Zool. J . Linn. Soc., 58: 129-145. With 1 plate and 4 figures
March 1976
Larval mortality and population regulation in
the butterfly Danaus chrysippus in Ghana
MALCOLM EDMUNDS
Department of Zoology, University of Ghana, Legon, Ghana"
Accepted f o r publication April I975
An ecological study was made of a population of caterpillars of the African queen butterfly
(Danaus chrysippus) feeding o n three species of asclepiad plants at Nungua, Ghana, over a nine
month period in 1972-73. The principal sources of mortality of caterpillars are probably the
parasitic hymenopterans Apanreles chrysippi and Charops sp. There is an inverse correlation
between the population of caterpillars and incidence of parasitization. This, and other evidence,
suggests that the t w o parasites are important in limiting the population of Danaus chrysippus
below the level imposed by the available food supply. Early instar caterpillars are probably
palatable t o birds but later instars may be edible or emetic depending o n the toxicity of their
food plant. I t is suggested that the early instar caterpillars are cryptic whilst late instars are
cryptic from a distance b u t conspicuous from nearby, and these may be aposematic or mimetic
according t o the nature of the food plant. Caterpillars parasitized b y Apanteles are paler and
hence more cryptic than normal caterpillars. There is also a green, cryptic morph present in t h e
population at low frequency. It is suggested that there is a correlation between colour of
caterpillars and the principal source of mortality: i.e., cryptic caterpillars are palatable t o birds,
suffer heavy predation b u t a low incidence of parasitization, whilst conspicuous caterpillars are
unpalatable to many birds, suffer little predation but have a high incidence of parasitization.
CONTENTS
Introduction
. . . . . . . . . . . . . . . .
The area studied
. . . . . . . . . . . . . . .
Method
. . . . . . . . . . . . . . . . .
Population estimates
. . . . . . . . . . . . .
Normal development
. . . . . . . . . . . . .
Mortality of eggs
. . . . . . . . . . . . . .
Mortality of caterpillars
. . . . . . . . . . . .
Parasitization b y Apanteles chrysippi Vier.
. . . . .
Parasitization b y Sturmia flavohalterata Bischof.
. . .
Parasitization b y Charops sp.
. . . . . . . . .
Other sources of mortality
. . . . . . . . . .
Pupae
. . . . . . . . . . . . . . . . . .
The effect of parasitization on the population of Danaus chrysippus
Colour of larvae
. . . . . . . . . . . . . . .
Sex ratio
. . . . . . . . . . . . . . . . .
Discussion
. . . . . . . . . . . . . . . .
Summary
. . . . . . . . . . . . . . . . .
Acknowledgements
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References
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Present address: Department of Biology, Preston Polytechnic, Corporation Street, Preston PR1 2TQ.
129
130
M. EDMUNDS
INTRODUCTION
Danaus chrysippus L. (known as the African queen or African monarch) is
one of the commonest butterflies in the savanna regions of Africa south of the
Sahara. I t is believed to be aposematic since there are records of its being
rejected as food by various species of birds (summarized by Reichstein, von
Euw, Parsons & Rothschild, 1968), and it is reported to be the model for a
number of species of mimetic butterflies (Owen & Chanter, 1968; Edmunds,
1969). The sex ratio and morph frequencies of Danaus chrysippus in east
Africa have been described by Owen & Chanter (1968), but apart from this
there appears t o be no study of the ecology of this insect.
Danus chrysippus feeds on plants of the family Asclepiadaceae (Owen &
Chanter, 1968). The population could be regulated by any of the following:
(1)
(2)
(3)
(4)
(5)
predators of the immature stages,
parasites of the immature stages,
shortage of food,
predators of the adult,
physical environmental factors.
Since some species of asclepiad plants are common in southern Ghana but
rarely decimated of foliage by Danaus caterpillars, the population appears t o be
maintained below the limit imposed by food supply. The present study is an
investigation of the mortality of the immature stages of a population of Danaus
chrysippus in southern Ghana. The palatability spectrum of adult butterflies to
potential predators in the area has been investigated by Brower, Edmunds &
Moffitt (1975). On the basis of these two studies it is possible to suggest
what may be the most important factors limiting this population of D.
chrysippus.
THE AREA STUDIED
The area investigated is part of the University of Ghana farm at Nungua, c.
20 km northeast of Accra, Ghana, latitude 5"41'N, longitude 0" 06'W.
