fecundity of ant queens in relation to their age and the mode of colony founding

Insectes Sociaux, Paris 1990, Volume 37, n ~ 2, pp. 116-130

�9 Masson, Paris, 1990

FECUNDITY OF ANT QUEENS IN RELATION TO THEIR AGE AND THE MODE OF COLONY FOUNDING

L. KELLER (1) and L. PASSERA (2)

(1) Musde Zoologique, Palais de Rumine, CP 448, 1000 Lausanne 17, Switzerland (2) Laboratoire d'Entomologie, Universitd Paul Sabatier, 118, route de Narbonne, F 31062

Toulouse Cedex, France, U.A. C.N.R.S. 303

Regu le 23 janvier 1989 Accept6 le 15 juin 1989

S U M M A R Y

The change over time in the fecundity and weight of queens was investigated in three monogynous, independent colony founding species, Lasius niger, Camponotus ligniperda and C. herculaneus, and two polygynous dependent colony founding species, Plagiolepis pygmaea and Iridomyrmex humilis. Queens of the three species founding independently exhibited a similar pa t tern with a significant loss of weight between mating and the emergence of the first workers. In contrast , weights of queens of the species employing dependent colony founding remained more stable. Fecundity of queens founding independently increased slowly with time whereas fecundity of queens founding dependently reached the maximum level some weeks after the beginning of the first reproductive season. These results are discussed in relation to some differences in the life history (e.g., life-span) between queens utilizing independent and dependent colony founding.

R E S U M E

Fdcondit6 des reines de fourmis en relation avec leur &ge et le mode de fondation de la soci6t6

On a 6tud6 dans ce travail les variations en fonction du temps de la f6condit6 et du poids des reines fondatrices de trois esp6ces monogynes h fondat ion ind6pendante (Lasius niger, Camponotus ligniperda, Camponotus herculeanus) et de deux esp6ces polygynes h fondat ion d6pendante (Plagiolepis pygmaea et Iridomyrmex humilis). Les reines fondatr ices des trois esp6ces ~ fondat ion ind6pendante mont ren t des similitudes avec une per te de poids significative entre le moment de l 'accouplement et celui de l '6mergence des premi6res ouvribres. A l 'inverse, le poids des jeunes reines h fondation d6pendante reste plus stable apr6s l 'accouplement. La f6condit6 des reines fondant de mani6re inddpendante augmente lentement avec le temps, alors que celle des reines fondant de fagon d6pendante atteint son niveau maximal quelques semaines seulement apr6s le d6but de la premi6re saison d'activit6. Ces r~sultats sont discut6s dans le cadre des diff6rences ph6nologiques (comme par exemple l 'esp6rance de vie) qui apparaissent entre les reines pra t iquant les deux types de fondation.

FECUNDITY OF ANT QUEENS 117

INTRODUCTION

A colony of social insects may have a single functional, i.e., egg-laying queen (monogyny) or more than one queen (polygyny) WILSON, 1974; HOLLDOBLER and WILSON, 1977). Monogynous species generally exhibit high intercolonial aggression. In contrast intercolonial aggression is generally lower in polygynous species (H/)LLDOBLER and WILSON, 1977; KELLER and PASSERA, 1989a).

Monogynous species generally employ independent colony founding i.e., after the nuptial flight, newly mated queens excavate a cell and rear the first brood in isolation without the help of workers. A few exceptions can be mentioned such as army ants which reproduce by colony fission (FRANKS and HOLLDOBLER, ~987). In contrast, many polygynous species can not found new colonies without the help of workers (dependent colony founding) (KELLER, unpublished). In those species, young queens remain within the mother nest after mating or they enter a foreign colony of the same species. Foundation of new colonies generally occurs by budding or fission; a process in which one or several queens move out of t he nest, accompanied by workers and establish a new colony.

A question of great interest is the adaptive value of polygyny vs. monogyny in the context of the evolution of sociality. Several authors have discussed the advantages of dependant and independent colony founding in relation to dispersal ability, probability, of successful colonization of a new habitat (H6LLDOBLER and WILSON, 1977 ; ROSENGREN and PAMILO, 1983 ; KELLER, 1988a) and relative investment of energy that each type of colony founding necessitates (KELLER and PASSERA, 1988). In the case of independent colony founding, it is well known that queens have low fecundity during the founding stage (see BRIAN, 1983). After the emergence of the first workers, fecundity of queens regulary increases with time. This can be explained first, by the fact that food input in the colony depends on the number of workers, and second by the fact that the number of workers limits th~ quantity of brood which can be raised in the colony. In contrast to species with independent colony founding, species with dependent colony founding have young queens which are accompanied by a high number of workers imme- diately after mating. This raises the question of whether these queens rapidly reach a high leveI of fecundity after mating or, by contrast, if the fecundity of queens increases as a function of their age. To investigate this question, which is important in assessing the adaptive benefits of independent vs. dependent colony founding, we compared the change in the fecundity of queens in relation to age in five species of ants, three exhibiting independent colony founding and two employing dependent colony founding.

118 L. K E L L E R a n d L. P A S S E R A

M A T E R I A L S A N D M E T H O D S

The fecundity of queens w a s investigated in three rnonogynous species, Lasius niger, Camponotus herculeanus, C. ligniperda (independent colony founding), and two poly-

gynous species, Plagiolepis pygmaea and Iridomyrmex humilis (dependent colony founding) for the two f irs t years of their life.

Monogynous species : L. niger is a monogynous species employing independent colony founding. Colony founding may occur either by haplometrosis (queens s tar t a new colony alone) or by pleometrosis (several queens associate during founding) (WALoFF, 1957).

C. herculeanus and C. ligniperda are generally monogynous although some nests may contain up to three queens (H6LLDOBLER, 1962). In these two species, colony founding may also occur by haplometrosis or pleometrosis (H~iLLDOBLFR, 1962).

Polygynous species : Plagiolepis pygmaea is a polygynous species wi th a mean of 17 queens per colony (MERCIER et al., 1985). In southern France, we have never observed queens founding new colonies claustrally. We therefore suspect that this mode of colony founding is absent or very rare in this species. New colonies probably result f rom budding and new queens are added by adoption of newly-mated queens after the mat ing flights occurr ing in mid-July.

