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J.
ent. Soc. slh. Afr. 1989
Vol. 52, No. I, pp. IIf}-128
The effect of temperature on the developmental rate
of the immature stages of large carpenter bees,
Xy/ocopa spp. (Hymenoptera: Anthophoridae)
by
R. H. WATMOUGH
Plant Protection Research Institute, Private Bag X 134, Pretoria
and
H. VAN ARK
Directorate of Biometric and Datametric Services, Private Bag X640, Pretoria 0001
The immature stages of Xylocopa caJfra (1.), X. capitala Smith and X. rufitarsis
Lepeletier, collected in the southern and south western Cape, were kept at
fluctuating temperatures and a range of constant temperatures. Developmental
times at these temperatures were measured. Linear regressions showed that
larvae of Xylocopa caJfra and X. capilala developed at the same rate. The prepupae
and pupae of X. capitala, however, developed more slowly than those of X. caJfra.
No difference in the developmental rate of pupae was evident between X. caJfra
and X. rufitarsis. The minimum lethal temperature for all stages of all three
species was about ISoC. The percentage of X. caJfra developmental time spent in
each of the stages was: egg 13%, predefaecating larva [2%, defaecating larva
10%, prepupa [5% and pupa 50%.
The limited time in spring and summer when mean temperatures are above
15°C and/or a possible shortage of flowers producing pollen and nectar in the dry
later summer cause X. caJfra to be univoltine in the south western Cape. Further
north where the summer is longer and there is summer rain X. caJfra has two or
more generations per year.
INTRODUCTION
The genus Xjlocopa consists of 24 species in southern Africa (Eardley Ig83). It
occurs almost everywhere when suitable nesting substrates are available. These substrates may be partly decayed branches, dead flower or vegetative stems with soft or
hollow centres or hollow reed culms. Thirteen Xylocopa species reach the southernmost
tip of Africa south of 33° south (Eardley Ig83). Together with a wide geographic
distribution Xylocopa shows variation between a facultative multivoltine condition and an
obligatory univoltine one depending on temperature, the degree of wetness of the climate
and the season of maximum rainfall (Watmough Ig74).
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The aim of this work was to obtain data on the variation of the developmental
rates of Xylocopa spp. larvae and pupae with temperature and to apply it in an attempt
to understand the causes ofunivoltinism. Another application for the data was to correct
for the uncompleted developmental time of immature stages in samples of Xylocopa from
natural populations (Watmough 1983)' More than one Xylocopa species was studied in a
range of temperatures to see whether the proportion of developmental time spent in the
egg, larval, pupal and prepupal stages was stable between species and temperatures.
MATERIALS and METHODS
The three Xylocopa species for which data were available were X. caJfra,
X. capitata and X. rufilarsis. In the southern and south western Cape, where all the
material studied for this paper was collected, X. caffra is present as a univoltine race with
obligatory adult reproductive diapause although this species is multivoltine further
north. X. capi/ata is a univoltine species endemic to the south and south western Cape
while X. rufitarsis, univoltine at least in the south western Cape, is more widespread and
reaches the Transvaal (Eardley 1983). The extent to which the univoltine state may be
imposed on X. caJJTa by temperature and rainfall was investigated by comparison of
average monthly mean temperatures and average monthly rainfall (Anonymous 1986)
for sites where univoltine and multivoltine X. caJJTa were studied in outdoor sheds. For
univoltine X. caJJra the sites were at Stellenbosch (Welgevallen Farm) and near
Oudtshoorn (Oudtshoorn Experimental Farm-Rooiheuwel). The multivoltine X. caffra
sites were at Pretoria, Potgietersrus and Mara Experimental Farm (Table 3). The lower
threshold of development for X. caffra was taken as 15°C.
