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. ' x ; ^ .v ,v r ': v
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m
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"15 "
Porcentege OBoaoole «cld
is*
Figure 3.12, Reletionehlp of 10HDA, 10HDAA and 2mheptamm# tc 0 # in
head axbraeta of queenleea A.w.adanaonll woarkere (quuanliai period
ted aontha)
■v-a;
1
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- a i',.
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aV-a
a a a /y ss :
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Flgum 3.13, m*latlon.hlp between BAA mnd eight eth er
In heed extraote of queenlBsa i»g*^aQ22Sto wrkers
/^ivlF
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Teble 3,15, Relationship between proportions of DAA,. lOHOAA^ S0H0A and
8=heptanona in head extracts of groups of queenless
A.m.adansonil workers and the degree of ovarlal development
Determined from Appendix Table 8
»j*
m ?'
Percentage chemical in secretion
-Ovarial _
development
DAA
1QHDAA
01
1
2
3
4
14.1
13.7
7.8
10.0
8.8
11.0
13.1
17.1
16.6
18.8
10HDA
B-heptanon#
36.4
44.8
87,3
61.9
80.9
34,1
*1.8
9 8
3.7
0.9
i s
Table 3,16. Relationship of lOIOAA, 10HDA and B-heptenon# to DM in
head extracts of groups of A.m.atiansonli workers rogarsk
le ss of ovarial development (November 1999). Determinad
f r • Appendix Table 5
'
»
i
Percentage DAA
in secretion
4•
i
-
Percentage otherchemical
10HDAA
19.4
18.6
16.7
11.1
6.6
'
i
WOA
70,2
63,4
Oj
81,6
9.4
40,3
24.2
*&*
44,6
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their M cretions were mere queenlike. Instead a ll three were found1to be
subordinate to others In th e ir group (th e ir average social Indew being
only 0»*B) end eoeewhmt inactive socially (averaging only twenty nine
IntOraetiohe during th e study period compared with an average o f f if ty
one interactions per bee among other individuals of sim ilar age),(Appendix
Table 7).
It was also thought, at the onset o f th is studyt th a t dominant
individuals would probably be more active so cially , end there wee
evidence to Indicate that this may be so. In seven of nine groups (the
data of group 2 was excluded as a ll the bees of th is group died by the
seventh day) the most active Individual had the highest or second
highest social Index, Howeve.
as occasions, dominant individuals
were the le a st active (Grout- r»,
-ml 9 ), and1in Group 1 the most active
Individual was the lea st domino,,* member, This worker was one of the
three Individuals found to be secreting 9KDA (Appendix Table 7).
lu m b e r ,o v a r lo lo s In the ovaries of A.m. wdnnsomii workers end cvsrlaf.
..development during queenlessness
■During the study, numbers of ovarioles In the ovaries of four samples of
i * edsnsonil workers were counted and cm,,pared (Table 3.19). Four
hundred end nineteen ovaries were assessed end the average number of
Cvsriolea per ovary was found to be 3,69. A highly sig n ificant difference
in the number of ovarioles per ovary was found between the bees sampled
in November 1979 <mandibular gland anal yule on pegs M) and the ether
groups, two of which were sampled in February 1979 (mandibular gland
analysis o f both not done) and the third in February 1980 (analysis on
page 115)» While two o f the February samples were sig n ificantly
different, neither was sig n ifican tly different from the th ird sample
(Table 3.20). The mean number of ovarioles found in the ovaries of
the February samples were 4.01, 4.36 amd 4.86, while the workers ex­
amined in November had only 2*80 ovarioles per ovary* The ovaries of
th is group were reduced to such e degree that in eleven instances
ovarioles were present only as minute filaments (none having developed
germerle) a situation found in only one bee dissected in February*
In addition, only one ovary dissected In the November sample had M ts
than seven ovarioles, while seventeen dissected in the February s®ropl«t
had more than seven, the largest of which consisted o f twelve overiclce. .
Of the bees dissected, 58 per cent were found to have ovaries with
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Tatola 3,20# Comparlsona between the number of overiol## per ovary In
fo u rc o lo n ia a o f A.m, adanaonli workara
Comparlaon
Nov.
Nov.
m ,.
Nov.
Fab.
Fab.
Fab.
1979 v Fab. 1979a
1979 v Fab. 1979b
1979 v Fab. 1900
1979 v Fab. meon
1979a v Fab. 1979b
1979a v Fab, 1980
1979b v Fab. 1980
D.F.
289
231
293
*17
122
184
126
# .g * *
*.#***
3 .8 8 "
7.74
0,B4N.S.
2.76
__________ 1.17N.5.
(underlined means not significantly different)
5 * 5
® Using central limit theorem x/n « aVn therefore u »
V hs
Fl»
an equal number of overiolea* or a difference of only one. In oontraett
1 5
p®$> cent were found to have a difference of four or more* the largest
difference being seven (Table 3.21). Differences in the number of ovariolea
between l e f t and right side ovaries were not found to be significant .
liable 3.22). Relationships between the number of ovariolea end ovarial
development were investigated in thy November 1979 sample only (Table 3.23)
It was found that ovaries with n ■ ■»*lopment had significantly fewer
overiolee then did ovaries that
developed. In addition, ovaries th a t
had developed to degree 'I* had significantly fewer ovariolea than
degrees '3 ' and '4 '. Although differences between degrees *2', *3' and
141
were s ta tis tic a lly in sig n ifica n t, i t appears th at there i s a trend
for ovarial development to occur more readily, or more ta lly , in ovaries
with greater numbers of ovarioles (Figure 3.14 end fable 3,24).