L humilis is a polygynous ant (NEWELL, 1909; MARKIN, 1970; KELLER, 1988b). In this species, workers are sterile (MARKIN, 1970; BARTELS, 1988); there is usually no nuptial flight by queens, mat ing occurs, in the nest (PASSERA and KELLER, 1987; PASSERA et al., 1988b), and colony founding is accomplished by budding (N~VELL and BARBER, 1913; MARKIN, 1970).

E x p e r i m e n t a l procedure

Founding queens of L. niger were collected in June 1987 near Lausanne, Switzerland and those of C. herculeanus and C. ligniperda were collected jus t af ter their nuptial flight in early July close to the Marchairuz pass in the Jura mountains , Switzerland. Young queens of these three species were housed in small nests (see PASSERA et al., 1988a) and were fed three t imes a week with honey and mealworms as soon as the first workers emerged. The number of eggs, larvae, pupae and workers was counted and the queens weighed weekly for two years. All colonies of the three species were overwintered at 12 - 3 ~ C for three months f rom the beginning of December to the end of February. There was high mortal i ty in the three species. Only data from queens survivir~g to the end of the exper iment were considered, i.e., 9 in L. niger and C. herculeanus each and 7 in C. ligniperda.

P. pygmaea colonies were collected near Toulouse, France, in early July before the yearly mat ing flight. They contained laying queens and sexual pupae. The ants were kept in small nests (see PASSERA, 1969) and maintained in a rearing room at 26.5 • 1 ~ C during the experimental period and at 12 • 1 ~ C during overwintering. After the emergence of the sexuals, mating flights occurred in a large experimental cage in the labo- ratory. The newly- inseminated queens shed their wings and re turned to the nests. At this time, each queen was marked wi th a spot of paint. As a result of the re turn of the newly mated females, at the beginning of October, colonies contained both young queens less than four months old and old queens collected f rom the field, at least 16 months old. These colonies overwintered until March of the following year. Then, they were split into 24 units containing one "young" queens now 9 months old and 24 units containing one "old ~'' queen being at least 21 months old. Each queen was

F E C U N D I T Y OF A N T Q U E E N S 119

nursed by 23 _ 4 w o r k e r s . Since in this species the fecundi ty of individual queens is re la ted to weight (MERCIER et al., 1985) we selected queens wi th s imilar we igh t : the mean weight of the young queens was 0.810 • 0.019 mg while tha t of the old queens was 0.808 • 0.017 mg. During the f i rs t days following of the beginning of the experiment , the uni ts were moni tored daily in order to de termine when the queens began to lay. Later, eggs were removed and counted at 7, 14, 21, 28 and 35 days af te r the beginning of the experiment . At the same t ime each queen and a r a n d o m sample of 10 eggs f rom both young and old queens were weighed.

Colonies of I. humilis were collected in December 1986 in Port-Leucate near Perpignan in sou thern France. They were reared in condi t ions s imilar to those described by PASSERA et al. (1988a) ; the ants were main ta ined at a cons tan t t empera tu re of 28 • 2 ~ C and fed wi th an art if icial diet (see KELLER et al. in press). Under these condi t ions queenless uni t s rear winged queens and males (PASSERA et al., 1988b). Mat ing soon occurs (5.1 ~- 2.0 days) a f te r emergence (KELLER and PASSERA, 1988; PASSERA et al., 1988b). Immedia te ly af te r mat ing and dealation, 10 newly-inseminated queens were weighed, then housed indivi- dually in exper imenta l uni ts consist ing of 700 workers . At 15, 30 and 45 days af te r the beginning of the experiment , each queen was weighed and subjected to an oviposi t ion tes t (see KELLER, 1988a) : each queen was confined to a small vial conta ining a layer of damp p las te r for 14 hours and the n u m b e r of eggs laid was counted wi th the aid of a dissecting microscope. To compare the fecundity of newly-emerged queens to tha t of old queens, 12 old queens which were collected on 7 April 1987 at the same place as the o the r colonies were submi t t ed to the same procedure. The age of these la t ter queens was unknow n bu t it was close to one year since queens are produced yearly in late spring. Fur thermore , mos t of them were probably not older t han one year since ca. 90% of the queens are executed by workers in May jus t before the t i m e of the p roduc t ion of new sexuals (KELLER et al., 1989).

Statistical analysis All da ta were found to be normal ly d is t r ibuted according to the Kolmogornov test .

All means were therefore compared wi th the t-test.

R E S U L T S

Species using independent c o l o n y f o u n d i n g

T h e t h r e e s p e c i e s e m p l o y i n g i n d e p e n d e n t c o l o n y f o u n d i n g e x h i b i t e d a

s i m i l a r : p a t t e r n i n t h e c h a n g e i n w e i g h t a n d f e c u n d i t y . D a t a a r e t h e r e f o r e

p r e s e n ~ t e d t o g e t h e r f o r ' t h e s e s p e c i e s . E g g : t a y i n g s t a r t e d r a p i d l y a f t e r t h e

m a t i n g f l i g h t (table I). T h e f i r s t l a r v a e w e r e p r o d u c e d f i r s t i n L. niger t h e n

i n t h e t w o C a m p o n o t u s s p e c i e s (table I). S i m i l a r l y , p u p a t i o n o f t h e f i r s t

b r o o d a n d e m e r g e n c e o f t h e f i r s t w o r k e r s o c c u r r e d e a r l i e r i n L. niger t h a n

i n t h e t w o C a m p o n o t u s s p e c i e s . I n t h e t w o C a m p o n o t u s s p e c i e s , C. l igniperda h a d t h e s l o w e r b r o o d d e v e l o p m e n t , p u p a e a n d w o r k e r s b e i n g o b s e r v e d ca .

o n e w e e k l a t t e r t h a n i n C. herculaneus .

120 L. K E L L E R and L. P A S S E R A

Tab le I. - - F i r s t r e c o r d of w o r k e r s a n d e a c h b r o o d s t a g e in t he co lon ies o f spec i e s e x h i b i t i n g i n d e p e n d e n t co l ony f o u n d i n g .

