan et al. (1990)
Hsieh et al. (1974)
Ferro et al. (1985)
Logan et al. (1985)
Tauber et al. (1988)
Julien & Bourne (1983)
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