It was also found th a t the le f t and right aide ovaries did not
necessarily undergo equal development $ although equal development had
.occurred in 51 per cent of the bees dissected. Thirty five per ceht had
ovaries whose development differed by one degree of development, 7 per
cent by two degrees, 6 per cent by three degrees mod one Individual was
found to have one en tirely inactive ovary end the other with ta lly
developed eggs While differences in development between the ovaries of
in Individual did occur, development did not occur more frequently m
one side than the other*
The bees dissected in th is sample had been queenleaa for a period
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Figure 3.14, Ptelatloryhip between the number of overlelee end ev«H»l
development in queenleae A.m.edaneenll workere
a %
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... " S " V . ; y - - :
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T«fel« 3,24, Blffereneee in the number of ovarlolee of etariea with
d if fe r* * degree# of overl#! development
Comparison
D.F.
•* * * '
»a* V *1’
73
87
101
50
84
98
47
112
61
79
2,67**
4 82**
6.23**
3.7***
1,84N.S.
2,97**
2 55*
1.10N,8.
1.06N.S.
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3
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2
.... 1.140
4
3.36*
(underlined meene not eignificently different it 5 per cent
■level)
® Comperieons calculated os for table 3,20.®
of at least two months and the distribution of ovarial development wee
therefore interesting when compared with that found in nawly jpeenltaa
be-ee, In the former only 16 per cent of ovaries were found to be in*
active and only 6 per cent hod fully-developed eggs* the majority
were found to have intermediate stages of development - 1& P#* W # '■
wart cla ssified *1', 30 per cent *2* end 32 per cent
©f in te re s t, too, were sequential changes in the d istrib u tio n o f
developed ovaries th at took place among the population o f newly
l e e s worker# during the fir st month (mandibular gland an ilyois page. S i)
(Table 3*25). Within three days 38 per cent of workers hod v isib ly .
sotive ovaries although none had reached stage 12*» After nearly
three weeks almost 60 per cent o f bees dissected s t i l l showed he
indication o f ovmrial a c tiv ity . The percentage o f inactive evade#
eventually diminished; a fte r six weeks only # per cent resadnsd
Inactive, while in the November sample after approximately two SdnthS
without a queen only 18 per cent were undeveloped*
Five days after queen lo ss, 1 per cent of the ovaries examined
were found to have reached stage *2', end only two days la te r , 30 psf
cent of the ovaries assessed were found to be moderately or well
developed, 3! per cent of which were found to have fullydevslaped
The percentage of bees with moderately to well-devslspsd ovaries
res® to about 40 per cent a fte r eix weeks end to almost # per o p t :
v.:.: ■:
‘M W
i& vii
a fte r twe month#. The number of bees whose ovaries were fully developed
reeched the highest level of six per oont a fte r two months of «pe«nleee®
meee. The differences in overiel a c tiv ity evident among d ifferen t age
groups ere important, not so much at the time they were sampled but
rather a t the time the queen- was removed (Table %26), The greatest
amount of overiel activity occurred in the ovaries of bees th at were
lees then three weeks old when the queen was lo st. After only three
days, 50 per cent of the ovaries of these Individuals had begun to
develop, the greatest a c tiv ity being found among ten day olds. Overiel
development in bees that were older than, three weeks at dequsonire­
appeared to be retarded in th a t, although some development did
eventually occur, the fir st active ovaries were found a fte r one week
end none was found to have developed beyond stage '2 ', fu rth er, overiel
a c tiv ity in bees th at ©closed a fte r loss of the queen also- appeared to
be s lig h tly retarded. The only five day olds found to have seme degree
o f development were individuals that ©closed two days a fte r deqweening,
Those that ©Hosed later were about ten days old before their ©varies
became active.
the -only workers, seven in a ll, that were found to have fully®'
developed eggs in their ovaries were individuals that had ecloeed befo*e
the queen was removed but were less than three weeks old a t the time.
This figure represents a very low percentage as nearly three hundred
bets were dissected.
laying behaviour appeared to be associated with overiel dsvelopbent
as might be expected, however the a c tiv ity was not lim ited to individuate
with mature eggs. Laying behaviour is here described ee the eetlOh o f
in sertin g the abdomen into c e lls , and the deposition o f eggs 1# m i
necessary, Of eight individuals captured while they were inserting
th e ir abdomens into c e lls , two had.mature eggs, the others having
only moderately to well-developed ovaries (Table 5.27), Six additional
workers were seen to be showing, laying behaviour, but these escaped
capture. These individuals were also under three weeks old at dsqweenihg
Other workers found with mature eggr that were captured during routine
sampling were not showing laying behaviour at the time, however i t i s
possible th a t these individuals could have attained th is behaviour.
The only bees that were sampled individually end found to bp
secreting 9K0A ware both less than five days old when the quean wee
removed from the colony, however neither had mature sgge although
th e ir ovaries were m il developed.
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leb is )*27. Ovarial davalopment of quaanleaa j&,a, adanaW i workers
ahawing laying behaviour (Age in 4ey»)
|S
l!
7
#
#
13
f
10
10
16
12
23
23
20
20
32
Age at
dequeening
Period
queenlese
1
1
1
1
2
3
3
4
5
16
16
16
17
19
?
7
0
13
?
7
1
12
7
77
?