Xylocopa eggs, predefaecating and defaecating larvae, prepupae and pupae were
extracted from their nests obtained during the sampling of natural Xylocopa populations
to study mortality. The nests were cut open to expose the larval cells and each immature
Xylocopa was placed on a piece of paper in a glass vial closed with cotton wool. The stage
of development was observed at 12 hour intervals and recorded as days. An individual
first observed to have entered a stage was taken as having entered that stage half way
between the present and previous observations.
A defaecating larva was readily distinguishable from a predefaecating larva
because it continuously and slowly excretes short, dark, hard, cylindrical faecal
fragments also visible below the skin around the anus. A larva was considered a prepupa
when it had consumed the last of its pollen paste food or was no longer making
continuous chewing movements with its mandibles if any food remained. In several cases
where the pupa died before sloughing off the pupal skin it could nevertheless be seen to
be mature because the pupal skin had been lost from the legs and mouthparts.
All the material used in this study was collected far from the laboratory in
Pretoria and a week or more elapsed before constant temperature facilities were
available. Because of this observations using daily fluctuating temperatures (maximum
and minimum temperatures used to calculate the daily mean temperature) in the
container with the material were made until arrival in Pretoria. The material was then
divided among a series of constant temperature cabinets. The result is a mixture of data
from constant and variable temperatures with some individuals spending a developmental stage partly at variable and partly at constant temperatures. The mean temperature
at which each individual developed through each stage was calculated separately by
obtaining the average daily mean (24 hour period) for the total number of days required
for passing through that stage.
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Watmough & van Ark: effect oj temperature on immature Xylocopa
J2 I
No data were available for the complete egg developmental time because there
was never certainty about the time when an egg found in the field was laid. The egg
developmental time was therefore estimated by multiplying the number of days taken by
eggs collected in the field to hatch by two assuming that on average eggs were halfway
through the egg period when found.
From scatter plots of the reciprocal of developmental time on temperature it
was evident that there were no differences in developemental rate between sexes for any
species or developmental stage, and the two sexes were therefore pooled. An unsuccessful
attempt was made to separate individuals kept at constant temperatures and those kept
at varying temperatures; no clear trends were evident (see also Howe 1967). The
available data did not show the curvilinear trend between developmental rate of the
larval and prepupal stages and temperature found by Davidson (1944), Wigglesworth
(1972), Logan et at. (1976), Taylor (1981) Samson (1984) and many others. Least
squares linear regressions were therefore fitted. For the pupal stage the retardation of
developmental rate at higher temperatures was especially noticeable for X. ca.fJra. Least
square logistic curves (Davidson 1944, Tsitsipis 1980, Gregg 1983, Liu Shu-Sheng and
Hughes 1984) could not be fitted satisfactorily, mainly because the minimum for the
point of inflection could not be found. Formula (10) of Logan et at. (1976), using least
squares fitted well for X. cafJra and X. capitata, but the maximum lethal temperature
estimations were nonsensical (see discussion). Least squares linear regressions were
therefore also fitted for the pupal stage, including only the developmental rates recorded
at temperatures below 33°C. Three pupae with extremely long developmental periods
(>IOO days) at the lowest temperatures (Fig. 3) were not included in the analyses (see
results and discussion). Comparison of developmental rates between species were made
by means of analyses of covariance (Snedecor and Cochran 1967).
TABLE I.
Details of the linear regressions of developmental rate on temperature for two Xylocopa
species. All the F-values due to regression were significant at P :s 0,01.
Developmental
stage
Species
n
Equation
F-value
due to Adjusted
regresR"
S10n
95%
Develop- Confimental
dence
time at limits of
time at
25 QC
2SoC
(days)
(days)
Predefaecating
X. caJJra larva
13 Y =
-0,2823+0,0195x
104,79
0,8964
4,9
3,8- 7,0
Defaecating X. caJJra
Larva X. caPitata
40 Y =
14 Y =
-0,2607+0,OI97x
-0,2840+0,0195x
56,37
14,63
0,586 7
0,5 11 9
4,3
4,9
2,7- 11 ,0
3,3-10,0
Prepupa X. caJJra
Prepupa X. capitata
49 Y
23 Y
-0,1986+0,0142X
-0,1299+ 0,0095x
6°5,96
220,30
0,9 26 5
0,9°88
6,4
9,3
5,1- 8,4
7,0- 13,3
Pupa X. caJJra
Pupa X. capitata
53 Y =
29 Y =
-0,0644 + 0,0045x
-0,oS I9+0,0038x
:206 5,7
0,9754
0,982 5
20,8
23,2
18,9- 2 4,4
21,7-26,3
IS74,o
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J.