Although the farmland provides an artificial habitat, the food plants concerned
occur with more or less equal frequency both on the grassland enclosed for
cattle and on the undisturbed savannas of the Accra Plains. The ecology of the
area is described by Lawson & Jenik (1967) and Okali, Hall & Lawson (1973),
and a map of the artificial lake on the farm is given by Thomas (1968). The
area from which caterpillars were collected comprises a strip of land 1000 m
long by 200-300m wide along the southern shore and near the dam of this
lake.
METHOD
Between 16 October 1972 and 25 July 1973, 25 collections of caterpillars
were made from asclepiad plants in the study area. At intervals of from one to
four weeks individual food plants were carefully searched and all caterpillars
and eggs found were recorded. Most of the caterpillars were collected and then
reared on the same food in the laboratory t o establish whether or not they
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
131
were parasitized. Not all plants were searched on each visit t o the area, and at
least two weeks elapsed before a particular plant was searched again in order to
allow the population to recover from the effects of the collection.
Three species of food plant occur in the area: Calotropis procera (Ait.),
Leptadenia hastata (Pers.) and Pergularia daemia (Forsk.). There were 18
Calotropis plants located in four groups. These plants have large, widely spaced
leaves, and it is easy t o search every plant thoroughly so that every egg and
caterpillar is recorded. Twenty-one Leptadenia plants occurred in two extensive
patches. Leptadenia is a straggling plant of thickets and hedges, and its mass of
intertwined branches means that it is difficult to search thoroughly. Five
Pergularia plants occurred in a small part of the area. This is also a straggly
climbing plant, difficult to search thoroughly for caterpillars in the wet season
when the growth is lush, but fairly easy to search in the dry season when
growth is small and when its leaves wither due t o water shortage.
POPULATION ESTIMATES
Because it was only possible to search Calotropis at all thoroughly for
caterpillars, estimates of the relative abundance of Danaus are based only on
collections from this plant. It was intended t o use the average number of
caterpillars per plant as an index of population size, but it was found that
caterpillars occurred much more frequently on some plants than on others.
Since not every plant was searched on each visit, such a method would not give
reliable estimates. The Calotropis plants grew in four places with 2, 3, 4 and 9
plants close together at each place. These four groups had respectively 4.8,4.2,
4.0 and 0.6 caterpillars per plant per visit. Hence to provide an index of
population the average numbers of caterpillars per plant from all plants in the
first three groups was used. Examination of plants from elsewhere on the Accra
Plains confirms that there is usually a lower density of caterpillars on dense
aggregations of Calotropis than there is on isolated plants or on isolated groups
of two or three plants. Thus, on disturbed ground at Teshie where there are
several hundred Calotropis close together, 50 plants examined 12 times over a
ten-month period in 1972-3 had from 0 to 16 caterpillars, an average of 0.105
caterpillars per plant. Even lower densities were found at Mampong quarry,
Shai Hills, (0.07 caterpillars per plant) and at Tema (0.00) where Calotropis is
even more abundant. On the other hand nine isolated plants from Kwabenya
and Legon averaged 5.0 caterpillars per plant.
The population index of caterpillars on the nine Calotropis plants from
Nungua described above shows a peak in January and February, a decline in
March, and a further peak in July (Table 1 and Fig. 4). Because of small
numbers of plants searched or of caterpillars found in February, March, April
and June, the bimonthly index given in Fig. 4 is probably more reliable than
the monthly figures given in Table 1. The population index based on the
numbers of eggs per plant is also given in Table 1 and for the first few months
shows a close correspondence with the numbers of caterpillars. The peak of
eggs, however, is in January, slightly earlier than the peak of caterpillars.
Assuming that the population peaks in January-February and in July do reflect
the population size of caterpillars, then the index of population can be used t o
relate incidence of parasitization to population.
M. EDMUNDS
132
Table 1. Population index of Danaus chrysippus based on
searches of nine Calotropis procera plants at Nungua, 1972-3
Month
November
December
January
February
March
April
MY
June
July
Number of
plants searched
Number of
eggs
Number of
Caterpillars
Eggs per
plant
Caterpillars
per plant
15
16
8
3'
6'
3'
9
6'
16
16
23
26
4
10
1
33
92
1.1
1.4
3.3
1.3
1.7
0.3
2.2
5.8
7.0
13.3
0.5
5.7
1.6
1.7
4.7
0
0
2
56
40
3
17
14
10
75
0.0
0.0
0.1
Indicates small sample liable to relatively greater error.