12
11
13
Ovarial
development
2/5
V3
3/2
5/2
as
■
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3/2
2/2
6/6
Ktonoonii worker contact with the amoen
Obsasvationo relating to worker contact with the queen were raids
Airing preparation for the age-related mandibular gland analyaia e f
newly queanleee bees (page 51)« Courts of worker bees were observed
over a period of sixteen days, with a total observation tiras of about
twelve hours* As bees observed attendi-ng the fuaen were net reeeved#
observations of particular individuals could n o t be regarded as
independent and
differencea oould not be tested s ta tis tic a lly . In
addition, when these observations were made, not a l l the workers e f
the colony were marked, and as a resu lt, a number o f unmarked Individual#
were eeen attending th e queen*
Indication# were that the court a c tiv itie s of feeding and licking
the guesn'wers performed by two distinct age groups of attendant *#*#**,,
although there was a considerable overlap (figure 1*15 and Table
Those individuals responsible for licking the abdomen e f the gusse weee
predominantly older than two weeks, 41*2 per cent 'being unmarked* It
i s sig n ifican t that none younger then six days wee seen to lic k the
gusen. In contrast $ workers responsible for feeding the gueen were
predominantly younger than two weeks, only 7.5 per cent were lawifflrilpd
while 38.® per cent were less then a week old,
The queen was approximately two months old wiien these stowrvatiiiw
,
'
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M
Bros Mcklng
.'A'airftYiKLi*.
mh--'
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a
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..
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Table 3,28, Agee of workers feeding end licklr^j the dueen
;1
Feeding
Age
(day*)
Licking
Count
Percentage
tount
Percentage
■ f ” ' I' •■
1
2
3
4
r
1
3
6
4
8
9
10
11
12
13
14
3
18
18
19
4
Unmarked
■jafflicaMB
Total
•
■
3
5
6
7
18
19
20
21
fl)
/ A
2.7
38.8
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3
38.8
4
7
3
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1
28.4
1
4
2
3
2
3
1
3
4
3
4
3
2
4
3
3
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Ttw relevant questions to th is discussion are those addressing the
relationship between chemical signals, easts differentiation and female
in te rc ss ts social in teractio n s. In attempting to elucidate these laawea
the study has provided i n i t i a l data on the mandibular gland secretions
of A # adanaonil queens and workers in th e ir natural habitat* The
investigation has revealed a number of in terestin g d if f -anoee th a t
ex ist between A.m, edbnsonii and certain other honeybee races including
the South African Cape bee, A.m. cspensis, and the European bees,
A.m. " s llif e r a and A.m. l igusU ca.
Under normal queenright conditions the A. melllfera queens influence
the physiology end behaviour of workers largely by the accretion Of * * *
from the mandibular gland. This influence not only in h ib its ovary
development in workers and provents the secretion of 9KDA by th e ir
mandibular glands, but prohobly also regulates normal worker behaviour
to a large degree (Reviewed by Cary, 1974; also see Table 1.2). This
has become more apparent th r o u g h recent studies of laying workers th a t
arise during queenless periods. During these periods the influences of
the queen are removed, and in A.m. melllfera and wore so in AsS® SESSS
a number of workers undergo extensive ovary development to the point
th at some have mature eggs in th e ir ovariolea (Perepelove, 1929; Valthuia,
1970b), Simultaneously these Individuals cease most normal worker
a c tiv itie s end become en tire ly involved In laying eggs Not only do
these bees change in both their behaviour and their physiology but in
addition, their Interactions with other workers are affected to a point
where they may begin to attract a sizeable court of attendant workers in
the same manner as a queen does. These changes in social position are
thought to be caused by changes in the mandibular gland signal, a#
amounts of 9KDA are secreted by laying, workers of at least A«m» ,os|>Bfi,t ,g.
(Valthuia, 1976; Ruttner, et e l, 1976),
Social position among colony members of most socially advanced wasp
end bee species (other than spine bees) is established by physical
harassment of weaker individuals by stronger ones Which resu lts in a
diatinct dominance hierarchy$ the most dominant individuals aaouttlng
tbs egg-laying role and the subordinates the worker role (Satrm, 1966;
Cumber, 1949; Free, 19»*M iehener, 1974; Mlchener end Brothers, 1974;
-Plowlglit smd Jsy, 1977; Spredbsry, 197); Wilson, 1971). In Ami# .
m ellifere the only display of overt aggression among colony member#
occurs during the in itia l periods of cjueenlessneee* Fighting is savors
among quesnloss A.m. caoensla workers and hundreds of bees may be k ille d
within a few days, The fighting eventually abates, possibly owing to the
establishment of laying workers which may have assumed a dominant position
by secreting dominant social signals from the mandibular glands (Anderson*
196) end 1968).
'Morphological d ifferen tiatio n between the queen end worker castes
of Aois species end A. m ellifera races la advanced and in tercastes are
almost unknown in natural situation* (Eckert, 19)4), although they can be
produced a r tific ia lly (Taber and Poole, 197)). Behavioural, physiological
andanatomical d iffe re n tia tio n , on the other hand, la more variable.