T a b l e a u I. - - D a t e s d ' a p p a r i t i o n des ouv r ib re s et du c o u v a i n d a n s les co lon ies d ' e sp6ces avec f o n d a t i o n i n d 6 p e n d a n t e .

Spec i e s F i r s t eggs F i r s t l a rvae F i r s t p u p a e F i r s t w o r k e r s

L a s i u s n i g e r 2.8 -- 1.7 d a y s 3 rd w e e k 4 th w e e k 5 th w e e k

C a m p o n o t u s h e r c u l a n e u s 2.8 • 1.8 d a y s 4 th w e e k 5 th w e e k 7 th w e e k

C a m p o n o t u s l i g n i p e r d a 2.1 • 1.3 days 4 th w e e k 6 th w e e k 8th w e e k

150

120

o 30- 30-

0 0

A : L niger ~ ~ young queens 30 -*

~176

0 1 2 3 4 5 6 7 8 g

Time s i n c e s t a r t of experiment ( w e e k s )

B : C. herculaneus -----0--- young queens . . . . . ~

�9 o l d q u e e n s

�9 i �9 i �9 i �9 , �9 , �9 , - , , , , , - ,

1 2 3 4 5 6 7 8 9 10 Time s i n c e s t a r t o f e x p e r i m e n t

30 �84

~ 2O

o

i E 7= lo

C : C. llgnlperda ~ young ~ueens �9 old q u e e n s ...

.,~

N S ~ . I N S ~ . . Fig. 1. - - M e a n s + SE n u t n b e r o f eggs p e r co lony of (A) Lasius niger (N = 9), (B) Camponotus herculeanus (N = 7) a n d (C) Camponotus ligniperda (N = 7) d u r i n g t h e 60 d a y s fo l lowing m a t i n g f l igh t ( young queens ) a n d 60 d a y s fo l l owing over- w i n t e r i n g (old q u e e n s ) . P robab i - l i t ies a re g iven fo r t - t e s t s ; * =

' �9 i - , - | - J �9 J �9 = . t - , �9 = �9 ,

1 2 a 4 s e z a o lo P < 0.05; ** = P < 0.01; *** = Timeslncestadofexpedment(weeks) P < 0.001.

Fig. I. - - N o m b r e d 'oeufs m o y e n (-- e r r e u r s t a n d a r d ) c o m p t 6 s darts de s soci~t6s de (A) Lasius niger (N = 9), (B) Camponotus herculeanus (N = 7) et (C) Camponotus ligniperda (N = 7) p e n d a n t les 60 j o u r s qu i s u i v e n t l e v o l n u p t i a l ( j eunes re ines) e t p e n d a n t les 60 j o u r s qu i s u i v e n t l ' h i b e r n a t i o n (vieilles re ines) . Les p robab i l i t 6 s s e n t d o n n ~ e s ap r~s app l i c a t i on d u t e s t de t ; * = P < 0,05; ** = P < 0,01; *** = P < 0,001.


Queen fecundity and brood composition

In the th ree species, the n u m b e r of eggs pe r colony regular ly inc reased a f te r colony founding (fig. 1). The m a x i m u m n u m b e r of eggs were r ecorded at week 6 in L. niger, at week 7 in C. herculanteus and at week 3 in C. ligniperda. After having reached this max imum, egg n u m b e r dec reased in the three species and no more eggs were r eco rded in the colonies f rom weeks 15, 9 and 10 onwards for L. niger, C. herculaneus and C. ligniperda, respect ively. The absence of eggs in the colonies r e su l t ed f rom the cessa t ion of egg laying by queens un t i l a f te r overwinter ing.

Compos i t ion of the colonies a f te r overwin te r ing is given in table II. All colonies of the three species con ta ined no eggs and no pupae. The n u m b e r of larvae and worke r s was s imi la r in the two species of Camponotus ( t - tes t , NS). In L. niger the n u m b e r of larvae and w or ke r s was far g rea te r ( t - tes t ; P < 0.001 for bo th larvae and workers ) than in the two species of Campono- tus. After overwinter ing, queens rap id ly s t a r t ed to lay eggs in the three species (fig. 1); the n u m b e r of eggs pe r colony regular ly inc reased in the th ree species and the m a x i m u m n u m b e r of eggs were r eco rded in the censuses p e r f o r m e d at weeks 4, 4 and 5 for L. niger, C. herculaneus and C. ligniperda, respect ively. In the three species, the n u m b e r of eggs pe r colony was h igher in the censuses p e r f o r m e d a f te r overwin te r ing than in the corres- pond ing ones p e r f o r m e d af te r nup t ia l f l ight (fig. 1). The difference was signi- f icant for all compar i sons except one in L. niger and C. herculaneus. In C. ligniperda, the n u m b e r of eggs was also always h igher a f te r overwinter ing, bu t the d i f ference was s ignif icant only for three censuses.

Weight of queens

After nup t ia l flight, queens of the three species exper ienced a dras t ic and cont inuous loss of weight up to the t ime of emergence of the f i rs t worke r s (fig. 2). Weight decreased f rom 27.6 • 2.6 mg to 15.1 - 3.2 mg (mean __ S D ; pa i r ed t - tes t ; P < 0.001; decrease 45 %), 118.6 +- 26.0 to 76.3 4- 24.0 (P < 0.001; decrease 36 %) and 164.6 --- 24.8 to "139.0 4- 17.1 (P < 0.001 ; decrease 16 %) in L. niger, C. herculaneus and C. ligniperda, res-

Table II. - - Composition of the colonies after overwintering.

Tableau II. - - Composition des colonies apr6s l'hibernation.

Species Number Number Number Number of eggs of larvae of pupae of workers

Lasius niger 0 38.4 • 14.7 0 23.5 • 4.3

Camponotus herculaneus 0 5.3 - 3.8 0 3.5 • 1.0

Camponotus ligniperda 0 7.1 • 2.8 0 3.5 - 4.3


A : L niger ---.--I=---. young queetls

4 0 1 �9 old queens 160.

J �9 ** *** . , . . . NS 140. �9 . ***

~' ~' 1 ~ .

z z ~ 19o-

80-

0 1 2 3 4 5 6 7 8 9 0 T i m e since start of experiment (weeks)

190

~ 170.