NORMAL DEVELOPMENT
In Ghana Danaus chrysippus eggs normally hatch within one week. The first
instar caterpillar is about 3 mm long and the caterpillar passes through five
instars before pupating at a length of about 3 5 mm. The caterpillar stage lasts
from nine to nineteen days (mean 12.0). The pupal stage lasts six or seven days
between November and March, but eight or nine days in July and August. This
difference is probably a direct effect of temperature: July and August are the
coolest months of the year, January and February are the hottest, and i t was
found that pupae reared in a cooled, air-conditioned room took up to 15 days
to hatch. Hence the entire life cycle can be completed in about four weeks,
agreeing with the observations made by Owen & Chanter (1968) in Uganda.
MORTALITY O F EGGS
Danaus chrysippus females lay their eggs singly on the under sides of leaves
so that one has to search many plants in order to find many eggs. This
behaviour is suggestive of high egg loss since spreading the eggs widely increases
the chances that a few will escape detection by predators. No careful study of
egg predation was made but an approximate estimate of egg loss can be
obtained from records of eggs present on each plant on a particular day
compared with the number of caterpillars of appropriate size on the same
plants one week later. Calotropis plants with a total of 14 eggs were examined
six or seven days later and only two caterpillars were found, thus indicating a
mortality of 86%. Ants were commonly seen foraging over Calotropis plants
and Pheidole megacephala was once found eating a Danaus egg. Owen (1971)
also considers ants to be serious predators of eggs of Danaus in Sierra Leone: he
estimates that 90%of all eggs laid are destroyed by ants, but unfortunately the
data on which this estimate is based are not given. However, in view of my own
findings described above, I would consider his estimate to be reasonable.
MORTALITY OF CATERPILLARS
Parasitization by Apanteles chrysippi Vier.
Apanteles chrysippi is a braconid which emerges from final instar caterpillars
and pupates round the skin of the dying host. Fifty or more Apanteles
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
133
normally emerge from each large (3040 mm long) caterpillar, but occasionally
a much smaller number emerge from caterpillars less than 30 mm long. I t is
usually possible to identify which last-instar caterpillars are parasitized by
Apanteles since they have a paler colour with less contrasting black bands than
do normal caterpillars.
Table 2. Incidence of parasitization by Apanteles
chrysippi in caterpillars of different length when
collected
Body length of
caterpillars (mm)
Number
parasitized
3
Number not
parasitized
12
74
23
11
9
8
0
11
11
20
23
20
23
4-6
7-9
10-12
13-21
22-27
28-40
%
parasitized
0
12.9
32.4 \ x ? l ) = 5.497,
64.5 J
P < 0.02
71.9
71.4
62.2
14
Note: Caterpillars collected in June and July have been omitted because
the mortality due to Apanteles at this time was very low (see
Table 3).
Table 3. Estimated mortality of Danaus chrysippus caterpillars due
to parasites
Apanteles chrysippi
Month
November
December
January
February
March
April
May
June
July
Charops
tachinid
n
% mortality
n
83
85
45
13t
18
38
29
8
0
3
5
8
sot
5
0
68
70
Ot
7
19
4
30
71
60
38
10
24
20
6
77
% mortality
10
0
1
30
Ot
1
% mortality
n
0
0
0
19
50
40
3
35
Ot
20
20
8
15
15
sot
5
42
71
total
mortality %
83
88
50
24
80
80.
90
80
50
n, Sample size.
Includes two caterpillars infected both by Apanteles and by Charops. The overall %
mortality is derived by deducting one from each of the totals of larvae killed by these
two parasites.
t Unreliable since based on very small samples.
Table 2 gives the incidence of parasitization by Apanteles chrysippi for
caterpillars of different length when collected. Infection could not occur in the
laboratory hence all parasitized individuals must have been oviposited in the
field. Since caterpillars of 10-12 mm and > 1 3 mm suffer a similar level of
parasitization whilst smaller caterpillars have a lower incidence, it is clear that
infection normally occurs in caterpillars between 4 and 10 mm in body length.
Hence any assessment of the incidence of parasitization in the population must
be based only on caterpillars which are > 10 mm in length when collected. The
slightly lower incidence of parasitization in very large caterpillars: though not
134
M. EDMUNDS
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
135
I""
80 -
-
.-.\
60 , \ " 40
-
Charops0 ,
20 -
-
..............a**..,
____-
0 1 oLI.l.l.l.o
1
I
Nav
Dec
--0-
I
Jan -Feb
/.'
-
0
,
,
....... ....Sfurmia
.............. ...............
/ -
0
4.<,,.