While these variations may indicate that caste d iffe re n tia tio n within
the species end races is merely o f a d ifferen t nature, there is also the
possibility that i t has evolved to varying degrees. This study he®
revealed a number of Interesting qualities regarding the behavioural,
physiological and anatomical differentiation of the female castes o f
l«fl» .adansonil which may suggest that caste d ifferen tiatio n and social
Interaction between queens and workers i s markedly d ifferen t from th at
Found in other A. mellifers races
In A.m, adansonilt the degree of caste d iffe re n tia tio n , Which i s
for a ll races controlled by .nurse workers in the diet fed to developing
larvae and which is also almost certain ly influenced by the dominant
attributes of the queen, is clearly evident in the anatomy of the
reproductive system of workers. The mean number of ovarioles per ovary
sampled from four populations varied from 2.88 to 4.86 and is consistent
with the results of Chsud-Netto and Bueno (1979) although in th e ir study
the range was sligh tly smaller, being one to eleven instead of aero to
twelve. With regard to the anatomy of the reproductive system, then*
l* f . id iMonli workers are similar to A.m, jjpllifar# in th a t both races
have distinctly fewer ovarioles per ovary then any other honeybee yet
examined (see Table 4.1).
Vslthuis (1976) has suggested that differences between the number of
ovarioles in the ovaries of queens and workers is Indicative of the
degree of difference between the two castas. In th is regard, It may be
eenelctered an Indicator of the degree of caste differentiation. The
immature female a t one atage of development hae about seventy overiole#*
and i t ia only d iffe re n tia l feeding that causes the number to diminish
in one ornate and Increase in the other (da Wilde* 1976), As
,*dw*w, a:* known to have the larg est ovaries* th is suggests th a t o a sts
differentiation la most advanced in A.m. mdanemil and A.g. ffy|.|lfajg»
Itble 4.1.
.■
The number of ovariolea in the ovaries of W o worker#
Specie#
No. worker ovariolea
M® S is s ia
Api# CindtcaJscerana
20
M S,
M i
Aim.
A **
A.m,
4
19
5
)
)
floree
mellifera cagenals
liowetice
"Rlllfpre
Sdanepnii
1
1-30
1-9
9-)9
1-24
1-19
0-12
The physiological ab ility of worker# to develop th e ir ovaries during
queenlesa period# can also be regarded a# indicative of the degree of
differentiation between the female ornate#.
(indice)*oermn§; A. |jgSg,|lf.l
and ^.m. caoenala workers undergo rapid ovarial 'development and within
a few weeks, certain individual# begin laying eggs (Velthuia, 1976).
Development among queenlesa j&.m. mell.lfera and A.m.
wcfhsrs 1*
rela tiv ely alow and th is study has shown that in the le tte r race,
functional laying workers do not appear during the f ir s t #i% week# of
queenl###neaa> The significance of these differences in the ab ility to
undergo ovarial development ia associated with behavioural differentiation
and should be viewed in that ligh t.
The mandibular gland secretion of queens has for a long time been known
to evoke retinue behaviour, suppress ovarial development in workers, end
influence a number of other important biological functions (see Table 1.2),
Apia dorsate* &, (iQdicsJ.cerenB end&.m. capsGgl# functional laying
workers have been termed false queen# ee they have been found to evoke
marked retinue behaviour end' exhibit queen*like 'behaviour, even to the
extent of euppresalng ovarial development in other worker#. (Sakmgemi,
I f 58, Velthule, 1976), I t is now known th at in A,m. capensle, these
l-nrfividuals undergo' substantial changes in th e ir mandibular gland aignala
and begin to secrete •ig n lfic w t amounts of 9KDA (CrfMa.and Vel&hwia,
IftUf Ruttner
a l , 1976). Recently, i t has been found that the functional
laying workers of A«m, well i for a also secrete appreciable amounts of 9KM,
aopporting observations that these Individuals are capable of evoking
retinue behaviour and in h ibiting ovarial development n others, although
to a lesser degree than the false queens of &.£. capenwle (Crewe and
Velthwis, 1980; Vclthuis et a l, 1965).
In contrast, A.m. adansonii laying workers have never Wen observed
to evoke retinue behaviour, and this study has shown that very few
individuals are capable of secreting 9KDA, As was predicted by Velthule
(1976) for A.m. m elllfera, many A.m. adansonii workers experienced acme
degree of ovarial a c tiv ity . The number of 1indifferent1 bees (a term
Velthule used to describe individuals whose ovaries remain in a ctiv e),
$■malned at between 50 e id 60 per cent during the first five weeks of
qoeenleasness, while in a separate investigation they were found to
number only 16 per cent after two montho without a queen. Very few bees
fleas than 3 per cent of those that hod been queenleoa le ss than six
weeks, and only 6 per cent of those quccnlesa for at least two months)
were found to have mature eggs in their ovaries. While i t is necessary
to take in to account environmental influences (that i s , influences of
season, quantities of available food, numbers of nurse bees and condition
of the qqeen) the substantial difference in ovarial development between
these two quoanleos groups is probably due largely to the length of time
the bees had been without s queen. With time, more and more bees were
able to 'develop their ovaries, the great majority to stages ’2* and *3®,
in important difference between A.m. adansonii and other races in which
laying workers begin to suppress ovarial development in time.