140 -

130-

120 O

- - - - o - - - young queens C : C. ~gniperda -----B-,,-- old queens

NS NS " " T T NS

. = - , - , . = . , . , . , . , . , . r 1 2 3 4 5 6 7 6 9 1 0

~ m e since start of oxpedmont (weeks)

- - - - D - - - young queens B : C. hercdeneus

~- o/d queens

INS * "

1 2 3 4 S 6 7 8 9 1 0

T i m e since start of experiment (weeks)

Fig. 2. --Means • SE weight of (A) Lasius niger (N -- 9), (B) Campo- notus herculeanus (N = 7) and (C) Camponotus ligniperda (N = 7) queens during the 60 days following mating flight (young queens) and 60 days following overwintering (old queens). Probabilities are given as in fig. 1.

Fig. 2. w Poids moyens (• erreur standard) des reines de (A) Lasius niger (N = 9), (B) Camponotus herculeanus (N = 7) et (C) Camponotus ligniperda (N -- 7) pendant les 60 jours qui suivent le vol nuptial (jeunes reines) et pendant les 60 jours qui suivent l'hibernation (vieilles reines). Les probabilit6s sent calcul6es comme dans la fig. 1.

pect ively . Af te r the t ime of e me r ge nc e of the f i r s t worke r s , t he weigh t of q u e e n s of the th ree species i n c r e a se d up to a va lue s l ight ly h i g h e r t h a n tha t f o u n d at the t i m e of m a t i n g fl ight. Weigh t of q u e e n s dec reased s l ight ly d u r i n g the t ime of ove rwin t e r ing , b u t i nc r e a se d aga in a f t e r o v e r w i n t e r i n g .

Species us ing dependent colony f o u n d i n g

Plagio lep is p y g m a e a

After t r a n s f e r r i n g colonies f r o m the r o o m w he r e they o v e r w i n t e r e d to the r e a r i n g room, q u e e n m o r t a l i t y was 12.5 % (N = 24) for y o u n g q u e e n s a n d 25 % (N = 24) for old queens . However , this d i f fe rence was no t signi- f i c an t 0r 2 = 1.23).

Young q u e e n s (N = 21) la id the f i r s t eggs 6.1 ___ 0.6 days a f t e r over- w i n t e r i n g , w h e r e a s old q u e e n s (N = 18) la id ca. two days l a t e r (7.9 • 0.6


d a y s ; P ( 0 . 0 1 ) . Eggs la id by the young q u e e n s were s ign i f i can t ly heav ie r (12.0 ~ 0.04 lxg) t h a n the ones la id by the old q u e e n s (10.8 - 0.01 ~ g ; P 0.01).

F e c u n d i t y of young queens was very s imi l a r to t ha t of old q u e e n s except a t weeks 1 a n d 5 whe re y o u n g queens h a d a h i g h e r f e c u n d i t y (fig. 3A). Overal l , the m e a n , n u m b e r of eggs pe r colony r e c o r d e d d u r i n g the 5 censuses was 31.4 ___ 29.0 for y o u n g queens a n d 17.8 - 16.7 for o ld q u e e n s (t = 1.71 ; NS). I n th is species, f e cund i t y of queens is d e p e n d e n t o n the n u m b e r of n u r s e s (PAssERA, 1972). S ince in ou r expe r imen t s , the n u m b e r of w o r k e r s p e r co lony was low (23 ~ 4), this expla ins the re la t ive ly low f e c u n d i t y of q u e e n s c o m p a r e d to tha t of the one obse rved in colonies n u r s e d by a h igh n u m b e r of w o r k e r s (PAsSERA, 1972).

We igh t of old queens was n o t s ign i f i can t ly d i f f e r en t of t ha t of y o u n g q u e e n s except a t week 2 (fig. 4A).

I r idomyrmex humilis

D u r i n g the 45 days of the expe r imen t , the f e c u n d i t y of y o u n g queens (N = 10) was s imi l a r to t ha t of the old ones (N=~ 12) (fig. 3B) a n d the tota l n u m b e r of eggs la id by young queens a n d old q u e e n s was s i m i l a r (11.9 ___ 8.1, r e spec t iv ly ; NS).

I n c o n t r a s t , y o u n g queens weighed less t h a n the old ones, this d i f fe rence be ing s i gn i f i s an t for all weeks (fig. 4B).

12-

1 0 -

o 6 �84

IE 4

0 0

A : P. pygmao= NS . - . - o - - - young queens 8 -

�9 ok[ queens 7 -

teS 6

0 4 '

Z 2 "

1

0 , ; " ~ - ~ - ~ - ; - :

T i m e I lnce start of experiment (weeks)

B : I. humitis

young queens NS

N,S; �9 o(d queens

Time since start o f experiment (weeks)

Fig. 3. - - (A) Means ----- SE number of eggs per colony of Plagiolepis pygmaea containing young queens less than 9 months old (White squares, N = 21) and old queens being one year older (black squares, N = 18). (B) Means ----- SE fecundity of Iridomyrmex humilis newly mated queens (white squares, N = 10) and old queens about one year old (black squares, N --- 12). Probabilities are given as in figure 1.

Fig. 3. - - (A) Nombre d'~eufs moyen ( - erreur + standard) compt6s dans des soci6t6s de Plagiolepis pygmaea contenant une jeune reine 5g6e de moins de 9 mois (carr6s blancs, N = 21) et une vieille reine ~g6e d'au moins un an (carr6s noirs, N = 18). (B) F6condit6 moyenne (• erreur standard) de reines nouvellement f6cond6es d'Iridomyrmex humilis (carr6s blancs, N = 10) et de reines vieilles ~g6es d'environ un an (carr6s noirs, N = 12). Les probabilit6s sont calcul6es comme dans la figure 1.


g

1.3-

L 2 -

1 . 0 �84

0 . 9

A : P. pygmaea - - - - o - - young queens

' �9 01d queens

NS NS NS

�9 i - ~ , = - = , = �9 , 1 2 3 4 5 6

T i m e s ince start o f exper iment (weeks)

A ca E

J=

4 .0 -

3.6 ~

3.4 ~

3.2 ~

3.0 ~

2.8 ~

ze~ 2.4

B : I. humilis young queens

. . �9 old queens

T i m e s ince s tar t o f e x p e r i m e n t (weeks )

Fig. 4. - - Means + SE weights of : (A) Plagiolepis pygmaea young queens less than 9 months old white squares, N = 21) and old queens being one year older (black squares, N = 18).' (B) Iridomyrmex humilis newly mated queens (white squares, N = 10) and old queens about one year old (black squares, N = 12). Probabilities are given as in figure 1.