1
Mar-Apr
1
May -Jun
I
Jul
Figure 2 . Incidence of parasitization of Danaus chrysippus in monthly and bimonthly samples
by Apanteles chrysippi, Charops sp. and Sturmia flavohalterata. Nungua, 1972-73.
statistically significant, may be due t o the fact that many parasitized
caterpillars of this size have already been killed and hence cannot be sampled.
Figure 1 gives the numbers of survivors and the mortality due to Apanteles
of all caterpillars 2 10 mni throughout the study period. In order to compare
this with the population index the figures have been summed in monthly or
bimonthly samples and presented in Table 3 and Fig. 2. There was high
mortality (65-90%) due to Apanteles in November and December and from
March to May with much lower mortality in January and February (38%)and
in July 7%.
Parasitization b y Sturmia flavohalterata Bischof
Out of the entire sample of 338 caterpillars collected and reared to adult,
eight (2.4%) were parasitized by the tachinid Sturmia flavohalterata
(determined by R. W. Crosskey). When collected these caterpillars measured 4,
4, 5 , 5, 7, 7 , 11 and 26 mm length
Infected caterpillars grow normally and pupate, but after a few days the
pupa turns dark brown and the tachinid larva burrows out of the side of the
chrysalis. In nature it probably falls to the ground and pupates in the soil. Two
tachinids emerged from one caterpillar and pupated successfully, but the
remaining pupae each had a single parasite. If the tachinid- oviposits in the egg
or first instar caterpillar, then the incidence of parasitization must be based on
the entire sample collected, as shown in Table 3 . Alternatively, if the tachinid
eggs are laid on the food plant and then eaten by the caterpillar, the incidence
of parasitization should be based only on final instar caterpillars. In either case
the incidence of parasitization is very low: Table 3 and Fig. 2 indicate a peak of
only 8% in February. This contrasts with Owen's report (1971) that infestation
by tachinids is nearly 100%in Sierra Leone, particularly at the beginning of the
dry season. At Nungua no tachinids were found at the beginning of the dry
season out of 32 caterpillars (two in October, 30 in November).
136
M. EDMUNDS
Parasitization b y Charops sp.
The third parasite found was an ichneumonid of the genus Charops
(determined by T. Huddleston). Numerous caterpillars collected when only
4 mm long were found to be parasitized so infection presumably occurs in the
egg or possibly the first-instar larva. The caterpillar grows normally until about
2 0 m m long when the parasite emerges and pupates hanging from a silken
thread attached close t o the shrivelled skin of the dying caterpillar. One
parasite emerged from a 22 mm long caterpillar, but although it pupated
normally the insects which emerged from the chrysalis were five Apanteles
ckrysippi. Presumably this caterpillar had been oviposited both by Charops and
by Apanteles with the latter acting as a hyperparasite. In a second doubly
parasitized caterpillar the Charops emerged and pupated successfully but a few
Apanteles also emerged from the caterpillar prematurely and died. Since
Charops emerges from caterpillars of about 20 mm length, estimates of the
incidence of parasitization must be based only on caterpillars < 19 mm length
when collected.
Table 3 and Figs 2 and 3 show that there were no Ckarops between
November and January but that the incidence of parasitization then rose
steadily to reach 42% by July. I t is not known if Ckarops was completely
absent between November and January or if it occurred at very low frequency,
but a single Charops was reared from a caterpillar collected at Legon in
October.
Other sources of mortality
Fortysix caterpillars (12.0%) died as a result of careless handling or for some
unknown cause and these have been omitted from the estimates of mortality
given in Table 3 . Some caterpillars released a dark brown fluid as they died and
may have been infected with a virus. There may also be mortality due t o heavy
rain or to hot, dry winds at certain seasons, but this has not been investigated.
Predators such as wasps, birds and lizards may also take some caterpillars, but
again no attempt has been made t o estimate these factors.
PUPAE
No data were collected o n mortality of pupae. Caterpillars pupate either on
the food plant, or, more usually, on neighbouring plants. The pupae can be
either green or brown depending on the immediate environment of the insect
just prior to pupation. In plastic containers most pupae on the lid were brown
but if green leaves were present and the insects pupated on or near these, they
turned into green pupae. The factors determining colour of pupae in Danaus
chrysippus are not known, but in papilionids they have been studied by Clarke
& Sheppard (1972) and by West, Snellings & Herbek (1972). Since two colours
of pupae occur, and since they are usually found on matching backgrounds,
this suggests that predation by visually hunting predators occurs and that pupal
colour and matching of background are an evolutionary response to selective
predation.