'During the investigation of newiy-quesnleee bees, only fourteen were
■observed inserting their abdomen into c e lls although none laid eggs
(Table 3*23). Of these, eight were captured and what i s significant i s
that only two had mature eggs and neither was secreting 9KDA, Only one
individual was found to be secreting 9KDA and th is bee merely had welldeveloped ovaries (degree '3') but did not have mature eggs. The remaining
five had neither mature eggs in th eir ovaries nor 9XDA in th e ir mandibular
gland secretion. Ovarial a c tiv ity , glandular a c tiv ity and queenlike
behaviour must however be loosely a llie d , since the secretion of 9K&A
'
y: 4
• i
if f - :
■
/
-/'*n
■ J.-f
End agg-lsyrtg behaviour were always associated with at least welldeveloped ovaries Cdegree *1’)*
.iegaiding social interaction, easts differentiation and the
;* r - name o f the queen j one of the moat lopdrtant aspects o f
;
M '***11 biology . o emerge clearly ia th a t worker# appear to be
Inoapable of secreting sufficient quantities of 9KDA, this -despite the
fbot th a t the two individuals found to have 9KDA in their samdibular
glands war# secreting lergefr amounts of the chemical than were A.g,
caoanaia and A.m, m elllfers laying workers (Crewe and Vslthuia,
IMO). None of the bees observed attracted courts of any size and
overt aggression was lim ited to mild harassment such as wing and lag
holding and occasional attempts to sting* The only indications th at
easts influence may have been exerted by either specific individuals
or by the queenless colony as a whole, was the fact that bees emerging
a fte r the colony had lost the queen appeared to be retarded in th e ir
a b ility to develop th e ir ovaries.
The most active workers were those that had emerged at the time
the queen was lost but which were then younger than three weeks* All
individuals found to have mature eggs, oe well as a ll those th a t showed
laying behaviour were from this group. In addition, the two indi­
viduals found to be secreting 9K0A were le ss than a week old when the
colony became queenless.
Bees older than three weeks at the time the queen was removed
were also retarded in their a b ility to undergo cvarlal development.
Whereas up to 85 per cent of ten day olds had experienced enme develop­
ment within three days, three week old bees took up to a week before
their ovaries became active.
It appears that two separate factors are responsible for these
differences between the different age groups of workers, namely the
influences of the queen prior to her loss and the influences of
queenless workers following; her lo ss, the former being considerably
more powerful, figure 3.15 Indicated that very young bets are
primarily responsible for feeding the queen and that i t is the older
that lick the queen, With regard to the hypothesis of the
;:er (19Mb),
transport by
proposed by
namely th at workers lick the substance o ff queans and transmit i t
to other colony members tro p h o llaeticelly , these observations of
an age-related difference in retinue behaviour by worker baa# #f#
provocative. The observations suggest that the exposure of vary young
i -
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fM k
■ „ 7 ;.y.V , V v .::;.
m
mm
ttlh
...
=: ; i l
S
: S |3
;ry -;
x iil
:« lf
M
■m*
"/*X.XX
' 'V-
V '-
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|l —•1
...........
............
i
#0
l . :
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I':::
and tgg-liyng behaviour were always aaeocialed with at least welldeveloped ovaries Cdegree ' 3‘),
leprdiing social interaction* caste differentiation and the
dmeinanoe of th e queen, one of the most ieportent ****** *f A$*
*d*n*onii biology to emerge clearly is that workers appear to be
incapable of eerreting eu fficien t quantities of 9KDA« this despite the
fact that the two individuals found to have 9KDA in- their mandibular
glands were secreting larger amounts of the chemical than were A,m,
caoansis and A.m. m ellifere laying workers (Crewe and Velthwia,
I960)* None of the bees observed attracted courts of any size and
avert aggression was lim ited to mild harassment such as wing and lag
balding and occasional attempts to sting* The only Indications th at
some influence may have been exerted by either sp ecific individuals
a r by the queenless colony as a whole, was the fact that bees emerging
a fte r the colony had lost the queen appeared to be retarded in their
a b ility to develop th eir ovaries.
The meet active workers were those that had emerged at the time
.the queen was lo st but which were then younger than three weeks. All
individuals .mind to have mature eggs, ae well as a ll those th at showed
laying behaviour were from th is group. In addition, the two indi­
viduals found to be secreting 9K0A were less than a week old When the
colony became queenless*
Bees older than three weeks a t the time the queen was removed
were also retarded in their ab ility to undergo ovarial development.
Whereas up to 85 .per cent o f ten- day elds had experienced some develop­
ment within three days, three week old bees took up to a week before
their ovaries became active.
It appears th a t two separate factors are responsible for these
differences between the d ifferen t age groups of workers, namely the
influences of the queen prior to her loss and the influences of
queenless workers following her lose, the former being considerably
more -powerful* Figure 3,15 Indicated that very young beta are
primarily responsible for feeding the queen and th at It is the older
ones that lick the queen* With regard to the hypothesis of the
mechanism of 9KDA transport by workers proposed by Butler (1954b),
namely that workers link the substance o ff queens and transmit I t
to other colony members tro p h cllactically , these observations i f
an age-related difference in retinue behaviour by worker bees are
provocative. The observations suggest that the exposure of vary young ;
...v
1: S
'" ''4
I
%
.. . . . .
# # 5
emss
i8,-f
. .1 ^ ,. .
,
.
*,»
I - - I I * # * ,j#
q»
.
....
“IM
M
ii#®a to 9KDA ie adnlmai, being lim ited to entemel contict with the queen
and to trophellaxla, while older individuale ere subject to greater
tiounte owing to their licking the queen-« IT th is is true* and the
effect# o f 9K0A ere eoowuletive* end provided th a t the chemloel 1#
eyeteekic reth er than olfactory in i t s action, (then the influqnoe# of
9MM upon the physiology end behaviour of workers are lik ely to bo more
raverslbly in young beaa than they are in older individuals; ®nd therefore afte r loss of the queen, i t would be the younger beaa th at would rapidly undergo physiological and behavioural change, while their
older neatmates would require a longer period before the Influences
of the queen1a signals dicripate* However, recently Seeley (19795 wee
unable to extract more than one nanogram of 9KDA from bees that le ft
the retinue, thereby seriously questioning the reasoning of th is
argument, He found that the dispersion of 9KDA was largely carried out
by 1messenger* bees leaving the retinue and dispersing the queen-right
-message through olfaction, supporting the surface transport hypothesis
of Vcrheijsrt-Voogd (1959)* The differences regarding the a b ility of
workers of various ages to develop their ovaries at the onaet. of qussnlesaneas is more lik ely , then, to bo a simple consequence of aging
and have no connection with exposure to 9KDA at all*
Wbrkera that emerge in queenless colonies, emerge Into a
situ atio n in which the Influence of the queen has been replaced by
the influence of queenless workers*
Among queenless A,m, Bciansonil colonies th is influence may be duo
to the combined amount of 9K0A secreted by -a number of individuals.