122
Table
2.
ent.
SOC.
sth. Afr. Vol. 52, No.
I,
1989
Results of the comparison of developmental rates of two Xylocopa species. Regression
coefficients marked with an asterisk were not significantly different at P :5:: 0,01. F-values
marked with an asterisk were significant at P 2: 0,0 I.
Regression coefficient
F-value
Developmental stage
X. capitala
Defaecating larva
Prepupa
Pupa
0, 01 95"
0,0095
0,003 8
X. caffra
0, 01 97"
0, 01 42
0,0045
0,001
29,°55"
21,5'7"
RESULTS and DISCUSSION
The details of the linear regressions fitted are given in Table 1 and the scatter
plots and regression lines are presented in Figures I, 2 and 3. The results of the
comparisons of developmental rates between species are given in Table 2.
The mean developmental time for eggs was 1 1,0 days, derived from ten
X. caJJra eggs at a mean temperature of 19,6 (± 0,4) °e. This egg developmental time was
added to the summed values of Y (days required for development) calculated from the
equations for successive stages of X. caJfra with X = 19,6°e (Table I). The resulting
total developmental time from the beginning of the egg stage to the end of the pupal stage
was 83,6 days. The egg stage occupied 13% of total developmental time, predefaecating
larva 12%, defaecating larva 10%, prepupa 15% and pupa 50%. These ratios for
X. caffra changed little with temperature. It was therefore assumed that the same applied
to the egg stage and developmental times for eggs at other temperatures besides Ig,6°e
were obtained by extrapolation. The relative length of each of the stages also differed
little between X. caJJra and X. capitata.
During the prepupal stage 47% of the time is spent voiding the waste from
larval feeding and the remaining time is spent resting before becoming a pupa. The pupa
passes through four phases during development, the first being a phase with no
darkening (17% of total pupal developmental time). In the second phase the eyes
become pale red and then darken through brown to almost black (33% of pupal time).
In the third phase the body darkens (21 % of pupal time) and the fourth and final phase
(2g%) starts with the hind legs becoming mobile and ends with the complete mobility
of the adult. In Xylocopa species with black males the percentage of pupal time spent in
each of the four phases is similar in both sexes. Xylocopa males with a dense pelt of pale
yellowish hair covering the body spend 37% of pupal time in the eyes darkening phase
and only 13% in the body darkening phase because the darkening of the body takes
longer to become visible under the developing pelt of pale hairs.
Larvae
The developmental rates of predefaecating and defaecating X. caffra larvae and
defaecating X. capitata larvae were very similar (Table 1 and Fig. 1). Developmental
time at 25°e was about 4,3 to 4,9 days. Four X. capitata predefaecating larvae kept
between 21,4 and 23,2 oe (mean 22,OOe) developed in 4,0 to 6,3 days (mean - 5,5
days). Two X. caffra predefaecating larvae at 22,3 and 23,2 oe developed in 6,l and 4,7
days (mean - 5,4 days) respectively.
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Watmough & van Ark: effect of temperature on immature Xylocopa
123
A
•
G.2
,...
,..
~
--
B
• •
CD
«1
...
-8.
'ii
OA
c:
CD
0
G.2
G)
>
CD
0
U
C
•
.~
.:
•
02
•
~
•
0
20
2S
Temperature
30
35
(0)
Fig. I. The relationship between developmental rate (I/Y) and temperature (OC) for A). X. caffra
predefaecating larvae. B) X. caffra defaecating larvae. C). X. capilala defaecating larvae.