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
"
2
137
M. EDMUNDS
138
THE EFFECT OF PARASlTlZATION ON THE POPULATION OF
DANAUS CHR YSIPPUS
Figure 2 and Table 3 give the percentages of mortality due to the three
parasites whilst the overall mortality (i.e., the sum of that due to the three
parasites but counting doubly parasitized individuals as only dying once)
is given in Table 3. In Fig. 4 the % of non-parasitized caterpillars
(= 100 minus %mortality) is plotted together with the population index
calculated as described earlier. The periods of high population coincide with high
lo
'
"
Nov
Dec
Jan-Feb
Mar -Apr
- Jun
Jul
Figure 4. Relationship between population index of D. chrysippus caterpillars on Calofropis
procera plants at Nungua (histogram) and percentage of caterpillars which escaped parasitization
(solid line), 1972-73.
survival of caterpillars. Unfortunately the monthly or bimonthly samples are not
sensitive enough to determine whether the population crash is preceded and
caused by high incidence of parasitization, and conversely whether the
population build-up in June-July is facilitated by low incidence of parasitization. Nevertheless it is possible that parasites regulate the population of Danaus
chrysippus at Nungua for the following reasons:
( 1 ) There is a very high incidence of parasitization (see Table 3 last column).
(2) Even with high levels of caterpillar infestation Cdotropis is very rarely
defoliated. This indicates that some factor other than food supply is
limiting the population.
( 3 ) Scattered plants have high caterpillar density whilst densely grouped
plants have low density (see earlier). This suggests that in high density
plants the parasites are so successful at finding caterpillars that these are
more heavily parasitized than are caterpillars on scattered plants, but
unfortunately my samples are not large enough to be able to test this
statistically.
Further evidence that parasites are density-dependent in their effects should
be obtained if it can be shown that where there are many caterpillars per plant
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
139
these suffer a higher mortality than do caterpillars which occur singly. For
Charops this is clearly demonstrated in the June and July samples when this
parasite was abundant (Table 4). For Apanteles it is necessary to consider
caterpillars greater and less than 10 mm separately since they suffer different
incidences of parasitization, and since they may belong to different broods and
hence reflect different densities of caterpillar for the ovipositing parasite. In
both groups there is a higher survival of single caterpillars than of caterpillars
with three or more per plant (Table 5), but the figures are not significant.
Table 4. Relationship between number of
caterpillars per Calotropis plant and incidence
of parasitization by Charops
Number of caterpillars per plant
1-2
3-4
5-7
10-17
Sample size
Number parasitized
% parasitized
16
1
6
7
1
14
12
6
50
48
25
52
3 1/60
2/23
xtl) = 11.087
P < 0.001
Table 5 . Percentages of caterpillars parasitized by Apanteles chrysippi with
different numbers of caterpillars per
Calotropis plant
Caterpillar size
<lo mm
210 mm
Numberof
caterpillars
per plant
1
2
3
Xt2)
p
5/18(28%)
6/24(25%)
56/130(43%)
3.84
0.2 > P
> 0.1
9/20(45%)
16/22(73%)
67/99 (68%)
4.42
0.2 > P
> 0.1
These data indicate that Charops and probably Apanteles may be density
dependent in their effect and hence that they are regulating the population of
Danaus chrysippus. However, whilst Apanteles is clearly of major importance in
November and December, Charops is the most important parasite in the rainy
season of June and July. Tachinids are of little importance in this population
but Owen (1971) considered tachinids to be the most serious parasites in Sierra
Leone.
COLOUR OF LARVAE
Two of the caterpillars collected at Nungua lacked black bands on the body
and hence appeared bluish or greenish due to the yellow and white of the body
and the dark green of food in the gut showing through the body wall
(Plate 1A). First instar larvae also have little pigment so the incidence of this
green morph must be based on caterpillars which were greater than 6 mm long
10
140
M. EDMUNDS
(i.e. second instar) or which lived in captivity to a size greater than this. One
green caterpillar was found in March out of a total of ten caterpillars, the other
in April out of 28 caterpillars, giving a frequency for these two months of 5%.
No green caterpillars occurred from October to February and from May t o July
(sample sizes for these months were 3 , 32, 80, 62, 40, 20, 6 and 81), so the
overall frequency of the morph is two out of 362, or 0.55%. The first green
morph was collected from Calotropis on 14 March and was reared from 8 mm
long to maturity. The second was 24 mm long when collected from Leptadenia
on 8 April and was parasitized by Apanteles. The green morph is very cryptic
on Calotropis, at least to the human eye. Hence if visually hunting predators
are important then one would expect the green morph to be at a selective
advantage relative to the typical form.