In the newly queenless colony investigated in th is study, a to ta l
amount of 378,3 micrograms of 9KDA was detected from twelve samples.
While this amount compares favourably with the amounts socrstsd by
individual queens, i t did no more than retard ovarial development
in newly-emerged bees, It la clear that despite the level of fKDft
being as high as that of a normal queenright colony, additional factors
th at allow recognition of the queen have possibly not boon simulated
lh the queenless situation in A,m, adensmil. It ie possibls that the
high level of 9KDA is not sustained, However an altern ative #*pla**tion
la that as 9KDA-secretlng IndivlduelB are not apparently recognised am
such by other workera, d istrib u tio n of the cnmpourtd is not adOquete
enough to induce a queenright situation, although I t Is sufficient
to retard ovarial development in beea that subsequently eelese into
the queenless situ atio n .
The study revealed that the majority of workers do net experience
marked changes in th e ir mandibular gland secretion despite undergoing
eoneidarable ovarial development.
It is not unreasonable to suggest
th a t ornate d iffe re n tia tio n in a hypothetical Aoia race oewld be ooaplat*
anevgih to prevent workers from changing the secretion of the 'MndttNdar
gland* Just as morphological and anatomical attributes are narrowly
determined, so i t ia possible to argue th a t physiological end behavioural
a ttrib u te s may also be canalised.
The degree to which these features are
capable of change would indicate the level of caste d ifferen tiatio n
experienced by Individuals during their development.
A.m. adaneonii workers, on the whole, do not experience marked
Changes In the mandibular gland secretion during queenless periods, however
changes that do occur appear to be toward a queenlike secretion.
No trace
of 9KDA was found In over 99 per cent of queenless bees analysed, and
substantial amounts were found In -only two individuals.
The mandibular
gland secretions of these workers were almost identical to those o f queens
except th at the quantities of most components were greatly reduced.
The
fact th at they failed to e lic it court behaviour among surrounding
neetmates suggests that their signals, though qualitatively sim ilar to
queen signals$ were quantitatively Inadequate.
The displays of overt aggression that occur in queenless colonise of
£ .» . m ollifere ere not between laying workers but instead the laying
workers are attacked by aggressive nestmatee with moderately developed
ovaries (Velthuis, 1976).
The layers appear to be submissive toward th e ir
aggressors ond never attempt to defend themselves but only attem pt.to
e#oapo.
Velthuis equates these aggressive reactions with behavioural
dominance and raises the question of laying workers being reprodueilwly.
dominant yet behaviourally submissive.
An altern ativ e explanation could
be th a t these laying workers are behaving in a manner sim ilar to strange$
introduced queens who offer no resistance when confronted by aggressive
workers and may even be killed i f unable to escape*
Stebo (1974a) found
th a t i f strange qqeens were either less attractive or more a ttra c tiv e to
workers then was their own queen * workers behaved aggressively toward*
them. Howeverj -queens that had sim ilar degrees of attra ctio n were accepted
without any aggressive reactions.
In A.m. m elllfera, laying worker#
possibly secrete queenlike signals in sufficient strength to be -regarded
i s strange queens thereby e licitin g aggressive tendencies in naeWatma,
and th e ir in a b ility to reciprocate aggressively may be due to -peenlike
behaviour.
Rather than being regarded as submissive, than, they should
be regarded as behaviourelly different*
The lack of overt aggression in queenlass A,». edensqndl colonies»
la the lig h t of the above argument, may be due to the fact th at laying
*##**# are incapable of secreting queenlike signal# in su fficien t
abqwhte t» reach a level necessary to evoke aggressive reactions in
tweHietea. H ills i t la possible that the level is higher for
t o . f S M BU.
f " M . M l i M l . « . avidene*
^
»
la mere lik ely that A.m. adenaonij workers have s very lim ited a b ility
o f secreting 9KDA despite being able to develop th eir ovaries.
In other
words, &.&. adsnsonii laying workers ere incapable of functioning as felae
queens.
The object of making colonies queenlass i s in fact simply to Induce
a single caste situ atio n in which a pseudo caste d ifferen tiatio n can
develop based purely upon physiological end behavioural changes among equal
noatastes,
I t follows that the queen suppresses these expressions in
quesnrlght situ atio n s and that the degree to whUh these expressions are
present in the worker caste depends upon the degree tr *toich the caste has
d iffe re n tia ted .