Prepupae
From Figure 2 it is clear that only one X. caffra prepupa showed possible
retardation of development when kept at 36,90C. This individual was omitted from the
calculation.
It can be argued that evidence also exists for retardation of developmental rate
for X. capitata at the higher temperatures. More data are needed, however, to verify this.
From Table I it is evident that the developmental rate for X. capitata is significantly
slower than for X. caffTa. Exclusion of the three developmental rates for X. capitata at the
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J.
124
ent.
SOC.
sth. lIfr. Vol. 52, No.1, 1989
A
•
•
.....,.,
••
O.
.-
•
•.~
••
• •
•
o
.......
"-
-8.
CD
ttl
~
-
lii
c
CD
0
CD
>
CD
0
~l
•
••
•
B
•••
-
.•
~
!
!
!
I
20
25
30
35
Temperature
(t)
Fig. 2. The relationship between developmental rate (I/Y) and temperature (0C) for A). X. caffra
prepupae. B). X. capitata prepupae, The open circle point in A was not included in the
regression calculation because it showed retardation of the developmental rate caused by
high temperalllre,
highest temperatures increased the regression coefficient to 0,0116, but this was still
significantly smaller than the regression coefficient for X. cajjra. The maximum lethal
temperature is below 37,9 to 39,8°C because seven X. caffra defaecating prepupae died
when kept in this range.
Pupae
The retardation of the developmental rate at high temperatures was very
noticable for X. caffra and to a lesser extent for X. capitata (Fig. 3). Formula (10) of Logan
et al (1976) was fitted to these data because this formula is 'of particular utility for
description of systems operating at or above optimum temperatures'. However, the
maximum lethal temperature for X. caffra was calculated at 34, 1°C, well below the
temperature of 37,9°C at which pupae still developed successfully. This may have been
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Watmough & van Ark: effect of temperature on immature Xylocopa
125
largely due to the large variations in developmental rate (heteroscedasticity) at the
higher temperatures. The calculated maximum lethal temperature for X. capitata was
64,4°C which seems far too high. More exact data are needed before the formulae of
Logan et at (1976) or other models can be fitted (see Fig. 3). To obtain comparable
developmental rates for X. caJJra and X. capitata linear regressions were therefore fitted
excluding all developmental rates which were probably retarded due to temperatures
above 33°C. From Table 1 it is clear that the developmental rates for the intermediate
temperatures were significantly slower for X. capitata. Data which were also available
only for X. rifitarsis pupae were treated in the same way as for X. caJJra and X. capitata,
but there was no significant difference between them and those for X. caffra pupae. Pupal
developmental time for X. rifitarsis at 25 cC was 19,8 days.
Successful adult emergence occurred only above 18,0°C. Two X. capitata pupae
taking 107,5 and 114,8 days to develop and one X. caJJra pupa which took 109,6 days
showed retarded development in relation to the temperature of 16,0°C. They were
-..
--
.
/ ...
0
°00
0
00
0
0
0
A
:10\
......
..
.~/
Q.06
"':P
00
/
A
0.03
¥.
( I)
(0
-i
~
-&
(0
B
c
8
(I)
0
Q.06
(j)
>
(I)
0
o.03~
l
/
..
.,
/~~
/
0
~
.
I
20
I
25
Temperature
I
30
I
35
(t)
Fig. 3. The relationship between developmental rate (l/Y) and temperature (0G) for A). X. caifra
pupae (B). X. capitata pupae. The open circle points were not included in the regression
calculations because they were affected by low or high temperatures dose to the thresholds
for development.
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126
J.
ent. Soc. sth. Afr. Vol. 52, No.