Larvae parasitized by Apanteles are also paler than are typical larvae with
less conspicuous black bands (Plate 1B). This makes them less conspicuous to
the human eye, and hence I presume less likely to be seen and eaten by birds.
However, caterpillars parasitized by Apanteles usually rest for a day or two in
conspicuous places on branches before the parasites emerge so they may be
found by birds at this time. If birds (or other visually huntingpredators) take
more typical caterpillars in proportion to their frequency in the population
than they do of parasitized ones, this will be of benefit to the parasite
population, and selection would favour those Apanteles which alter the colour
of the host to the greatest extent t o make it more cryptic. Conversely selection
should also favour those Danaus genotypes which, when parasitized, are more
conspicuous and hence are more likely to be preyed on. This could only
operate through kin selection since the caterpillar which is parasitized is certain
to die. Although experimental evidence is lacking this reasoning implies that
the colour of the parasitized larvae is of benefit to the parasite, not to Danaus.
SEX RATIO
Owen & Chanter (1968) examined the sex ratio of wild populations of adult
Danaus chrysippus in Uganda and found that whilst some populations have a
1 : 1 sex ratio, in others there is an excess (64%) or a deficit (31%) of males.
An apparent excess of males could be due to greater activity and hence a
greater likelihood of capturing males than females. This is also what I found
when capturing adults by hand net at Legon and Achimota between October
1965 and July 1966: I captured 225 males and 91 females (71.2%males) but I
recaptured only three males and eight females. During this survey I noticed that
many insects were moving southwards and if males move more than females
this would account for the excess of males.
Amongst the butterflies reared from caterpillars collected at Nungua 88 were
male and 86 female, whilst of a smaller sample collected at Legon nine were
male and ten female. Evidently in both of these areas the sex ratio of
caterpillars and of newly emerged adults is close t o equality.
By studying broods from individual female Danaus chrysippus Owen &
Chanter (1968) found that nine females produced offspring with an equal sex
ratio whilst 11 others produced only female offspring. This habit would
account for the populations they observed in which females were more
abundant than males.
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
141
I have not studied broods from isolated females. but nevertheless there is
evidence for some unusual features in the sex ratio of caterpillars from Nungua.
Although the overall sex ratio was close to equality, one large collection of
caterpillars from a single Calotropis plant on 29 January 1973 produced 17
males and only five females. This differs significantly from the expected 1 : 1
ratio (xf,,= 6.54, P < 0.01). These 22 caterpillars ranged in size from 4 to
40 mm so could not all have come from eggs laid by the same female at the
same time. The ten largest caterpillars were between 16 and 40 mm and could
have come from eggs laid on the same day. These were all male; the probability
of this occurring by chance with a 1 : 1 sex ratio is less than 0.001. The
remaining caterpillars were all between 4 and 8 mm long and had a near equal
sex ratio: 7 d : 5 0 . Thus there is some evidence forrtheroccurrence of’all male
broods in Danaus chrysippus in Ghana. If this batch of ten males is omitted
from the total number of caterpillars reared to maturity, the sex ratio becomes
78 : 86 which is not significantly different from equality.
DISCUSS ION
In this paper I have suggested that the population of Danaus chrysippus at
Nungua is regulated by parasites, especially Apanteles chrysippi and Charops
sp.; that shortage of food is not a limiting factor; and that predators are
probably not important sources of mortality of the caterpillars. My own
experience of rearing cryptic palatable caterpillars (over 30 sphingids of eight
different species) suggests that these have a low mortality due to parasites and a
high mortality due t o predators (see also Curio, 1970a,b), whilst aposematic
caterpillars (Danaus chrysippus and the ctenuchid Euchromia lethe) have high
mortality due to parasites and (probably) low mortality due to predators. This
generalization is supported by more detailed studies of other workers,
especially on two species of Pieris one of which is cryptic and palatable, the
other more conspicuously coloured and distasteful to some predators (see
Table 6). Table 6 only gives data relating to parasitization of late instars,
principally by Apanteles, because this is often the commonest parasite present.
However, it should be recalled that in D. chrysippus when Apanteles is scarce
(7% of the population parasitized) another parasite, Charops, is very common
(42%parasitized).