The more complete this differentiation i s , the more
queenlike and the more workerlike the two female castes are and the more
unlikely i t la that pseudo differentiation w ill occur in the absence o f
the influences of the queen.
the workers ere brought back in an antique
laaa
r i n ^ l s ^ t u % J d % n d s on^whet
remains of th e ir antique equipment, thus pointing to the
o rig in from which both queen end worker are derived *
VOlthuie, 1976.
the antique equipment referred to in this quotation must include all
the a ttrib u te s , both morphological, anatomical, physiological and
behavioural, which normal ancestral females would possess* following
caste d iffe re n tia tio n moat of the a ttrib u te s regarding dominance end
reproduction are irrev ersib ly lo st from the worker caste, end those th a t
remain are suppressed by the communication of dominant signals by the
queen individual.
From the evidence provided In this study, and in the
ligh t of the above argument, i t would appear that caste differentiation
in &.&. edaneonll is ot a level high enough to render the worker ornate
unable to secrete dominant mandibular gland signals, despite certain
individuals being able to a lte r th e ir signals to some extent*
The suppressive ab ility of the queen is almost certainly associated
with her mandibular gland signal. The average secretion of mated A, m.
ffidanaonll queens was found to have very significant differences In the
amounts and proportions of certain components compared to that of A* m,
m alllfera queen# (Callow e& o l, 1964). The average amount of 9KDA was
250.5 mierogroma (Table 5*1) compared with their two hundred micrograma.
The level of 9HOA wee lower, averaging only 80.9 micrograma (T#bl# 3*1)
oomparad with one hundred and fourteen mi(*ogrmme in &. &.
queena, Donaequently these important queen pheromonss were found in a
wary d lffe rtn t ra tio in A. m. adensonil queens. While the 9KDA : 9H0A
ra tio in A. m. w elllfare queens was nearly 10*6 (Simpson, 1979), in the
queena of A, m. ndam-onil the ratio whs only 10*3. 'Recently Crewe and
Velthiue (1980) found that in five mated, laying A. m, m ell^fsa <F®sn8
the 9KDA t 9H0A ratio was nearly 10*9. The queens produced on average
71,2 microgreRm of 9KDA and 63.5 micrograms of 9H0A, the chemical#
constituting 36.1 per cent and 32.2 per cent of the acid secretion
respectively.
Of additional interest were the lev els nf DAA, a compound that la
not known to have specific biological a c tiv ity . While the amounts of
DAA are reasonably high in A. m, melllfera queens (twenty five micrograms per head)(Simpson,1979), the amounts were extremely low in the
queens of A. m, edansonli, averaging only 2,4 micrograms (Table 3 .1 ),
Consequently the 9KDA i DAA ration were very d iffe re n t, being 111 In the
former race and 100*1 in the letter. In contradiction, Crewe find Valthuia
(1980) found no trace uf DAA in A. m. m elliferi queena during their
recent study. The level of DAA in A. m. m elliferi workers has not
Induced comment in the lite ra tu re , end i t can only be concluded than
that the compound is probably not found in appreciable quantities In
these individuals. In contrast, DAA was usually found to be a major
component of the mandibular gland secretion of older A. m, adantonll..
workers. While the levels of DAA in A. m. melllfera queens end workers
appear to arouse l i t t l e in terest, the levels found in the female c te lie
o f A.m. adansonll do. In younger workers DAA was founu to be om eletently less than 5 per cent of the secretion, but after the fir st week
of * lfs bees began to Increase their secretion of DAA until the compound
regularly comprised over 25 per cent of the secretion, end in one bee
surpassed 50 per cent (Appendix Table f ) . The biological function o f '
DAA, i f any, 1* unknown, however in quaanleea bets the amount o f DAA
decreased considerably with ovoriol development, and in individuela
vdth well developed overtee wee absent» suggesting that the compound may
in some way be a consequence of worker suppression in A.m. adansonii.
Levels of 2 -heptanone, an alarm pheromone secreted by the mandibular
glande o f works* honeybee# (Mssohwltx, 1964) were also found to doermama
mubetantially with ovarial development. In the only group of gweenlaaa
Seoa analysed for 24wptanona* the average amount wee found to decfOtto
f*om 17.9 miorogrsm# per head in worker# with undeveloped ovaries to
0.4 micrograms per heed in workers whose ovaries contained mature # # #
(Figure ? . 1 0 , Table 3.15). The decreased level of 2-heptanone in queenless colonies may well Influence the b e h a v i o u r of ouch e group, end i t
la possible that this feature is a contributing factor to qusenlese beoe
often being noticeably le ss aggressive towards intruders than th e ir
quesnright counterparts (personal observation)
Velthuis (1976) concluded that for ’M 3 . th« capacity of the worker
to develop into a false queen is lim ited'. The degree to which workers
. *e capable of becoming false queens in various species end races of
Kola depends uoon the degree of caste differentiation, a process that
is almost certianly influenced by the mandibular gland signals of the
queen. This study has revealed that the queens of A.m. adansonii have a
markedly different mandibular gland signal from A.m. mellifgra queensf
mated, laying individuals secreting considerably greater amounts of
most of tho acids including 9K0A,9HDA and 10HDA, and having a markedly
different 9KDAt9HDA ratio than their european counterparts. In addition
i t has shown the amounts of iOliOA in queenright workers are reasonably
similar lo those found in European workers (Boch and Sheerer, 1967)
although the chemical appeared to be more prevalent in younger bees,
two to five day olds having an average of 43.1 microgreme, and els to
eighteen hour olds having 13.9 micrograms. It i s possible th at this
early secretion of 10HDA represented an accumulation of the chemical prior
to the onset of nursing behaviour, 10HDA being the mein lipoid component
of larval food ( B a r k e r dais 1959),as the chemical decreased noticeably In
seven to ton day olds. Although i t la te r increased to an average of
4 7 . 8
micrograms in fifteen day olds, i t subsequently declined to only
19.9 micrograms in four week old bees, The study has also shown that the
total absence of false queens in queenless groups of this race la hot
the result of an inability to develop Lite ovaries ( functional laying
workers are present in a ll queenless A.m. adansonii. colonies) blit
rather the result rf an in a b ility to a lte r adequately the mandibular
gland worker signal to a queenlike signal. While this is to, certain
■■
...............................
t
,.... r,;v>
r.