Fig. 4. - - Poids moyens (-- erreur standard) de : (A) jeunes reines de Plagiolepis pygmaea -~g6es de moins de 9 mois (carr6s blancs, N = 21) et de vieilles reines fig6es d'au moins un an (carr~s noirs, N = 18). (B) reines d'Iridomyrmex humilis nouvellement f6cond6es (carr6s blancs, N = 10) et de vieilles reines fig6es d'environ un an (carr6s noirs, N = 12). Les probabilit6s sent calcuMes comme dans la figure 1.

D I S C U S S I O N

F o r q u e e n s o f t h e t h r e e spec i e s w i t h i n d e p e n d e n t c o l o n y f o u n d i n g , t he n u m b e r of eggs l a i d i n c r e a s e d r e g u l a r l y d u r i n g the f i r s t w e e k s a f t e r t he m a t i n g f l i gh t a n d t h e n d e c r e a s e d w h e n the f i r s t l a r v a e h a t c h e d . Th is p a u s e in egg- lay ing d u r i n g the g r o w t h o f t he f i r s t b r o o d is w e l l - k n o w n in i n d e p e n - d e n t c o l o n y f o u n d i n g a n t s ; i t h a s b e e n o b s e r v e d b y POLDI (1963) in Tetra- m o r i u m caespi tum, MARKIN et al. (1972) in Solenopsis invicta ONOYAMA (1981) in Messor aciculatus a n d KITAMURA (1984) in Formica (Serviformica), japonica. This d e c r e a s e in egg n u m b e r m a y r e s u l t e i t h e r f r o m o o p h a g y of eggs b y l a r v a e a n d / o r p h e r o m o n a l i n h i b i t i o n o f q u e e n f e c u n d i t y b y l a rvae .

A f t e r o v e r w i n t e r i n g , t he p a t t e r n w a s s i m i l a r to t he f o u n d i n g s t age w i t h a r a p i d i n c r e a s e in egg n u m b e r f o l l o w e d by a d e c r e a s e . H o w e v e r , in a l l t h r e e spec ies , t h e n u m b e r o f eggs in t he co lony i n c r e a s e d a t a f a s t e r r a t e a n d r e a c h e d a h i g h e r n u m b e r a f t e r o v e r w i n t e r i n g t h a n j u s t a f t e r m a t i n g . S i m i l a r r e s u l t s h a v e b e e n f o u n d in o t h e r spec ies w i t h i n d e p e n d e n t c o l o n y f o u n d i n g ; in Myrmica rubra (BRIAN, 1957), Odontomachus haematodes (COLOMBEL, 1970), Solenopsis invicta (MARKIN et al., 1973; LOFGREN et al., 1981), Messor ebeninus (TOHMr 1975) a n d M. barbarus (CERDAN a n d DELYE, 1987), f e c u n d i t y o f q u e e n s w a s f o u n d to i n c r e a s e as a f u n c t i o n o f t h e i r age a n d age of t h e co lony . S i m i l a r l y , in Leptothorax nylanderi t h e r e is a cons-


tant increase in the n u m b e r of larvae presen t dur ing the f irst 7 years of colony life (PLATEAUX, 1986). All these data are in ag reemen t wi th histological and ana tomica l observat ions on queens of Camponotus lateralis (PALMA-VALLr and D~LXE, 1981) showing that the n u m b e r of follicles per ovary increased with the age of the queen f rom 2 to 8 in young queens (1 to 3 years old) to over 20 in old queens (5 to 6 years old).

General ly speaking, this increase of queen fecundi ty and b rood quant i ty in colonies as a funct ion of queen and colony age is l inked to the exponent ia l g rowth of the colonies during the f irst years of the i r life (see BRIAN, 1965 and ELMES, 1965 and ELMES, 1973). Fecundi ty of queens is p robab ly dependent on the n u m b e r of worke r s which can feed them and care for the brood. In this respect , it is wor thwhi le to ment ion the higher increase of egg n u m b e r / c o l o n y a f te r overwin te r ing (as com pa red to the t ime a f te r the mat ing flight) in L. niger t han in the ' two Camponotus. This higher increase p robab ly resul ted f r o m the h igher n u m b e r of worke r s in the L. niger at the end of overwintering.

The pa t t e rn exhibited by the dependent founding species P. pygmaea and I. humilis cont ras ts sharply wi th that found in the independent founding species. I. hurnilis queens reached very early, i.e., less than two weeks a f te r emergence, the i r maximal fecundity. Similarly; fecundity, of young P. pygmaea queens, only a few month old, was at least equivalent , if not higher, than tha t of queens one year older. These data suggest tha t in con t ras t to the queens wi th independent colony founding, newly-mated queens of species utilizing dependent colony founding are able to reach their maximal ra te of egg ou tpu t when they are very young : a few weeks old for I. humilis, and a few mon ths old for P. pygmaea. However , the scarci ty of research conducted on the fecundi ty of young dependent ly founding queens prevents generalisa- tion. EDWARDS (1987) obta ined different resul ts in Monomorium pharaonis. Fecundi ty of young queens was far infer ior to that of older queens. Similarly, young queens of Myrmica rubra are less fecund than older ones (BRIAN, 1988). However , it is necessary to ment ion that queens of these two species p resen t some pecular i t ies ; Monomorium pharaonis queens exhibit a life-cycle clearly separa ted into three distinct per iods character ized by a change in the i r inhi- b i tory power over sexual product ion. Fecundi ty of queens m a y therefore de- pend on this cycle. Gynes of Myrmica rubra may ei ther found new colonies independent ly by non claustral colony founding or join an incipient nest (G.W. ELMES pets . com.). This species may therefore not be a typical dependent colony founding species.