Too much reliance should not be placed on the figures given in Table 6 since
there is tremendous variation in incidence of parasitization both within a single
population in different years and between different populations of the same
species. Furthermore, several of the “conspicuous caterpillars” listed in Table 6
are probably not typical of aposematic caterpillars. Thus Pieris brassicae
caterpillars are edible to some birds and are cryptic on certain backgrounds
(Baker, 1970), whilst some populations may suffer higher loss from predators
(birds and arthropods) than from parasites (Apanteles) (Chansigaud, 1964). In
this particular experiment the loss due to predators was positively density
dependent while that due to parasites was negatively density dependent hence
the predators may have been regulating the population just as they probably do
with many cryptic caterpillars.
Tyria jacobaeae is brightly coloured and distasteful to predators so probably
has aposematic coloration. In the one population that has been intensively
Apanteles glomeratus (L.)
A . glomeratus
A. glomeratus
Apanteles popularis Hal.
Apanteles chrysippi Vier
Patelloa sp (Tachinidae)
Apanteles caberae Marshall
Apanteles rubecula (Hal.)
A . rubecula
A . rubecula
Apanteles glomeratus (L.)
A. glomeratus
A . glomeratus
Species of parasite
79 (68-85)
9 months
4 months
Young, 1971
22.0 (12.8-35.7) Dempster. 1971
67 (7-85)
This paper
1 year
5 years
Moss, 1933
Richards, 1940
Baker, 1970
Moss, 1933
Richards, 1940
Dempster, 1967
Moss, 1933
Richards, 1940
Baker. 1970
Klomp, 1966
Reference
84.2
53.5 (29-100)
80
1.6 (0-9.4)
12.3
29.8,69.0*
1.9,4.0,20.4
18.8
3.4 (0-16.7)
12
parasitized:
mean (range)
~~~
1 year
5 years
Not given
3 years
1 year
5 years
1 year
1 year
15 years
Period of
study
29.8 was for a plot of widelyspaced food plants, 69.0 for a dense mass of food plants.
Pieris brassicae L.
P. brassicae
P. brassicae
Tyriajambaeae L.
Danaus chrysippus L.
Battus polydamus L.
CONSPICUOUS CATERPILLARS
&palus pinkrrius L.
Pieris rapae L.
P. rapae
P. rapae
P. r a p e
P. rapae
P. rapae
CRYPTIC CATERPILLARS
Species of Lepidoptera
% of late instars
Table 6. Incidence of parasitization of late instar caterpillars of cryptic and conspicuous
Lepidoptera
N
P
.-I
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
143
studied, Dempster (1971) found a low incidence of parasitization and a high
loss due to arthropod predators, but whether this is typical for other
populations is not known. Much more extensive life table data are required
before the hypothesis of a relationship between conspicuousness and
parasitization can be regarded as proven.
The palatability of Danaus chrysippus caterpillars to predators has not been
tested, but, like the American monarch (D.plexippus), it feeds on asclepiad
plants and accumulates toxins from the plants in its body. The eggs and first
instar caterpillars presumably have little or no cardenolide so are probably
edible. Later instars (and adults) which have fed on Calotropis procera contain
considerable quantities of cardenolide and are presumably emetic to small birds
which eat them, but caterpillars which have fed on Leptadenia hastata contain
little or no cardenolide so are presumably perfectly edible to these birds
(Brower, Edmunds & Moffitt, 1975). Hence it is questionable whether it is of
advantage for African queen caterpillars to be conspicuous since such
caterpillars on Leptadenia and similar plants would be quickly found and eaten
by birds. The conspicuousness of caterpillars to birds has not been studied, but
the first instar caterpillars have such narrow transverse bands of black, white
and yellow that they are difficult to see to the human eye, and hence they are
probably cryptic t o birds as well. Even the later instars are not easily seen from
a distance, and I have elsewhere (Edmunds, 1974) suggested that caterpillars of
D. chrysippus (and of T. jacobaeae) are cryptic from a distance but
conspicuous from nearby. Caterpillars on Leptadenia would then be batesian
mimics of caterpillars on Calotropis, but the primary defence of all caterpillars
would be crypsis.
A survey of the cardenolide content of D,chrysippus butterflies from Legon,
which is close t o Nungua, has revealed that only 6% of the population have
appreciable quantities of cardenolide implying that they are toxic to predators
and have fed OI? Calotropis (Brower, Edmunds & Moffitt, 1975), whilst the
rest of the population had fed on plants with low or zero cardenolide content.
In such a population one might expect selection t o favour caterpillars which are
always cryptic since the chances of a bird finding an emetic caterpillar are
small. Hence one might expect to find a high frequency of caterpillars of the
green, cryptic morph in populations feeding largely on plants of low
cardenolide content, and a low frequency of green caterpillars in populations
feeding largely on plants of high cardenolide content. Further work on
different populations is required to confirm this hypothesis.