■'"'r-
«
96
significant changes in the biology of queenlese bees did occur, suggesting
s sh ift toward queenness. There was a substantial increase in longevity,
queenlese bees living at least twice as long a queenright individuals#
Numerous workers experienced ovarial development and e few began to ley
#ggs Workers with developed ovaries had decreased lev els of 9AA and
1 -heptsnone, both features of the mandibular gland secretion of the queen,
and e small percentage began to secrete 9K0A.
In itia lly , queenlese workers were also found to undergo a rapid and
substantial decrease in the secretion of 10HDA, levels dropping from an
average of 3 3 . 6 microgrnis in ten samples
just prior to dequeeningto
only 7 , 9 micrograms in thirty six samples
during the fir st two weeks of
queenlessness. The cause of th is drop is unknown and no reasonable
explanation is apparent as larvae wore not present in the colony. With
time workers began to secrete more 101OA and in bees that had been
queenless for ovet two months the average
secretion contained 32.1micro­
grams of 10HDA. Another interesting feature was the differences in the
secretion of 10HDAA and especially 10UDA in these workers, the levels of
these chemicals increasing significantly with ovarial development (Figure
3.11). The increase in the amount of 10HDA very closely followed a
decrease in 2-heptanono, which, in view of I 1 opinion of Simpson
(1960), may further suggest that 2 -heptanono is derived from the breakdown
of 10HDA.
Despite the in itia l changes toward queenlike signals in the
mandibular gland secretions of newly queenless bees, Including the
secretion of 9KDA, no workers evoked retinue- behaviour among nestmates
and ovarial development was not inhibited. In addition, overt aggressive
reactions in newly queenless colonies were minor and no individuals were
stung to death.
Although these data were compiled from observations of only a few
colonies, end generalisations must therefore be viewed cautiously,
together they indicate that the relationships between the queen and
worker castes in A.m. adansonii may possible be more ad* ancod then
in most races. They suggest that the process of caste differentiation
may bo so complete, morphologically, anatomically and physiologically
bp to exclude a l l workers >vom altering their behavioural position
su fficien tly to imitate the queen, explaining why 1 Folse1 queens heve
never been observed in queenless colonies despite the presence of
laying workers. It was hoped that data gathered from the small cage
study would provide evidence of the extent to which
m rinnaaniili
workora were capabla of dominating othor individuals 'during gusenlsss
periods, however the experiment was inconclusive due to an alimentary
ailment which interfered with normal behaviour and caused the premature
death of a 'number of individuals# At that stage, the ovaries of a ll bee®
had just, become active (although none had begun to deoompartmentall##)
and although three individuals were found to hove minute amounts o f
9KDA in their mandibular gland secretion, in general, secretion® were
not sig n ifican tly different in their composition.
Some of the most interesting features emerging from this study, then,
were the apparent secretion of mature mated queen signals by A.m.pdansonil
queens in which at least the 9KDA:9HDA$10HDA ratio is reasonable
homogenous $ the significance of the ago of workers at the time the
queen is lost on their ab ility to undergo changes toward a queenlike
disposition while queenlcss $ the discovery that these changes (the
secretion of queenlike mandibular gland sign als, ovarial development
and laying behaviour) ore not necessarily synchronous $ and la stly , the
unexpected prominence of DAA In the mandibular gland secretions of
older workers.
The study showed conclusively that the mandibular gland secretions
of virgin queens are very dissimilar from those of mated queens, especially
during the fir st two to three days of l i f e . Also the dissim ilarity between
the secretions of different virgins indicated that thoir mandibular glands
were probably in a transitory phaoe of activity* The sample size was,
however, too small to reveal the precise timing and sequence of these
changes.
The p ossib ility of there being n mature mated queen signal (in this
study the 9KDA:9HDAilOIDA ratio was approximately 10:4*2 and the three
components composed 80 per cent of the acid secretion) raised some
interesting questions. Is the signal age related, in other words, do
a ll queens achieve a mature signal at some stage? Is the signal related
to the season or to intrahival conditions? la It related to the
development period of the individual and to weight$ in other words are
some queens unublo to achieve a mature signal? And most importantly,
i f certain queens do not achieve the signal (as appears to ue the case
from this study) can thin in ability be related to factors in the colonies
they head} factors such as small colony size, poor brood patterns and
perhaps a poor foraging behaviour?
.p g w '" ''
..............
...... ..
The study very d efin itely showed th a t workers th at experience the
eo rt rapid end most complete changes in th e ir anatomy, physiology end
«
#
#
in the m an d ib u lar gland secretions of A.m. odaneonii workers.
=
-
s
=
e
=
=
:
a
T h is
.
.
k:-
function in A.m. adansgnH «
I t is hoped th at th is study w ill i n i t i a t e sdded in te re st in A.»«
questions ra ised
adanoonli and induce furtlwr research into some
during the discussion.
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Author Jackson M E
Name of thesis The effect of Social Interactions on the production of Mandibular Gland Signals in Female African
Honeybees (Apis Mellifera Adansonii L.) 1982
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