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1989
Table 3. The number of months with monthly mean temperatures above and below 15°C compared
for five sites where X. caffra populations were kept for study in outdoor sheds. Also shown
is the total rainfall for each period above and below 15°C. The number of days required
for X. caffra to develop from the start of the egg stage to the end of the pupal stage is
compared for each site with the total number of days in the annual period with monthly
mean temperatures above 15°C.
Stellenbosch Oudtshoorn
Pretoria Potgietersrus
(Welgevallen) (Rooiheuwel)
Number of months with
monthly mean temperature
below 15°C and average
monthly mean temperature
eC) for period (in brackets).
Number of months with
monthly mean temperature
above 15°C and average
monthly mean temperature for
period (in brackets).
Annual average monthly mean
temperature (OC).
Total mm rain in period below 15°C
Total mm rain in period
above 15°C.
Number of days in period
above 15°C = A,
Total days required for development at mean temperature
of period above 15°C
B.
B/A
7(18,9)
7(20,7)
8(:20,2)
10(20,9)
Mara
10(20,8)
16,6
17,2
17,7
19,6
19,6
504,8
101,8
39,0
8,0
9,0
23 6 ,7
134,8
665,0
601,0
46 5,0
212
212
242
30 4
30 4
95,9
0,45
69,4
0,33
75,1
0,3 1
67,3
0,22
68,3
0,22
excluded from the regression calculations. The lower threshold for development must be
between 16"C and 12,3 "c as six X. caffra pupae kept at the latter temperature died after
showing only slight darkening of the eyes. The sparse data available from close to the
lower threshold of development suggests that this threshold is about 15°C.
Ecological considerations
At Stellenbosch X. caffra requires 45 % of the available days in spring, summer
and autumn with average monthly mean temperatures above 15 "C for development from
egg to adult. At Oudtshoorn and Pretoria only about 30% is required (Table 3). X. caffra
is univoltine at Stellenbosch and Oudtshoorn but multivoltine at Pretoria. At Stellenbosch it is likely that the univoltine state is imposed by the shortage of time available
with mean temperatures above 15°C. Although only 45% of the available time is used
for development of the immature stages the fact that the young adult bees need still
further time to mate and mature before they can start to reproduce means that 45 % is
too long and does not leave enough time for a second generation. Also the natural fynbos
vegetation of Stell en bosch has its peak flowering time in spring with a rapid decline into
summer when desiccation occurs (Kruger Ig81). At Oudtshoorn, as at Pretoria, there is
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Watmough & van Ark: effect of temperature on immature Xylocopa
127
enough time for more than one generation, but Oudtshoorn (succulent Karoo) has much
less rain than Pretoria during the period when monthly mean temperatures are above
ISoC (Table 3). The vegetation is therefore likely to be desiccated with few flowers
available for Xylocopa in the latter half of the summer, probably only enough to maintain
adult bees. The vegetation of the Karoo has a spring and an autumn growth period with
summer dormancy (Tainton 1984). Therefore desiccation probably imposes univoltinism on X. caffra by reducing the period with enough pollen and nectar available for
stocking larval cells. At Potgietersrus and Mara only 22% of the available time with
monthly mean temperatures above IS °C is required for development and almost all the
rainfall occurs in this period although there may be times when a shortage of rain
restricts reproduction (Table 3). X. caffra is multivoltine at Potgietersrus and Mara.
Xylocopa will not reproduce in very wet seasons even though temperatures may
be above the developmental threshold (Watmough 1974). However, it is unlikely that
there is enough rainfall to interfere regularly with reproduction at Pretoria, Potgietersrus
or Mara. In the much wetter summer rainfall eastern escarpment of southern Africa
where rainfall may be two or three times that for Pretoria, Potgietersrus and Mara there
are univoltine Xylocopa species on which this state is imposed by the continuous wetness
of the nesting wood with the danger of the pollen paste larval food becoming mouldy.
These Xylocopa species spend the wet summer months entirely as adults with obligatory
reproductive diapause and lay eggs in the latter half of winter and spring when the
weather is mostly warm and dry.
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Accepted 5 May 1988