No information is available on mortality of adult Danaus chrysippus at
Nungua, but eight of the 91 females captured, marked and released at Legon
and Achimota in 1965-6 were subsequently recaptured. They had lived a total
of 28 days giving an expectation of life of 28/8 = 3.5. (Of the 225 males
captured in the same period only three were recaptured, each having survived
only one day. This difference is probably due to the males being partially
migratory, but it does mean that males have to be ignored for the purposes of
calculating mortality. I t also renders the survival rate of 0.775 given in
Edmunds, 1969 (fig. 2), unreliable since this was based on both sexes
combined.) I have shown elsewhere (Edmunds, 1969) that expectation of life
calculated in this way is very similar to the figure derived from survival rate
calculations using the method of Fisher & Ford. Using the formula E = 1/( 1-s),
144
M. EDMUNDS
where E is the expectation of life and s the survival rate, this gives an estimate
of survival rate of 0.71, or a daily mortality of 29%. Female Hypolimnas
misippus captured over the same period have an expectation of life of 2.93
days and a mortality of 34% per day. These survival rates are slightly lower
than those of other Lepidoptera (summarized by Cook, Frank & Brower,
1971).
SUMMARY
As part of an ecological study of Danaus chrysippus in Ghana, caterpillars
were collected from three food plants at Nungua at intervals between October
1972 and July 1973.
An index of population was calculated on the basis of the numbers of
caterpillars per Calotropis plant in a part of the study area. The population
index was high in January and February, declined in March, and rose to a
second peak in July.
The entire life cycle takes about four weeks in Ghana.
Eggs are laid singly on the undersides of leaves and probably suffer a high
incidence of loss from ants.
Caterpillars suffer high mortality (65-90%) from Apanteles chrysippi in
November and December and from March to May with much lower mortality
in January-February (38%) and in July (7%). Charops sp. was not recorded
before February but then increased in frequency till in July 42% of caterpillars
were parasitized. A tachinid parasite was also present but was never common.
Other sources of mortality (viral infection, physical factors, predators)
probably accounted for some losses but were not estimated. I t is suggested that
Charops and Apanteles exert some regulating effect on the Danaus population
since (a) they occur at high frequency when the caterpillars are at high density
and at low frequency when caterpillars are at low density; and (b) there is an
inverse correlation between population index and incidence of parasitization.
Caterpillars are dimophic with a cryptic green morph occurring at low
frequency in the population. Pupae are also dimorphic (green or brown), but
this is an environmental polymorphism suggesting that it has evolved as a result
of visually hunting predators taking more conspicuous pupae than cryptic
pupae.
Caterpillars parasitized by Apanteles are paler and more cryptic than are
unparasitized caterpillars suggesting that they may be less likely to fall prey to
birds.
The sex ratio of caterpillars is 1 : 1 but there is evidence for the existence of
some all male broods.
I t is suggested that there is a correlation between colour of caterpillars and
the principal source of mortality: i.e. cryptic caterpillars are palatable t o birds,
suffer heavy predation but a low incidence of parasitization, whilst conspicuous
caterpillars are unpalatable to many birds, suffer little predation but have a
high incidence of parasitization. However, intermediates between these two
extremes occur, for example, Danaus chrysippus caterpillars are probably
cryptic from a distance but conspicuous from nearby,
ACKNOWLEDGEMENTS
I am grateful t o Messrs R. W. Crosskey, T. Huddleston and G. E. J . Nixon of
the British Museum for identifying the parasites; t o Mr J . B. Hall of the
Plate 1
M. EDMUNDS
(Facing p . 145j
POPULATION REGULATION IN A GHANAIAN BUTTERFLY
145
Department of Botany, University of Ghana, for identifying the plants; and to
my wife Janet for critically reading the manuscript. Professor D. W. Ewer and
the staff of the Zoology Department, University of Ghana, assisted with the
field work, rearing and discussion. The work was prepared for publication
during the tenure of a Senior Resettlement Fellowship of the Inter-University
Council at the Department of Biological Sciences, Exeter University, and I am
grateful to Professors D. Nichols and J . Webster for providing laboratory
facilities.
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EXPLANATION O F PLATE
PLATE 1
A. Green morph (on the left) and typical final instar caterpillars of Danaus chrysippus o n leaves
of Leptadenia hastata.
B. Two. typical final instar caterpillars of Danaus chrysippus on Calotropis procera of which the
one on the left is parasitized b y Apanteles chrysippi, the one on the right is not parasitized.