Queens of species with independent a n d , dependent colony founding also di f fered drast ical ly in weight change Over t ime. During the f i rs t weeks of colony founding pr ior to the emergence of the f irst workers , there was a significant drop in weight for queens founding independent ly . This drop resul ted f r o m the ca tabol ism of the flight muscles and large fat reserves that gynes accumula ted p r io r to nupt ial flight. At swarming, fat content repre-

126 L. KELLER and L. PASSERA

sents 51, 43 and 46 % of the dry weight of gynes of L. niger, C. herculaneus and C. ligniperda, respect ively (KELLER and PASSERA, 1989b). These fat reserves p rov ide the energy needed by queens to feed themselves and the f i rs t b r o o d unt i l the f irst worke r s s t a r t foraging. In contras t , queens of P. pygmaea and I. humilis did not lose weight dur ing the f irst per iod of thei r r eproduc t ive activity. This can be explained by the fact that soon a f te r mat ing, these queens are immedia te ly fed by workers . In this respect , it should be men t ioned that gynes founding dependent ly do not accumula te large am oun t s of fat p r ior to mat ing (KELLER and PASSERA, 1989 b). For example , fa t const i tu tes only 25 % of dry weight of m a t u r e gynes of I. humil is (KELLER and PASSERA, 1988 ; KELLER and PASSERA, 1989 b).

The weights of queens of species founding independent ly increased rap id ly a f t e r the emergence of the f irst workers . At the t ime of overwinter ing, the i r weight was s imilar to that at the t ime of the nupt ia l flight. Dissection of queens showed that this increase in weight resul ted at least par t ia l ly f rom the deve lopment of the ovaries and s torage of new fat reserves (KELLER and PASSERA, unpub l i shed data). After overwinter ing, the weight of queens fu r the r increased, bu t at a slow rate, being p robab ly due mos t ly to ovary deve lopment .

Young queens of I. humilis were significantly l ighter than old ones. In I. humilis, fecundi ty of queens is l inked to thei r weight, heavier queens having a higher fecundi ty (KELLER, 1988b). ,Our resul ts the re fore seem cont rad ic tory since old queens were heavier but had s imilar fecundi ty to young ones. One possible explanat ion is that l abora to ry condit ions m a y have influenced the process of fat accumulat ion. Young queens which unde rweg t all of their m a t u r a t i o n in the labora tory may have had less oppor tun i ty to accumula te fat reserves in compar i son to the old queens which were collected in the field. In P. pygmaea, there was only little difference be tween young and old queens bo th for weight and fecundity.

Consider ing the reproduct ive potent ia l i ty of the queens mus t take into account the i r life-span. Queens of L. niger have been observed to live more than 28 years (KUTTER and STUMPER, 1969). One colony of Camponotus ligniperda was still alive af ter 7 years of observa t ion (KELLER unpubl i shed data). Although young colonies of C. tigniperda may occasionally conta in several queens (H/:iLLDOBLER, 1962), we have never found m o r e than one queen in m a t u r e colonies (KELLER unpubl i shed data), suggesting tha t the queen of the above m e n t i o n n e d colony has been alive for more than 7 years. While we should r em a i n caut ious because mos t data come f r o m labora to ry observations, a survey of the l i terature seems to indicate tha t long life-spans of m a t e d queens m a y be a com m on fea ture of monogynous independent founding species. The survivorships of queens was at 1east 5/6 years in Camponotus lateralis (PALMA VALLI and DgLYE, 1981), 5/6 years in several Myrmecia (HASKINS and HASKINS, 1980), 10 years in Ectatomma quadridens (D. FRESNEAU


and J.P. LACHAUD, pers. com.), 9 years in Ectatomma ruidum (HASKINS and HASKINS, 1980), Messor semirufus (ToHM~ and TOHM~, 1978) and Lasius alienus (JANET, 1904), 10 years in Apnaenogaster picea (HASKINS, 1960), 11 years in Camponotus perthensis (HASKINS and HASKINS, 1980), 12.5 years in Rhytido- ponera purpurea (HASKINS and HASKINS, 1980), 11 to 20 years in several Lepto- thorax species (PLATEAUX, 1986), 17/18 years in Stenamma westwoudi (DoNISTHORPE, 1936), 20 years in Crematogaster scuteUaris (J. CASEVITZ- WEULERSSE, com. pers.) and at least 22.5 years in Lasius flavus (PRESCOTY, 1973). Similarly, physiological studies by de te rmin ing s p e r m deplet ion in ~spermatheca gave an approx ima t ion of 6/7 years for the mean life span of .queens in the monogynous f o r m of Solenopsis invicta (TSCHINKEL, 1987).

The life-spans of queens f rom polygynous dependent colony founding species seem to ~be shorter . Queens have been es t imated to live less than one year in Monomorium pharaonis (PEACOK and BAXTER, 1950; PETERSEN- BRAUM, 1975), 4.5 years in Odontomachus haematodes (HASKINS and HASKINS, 1980), and p robab ly less than 2 years in Wasmania auropunctata (P. ULLOA o CHACON and D. CHERIX, pets . com.). According to ELMES (1980) it is very dif- ficult to main ta in Myrmica queens in the l abora to ry for more than one season. Empi r ica l data suggest that in the field, the queens of Myrmica sulcinodis may live 4/5 years (ELMES, 1987). The life-span of mos t queens of. I. humilis is less than one year, resul t ing f r o m a mass ive regicide that occurs each year at the beginning of the reproduc t ive season (KELLER et a!., 1989). No data are present ly available concerning the life-span of P. pygmaea queens but it should be recalled tha t in the exper iment repor ted here the mor ta l i ty was es t imated at 25 % for old queens a t the end of overwintering. I t is reasonable to in te rpre t these da ta as the resul t of a ra ther shor t life-span of queens in this species.

Thus, a m a j o r difference in the life his tory of queens using dependent and independent colony founding may be a shor te r life span a shor te r delay in reaching m a x i m u m egg-output for the former . Fu r the rmore , since the u l t imate fac tors influencing the f i tness of queens is not the n u m b e r of workers , bu t the n u m b e r of sexuals produced, it should be ment ioned that queens of species wi th independent colony founding have a chance to produce sexuals only when the colony is ma tu re , i.e., only a f te r several years (see Oster and WILSON, 1978), whereas queens employing dependent colony founding m a y produce sexuals when they are young, e.g., less than one year in I. humilis (KELLER and PASSERA, unpubl i shed data).

Finally, NONACS (1988) developed a series of kin selection models in which in invest igated factors which m a y favor polygyny in eusocial Hymenop te r a . Polygyny was found to be favored by shor te r l ife-span of queens. Our review on the l i t te ra ture of l ife-span of queens of monogynous vs. polygynous species seems to suppor t the models of NONACS. However , as ment ioned by

128 L. K E L L E R a n d L. P A S S E R A

NONACS h i m s e l f , i t i s n o t p o s s i b l e t o d e t e r m i n e w h e t h e r s h o r t - l i v e d q u een ~ .

f a v o r p o l y g y n y o r , a l t e r n a t i v e l y , i f p o l y g y n y s e l e c t s f o r s h o r t - l i v e d q u e e n s .

ACKNOWLEDGMENTS. - - Our special thanks are due to E. L. VARGO and two anonymous: r e fe rees for helpful criticisms and for English language editing.

References

BARTELS P.J., 1988. - - Reproductive caste inhibition by Argentine Ant queens : new me- chanisms of queen control. Insectes Soc., 35,

BRIAN M.V., 1957. - - The growth and development of colonies of the ant Myrmica. Insectes Soc., 4, 177-190.

BRIAN M.V., 1965. - - Social Insect Populations. Academic Press, publ., London and New York, 135 p.,

BRIAN M.V., 1983. - - Social Insects. Ecology and Behavioural Biology. Chapman and Hall, publ., London, 377 p.

BRIAN M.V., 1988. - - The behaviour and fecundity of queens of different ages in synthetic groups of Myrmica rubra L. with different worker populations. Insectes Soc., 35, 153-166.

CERDAN P., DELYE G., 1987. - - La fondation et les premi6res ann6es du d6veloppement de la soci6t6 de Messor barbarus (L.) (Hymenoptera, Formicidae). C. R. Acad. Sci. Paris, 305, s&ie 1II, 31-34.

COLOMBIER P., 1970. ~ Recherches sur la biologie et l '6thologie d'Odontomachus haema- Lodes (Hym., Formicoidea, Poneridae). Biologie des reines. Insectes Soc., 17, 199-204.

DONISTHORPE H., 1936. ~ - The oldest insect on record. Entomol. Rec. and J. Var., 48, 1-2. EDWARDS J.P., 1987. - - Caste regulation in. the pharoh 's ant Monomorium pharaonis : the

influence of queens on the product ion of new sexual forms. Physiol. Entomol., 21, 31-39.

ELMES G.W., 1973. - - Observations on the density of queens in natural colonies of Myrmica rubra L. (Hymenoptera, Formicidae). J. Anita. Ecol., 42, 761-771.

ELMES G.W., 1980. - - Queen numbers in colonies of ants of the genus Myrmica. lnsectes Soc., 27, 43-60.

ELMES G.W., 1987. ~ Temporal variaton in colony populations of the ant Myrmica sulcinodis. I. Changes in queen number, worker number and spring production. J. Anita. Ecol., 56, 559-571.

FRANKS N.R., H/~LLDOBLER B., 1987. ~ Sexual competi t ion during colony reproduct ion in army ants. Biol. J. Linn. Soc., 30, 229-243.

HASKINS C.P., 1960. ~ Note on the natural longevity of fertile females of Aphaenogaster picea. J.N.Y. Entomol. Soc., 68, 66-67.

HASKINS C.P., HASKINS E.F., 1980. Notes on female and worker survivorship in the archaic ant genus Myrmecia. Inectes Soc., 27, 345-350.

H/SLLDOBLER B., 1962. - - Zur Frage der Oligogynie bei Camponotus ligniperda Latr. und Camponotus herculeanus L. (Hym. Formicidae). Z. angew. Ent., 49, 337-352.

HOLLDOBLER B., WILSON E.O., 1977. - - The number of queens : an impor tant trait in ant evolution (Hym. Formicidae). Naturwissenschaften, 64, 8-15.

JANET C., 1904. - - Observations sur les fourmis. Ducourtieux et Gout, publ., Limoges, 144 p. KELLER L., 1988a. - - Evolutionary implications of polygyny in the Argentine ant, Irido-

myrmex humilis (Mayr) (Hymenoptera : Formicidae) : an experimental study. Anim. Behav., 36, 159-165.

KELLER L., 1988b. - - Pouvoir at tractif des reines de la fourmi d'Argentine, Iridomyrmex humilis (Mayr). R61e de la polygynie et du statut physiologique des reines. Bull. Soc. Vaud. So. Nat., 79, 92-103.

KELLER L., CHERIX D., ULLOA-CHACON P. (in press). - - Description of a new artificial diet for rearing ant colonies as Iridomyrmex humilis, Monomorium pharaonis and Wasmannia auropunctata (Hymenoptera : Formicidae). Insectes Soc.

F E C U N D I T Y OF A N T Q U E E N S 129

KELLER L., PASSERA L., 1988. - - Energy investment in gynes of the Argentine Ant Irido- myrmex humilis (Mayr) in relation to the mode of colony founding in ants (Hyme- noptera : Formicidae). Int. J. Invert. Repr. and Dev., 13, 31-38.

KELLER L., PASSERA L., 1989a. m Influence of the number of queens on ne tsmate recognition and at tractiveness of queens to workers in the Argentine Ant Iridomyrmex humilis (Mayr). Anita. Behav., 733-740.

KELLER L., PASSERA L. 1989b. - - Size and fat content of gynes in relation to the mode of colony founding in ants (Hymenoptera , Formicidae). Oeeologia, 80, 236-240.

KELLER L., PASSERA L., SUZZONI J.P., 1989. -- Queen execution in the Argentine Ant, Iridomyrmex humilis. PhysioL Entomol., 14, 157-163.

KITAMURA S., 1984. - - Colony fotmdation and development of Formica (Serviformica) japonica Motshulsky (Hymenoptera, Formicidae). Kontyu, 52, 411-426.

KUTTER H., STUMPER R., 1969. - - Hermann Appel, ein leidgeadelter Entornologe (1892- 1966). Proc. 6th Int.. Cong. IUSSI, Bern, 275-279.

LOFGREN C.S., BANKS W.A., GLANCEY B.M., 1975. - - Biology and control of impor ted fire ants. Ann. Rev. Entomol., 20, 1-30.

MARKIN G.P., 1970. - - The seasonal life cycle of the Argentine ant Iridomyrmex humilis (Hymenoptera, Formicidae), in southern California. Ann. Entomol. Soc. Am., 63, 1238-1242.

MARKIN G.P., COLLINS H.L., DILLIER 3.H., 1972. - - Colony founding by queens of the red impor ted fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am., 65, 1053-1058.

MARKIN G.P., D~LLIER J.H., COLLINS H.L., 1973. - - Growth and development of the red impor ted fire ant, Solenopsis invicta. Ann. Entomol. Soc. Am., 65, 1053-1058.

MARKIN G.P., DILLIER J.H., COLLINS H.L., 1973. - - Growth and development of colonies of the red impor ted fire ant Solenopsis invicta. Ann. Entomol. Soc. Am., 66, 803-808.

MERCIER B., PASSERA L., SUZZONI J.P., 1985. - - Etude de la polygynie chez la fourmi Pla- giolepis pygmaea Latr. (Hym. Formicidae). I. La f6condit6 des reines en condition exp6rimentale monogyne. Insectes Soc., 32, 335-348.

NEWELL W., 1909. - - The life history of the Argentine Ant. I. Econ. Ent., 2, 174-192. NEWELL W., BARBER T.C., 1913. - - The Argentine Ant. U.S.D.A. Bureau of Entomology Bull.,

122, 98 p. NONACS P., 1988. - - Queen number in colonies of social hymenoptera as a kin-selected

adaptat ion. Evolution, 566-580. 'ONOYAMA K., 1981. - - Brood rearing by colony founding queens of the harvester ant

Messor aciculatus. Kontyu, 49, 624-640. OSTER G.F., WILSON E.O., 1978. - - Caste and Ecology in the Social Insects. Princeton

University Press, Princeton N J, 352 p. PALMA-VALLI G., DELVE G., 1981. ~ Contr61e neuro-endocrine de la ponte chez les reines de

Camponotus lateralis Olivier (Hymdnopt6res, Formicidae). Insectes Soc., 28, 167-181. PASSERA L., !969. - - Biologie de la reproduct ion chez PIagiolepis pygmaea Latr. et ses deux

parasi tes sociaux Plagiolepis grassei Le Masne et Passera et Plagiolepis xene St. (Hym. Formicidae), Annls Sci. nat. Zool., Biol. anim. 12e sdrie, 11,. 327-481.

PASSERA L., 1972. - - Etude de quelques facteurs r6glant la fdcondit6 des reines de PIagiolepis pygmaea Latr. (Hym. Formicidae). lnsectes Soc., 19, 369-388.

PASSI~RA L., KELLER L., 1987. - - Energy investment during the differentiat ion of sexuals and workers in the Argentine ant Iridomyrmex humilis (Mayr). Mitt. Schweiz. ent. Ges., 60, 249~260.

PASSERA L., KELLER L., SUZZONI J.P., 1988a. - - Control of brood male product ion in the Argentine Ant Iridomyrmex humilis (Mayr). Insectes Soc., 35, 19-33.

PASSERA L., KELLER L., SUZZONI J.P., 1988b. - - Queen replacement in dequeened colonies of the Argentine Ant Iridomyrmex humilis (Mayr). Psyche, 95, 59-65.

PEACOCK A.D., BAXTER A.T., 1950. - - Studies in Pharaoh's ant, Monomorium pharaonis (L.). 3. Life history. Entomol. Mort. Mag., 86, t71-178.

PWrERSEN-BRhuN M., 1975. - - Untersuchungen zur Sozialen Organization der Pharaoameise Monomarium pharaonis (L.) (Hymenoptera, Formicidae). 1. Der Brutzyklus und seine Steurung dutch Populationseigene Faktoren. Insectes Soc., 22, 269-292.

PLATEAUX L., 1986. - - Comparaison des cycles saisonniers, des dur6es des socidtds et des product ions des tro~s esp6ces de fourmis Leptothorax (Myrafant) du groupe nylanderi. Actes Coll. Insectes Soc., 3, 221-234.


POLDI B., 1963. - - Studi sulla fondazione dei nidi nei Formicidi. I. Tetramorium caespitum L. Syrup. gene. biolo, ital., 12, 132-199.

PRESCOTT H.W., 1973. - - Longevity of Lasius flavus (F.) (Hym. Formicidae) : a sequel , Entomol. Mort. Mag., 109, 124.

ROSEN6RF.n R., PAMILO P., 1983. - - The evolut ion of polygyny and polydomy in m o u n d - bui ld ing Formica ants . Acta Entomol. Fenn., 42, 65-77.

TOHME G., 1975. - - Ecologie, biologie de la reproduc t ion et 6thologie de Messor ebeninu~ Forel (Hymenoptera , Formicoidea, Myrmicidae). Bull. biol. Ft. Belg., 59, 171-251.

TOHME G., TOHME H., 1978. - - Accro issement de la socidtd et longdvitd de la reine et des. ouvri6res chez Messor semirufus (Andrd) (Hym. Formicoidea). C. R. Acad. Sci.,. Paris, 286, D, 961-963.

TSCHINKEL W.R., 1987. ~ Fire an t queen longevity and age es t imat ion by spe rm deplet ion. Ann. Entomol. Soc. Arru, 80, 263-266.

WALO~ N., 1957. - - The effect of the n u m b e r of the queens of the an t Lasius flavus (Fab.), (Hym. Formicidae) on thei r survival and on the ra te of development in the f i r s t brood. Insectes Soc., 4, 391-408.

WILSON E.O., 1974. - - The popula t ion consequences of polygyny in the an t Leptothora_v curvispinosus. Ann. Entomol. Soc. Am., 67, 782-786.

Wood L.A., TSCHINKEL R., ,1981. - - Quant i f icat ion and modif ica t ion of worker size var ia t ion in the fire an t Solenopsis invicta. Insectes Soc., 28, 117-128.

fecundity of ant queens in relation to their age and the mode of colony founding

Documents