Chapitre 3 The importance of the queen's body size on reproductive success in bumblebee field colonies.

Résumé

Les reines bourdons plus grandes que les autres peuvent possiblement être avantagées par une meilleure survie, fécondité, efficience de butinage, thermorégulation, dominance et capacité à repousser les usurpatrices. Nous avons donc testé l’hypothèse que les plus grandes reines devraient avoir un succès reproducteur plus élevé au sein de leur espèce, ceci en suivant le développement de 185 colonies de huit espèces de Bombus ( B. impatiens, B. fervidus, B. perplexus, B. terricola, B. bimaculatus, B. ternarius, B. rufocinctus et B. vagans vagans ) sur le terrain, dans la région de Québec, en 1999 et 2000. Nos résultats ont confirmé que les plus grandes reines avaient plus de chances de se reproduire et, parmi celles qui y sont parvenues, le nombre de sexués produits était positivement relié à la taille de la reine. Le meilleur succès des plus grandes reines est attribuable, du moins en partie, à la production de plus grosses colonies et, chez certaines espèces, à la capacité à mieux repousser les usurpations de Psithyrus (un sous-genre de bourdons parasites). Le meilleur succès des plus grandes reines n’était pas relié à la date de nidification ou à l’usurpation par d’autres reines Bombus , basé sur des données de colonies fondées naturellement par la reine en milieu naturel. Les reines ne gagnaient pas plus souvent les combats contre les usurpatrices Bombus en étant plus grandes que ces dernières que lorsqu’elles étaient plus petites. D’autres études seront nécessaires pour mieux comprendre les mécanismes sous-jacents, incluant l’effet de la taille de la reine sur le taux de croissance de la colonie et sur la dominance exercée sur les ouvrières.

Abstract

Bumblebee queens may benefit from being larger by increased survival, fecundity, foraging efficiency, and better thermoregulation, dominance, and ability to fight usurpers. We tested the hypothesis that, within a given species, larger queens should have a greater reproductive success by following the development of 185 field colonies of eight Bombus species ( B. impatiens, B. fervidus, B. perplexus, B. terricola, B. bimaculatus, B. ternarius, B. rufocinctus , and B. vagans vagans ) in the Quebec City area, in 1999 and 2000. We confirmed that larger foundress queens were more likely to reproduce, and, for queens that did so, there was a positive relationship between their body size and the number of sexuals produced. The higher success of larger queens is, at least in part, attributable to the production of larger colonies and, in some species, to the ability to prevent usurpations by Psithyrus (a parasitic subgenus of bumblebees). The higher success of larger queens was not related to the date of nest establishment or to usurpations by other Bombus queens, based on data from naturally established colonies. With regard to one-on-one fights with Bombus usurpers, size differences did not affect the outcome of fights from the resident queens' perspective. Additional research is required to obtain a clearer understanding of the mechanisms involved, including the effect of queen size on the growth rates of colonies and dominance over workers.

Introduction

Insect body size continues to be one of the most important morphological traits studied from an evolutionary perspective because of its strong association with many fitness characters such as fecundity, mating, and survival. More than often, studies show that a large body size is beneficial to the individual. Within a species, large females are generally more fecund (Honek 1993; del Castillo et al. 1999; Sokolovska et al. 2000) and large males often have an increased mating success (Abell et al. 1999; del Castillo et al. 1999; Starks & Reeve 1999; Sokolovska et al. 2000; Andersen & McNeil 2001; Coelho & Holliday 2001; Jamieson 2002). Furthermore, mating is often assortative with respect to body size (del Castillo et al. 1999; Harari et al. 1999), so large males can increase their fitness by mating with the larger, more fecund females. In addition, large individuals often have a higher survival, sometimes as a result of size-selected predation (Rhainds et al. 1999; Van Dongen et al. 1999; Sokolovska et al. 2000).

In social insects, there is usually an important size dimorphism between the female reproductives (queens) and non-reproductives (workers), with queens being the largest individual in a colony (Hölldobler and Wilson 1990; Michener 2000). Even among queens large size may confer reproductive advantages. In polygynous colonies of various social Hymenoptera, large size may help establish dominance (refs in Cameron & Jost 1998; Richards & Packer 1998; Keeping 2000) and increase survival (Bernasconi & Keller 1998). An extreme case of size advantage is found in some species of ants where two distinct sizes of queen exist, with the smaller queens (microgynes) having a markedly reduced reproductive capacity and dispersal ability compared with the larger ones (macrogynes) (Lachaud et al. 1999). However, evidence for a queen size advantage in social insects is still rare and relate mostly to polygynous situations.

Primitively eusocial bumblebees are monogynous in temperate regions, and size may affect the reproductive success of queens in several ways. Queens are usually produced at the end of the summer, mate, overwinter in the ground, and emerge the following spring to establish a colony. At this stage, larger queens are already advantaged by a higher incidence of winter survival (Owen 1988; Sutcliffe and Plowright 1988). They may also have greater fat reserves upon emergence in spring, and a superior physical condition at this time may help them acquire the best available nesting sites.

In the first weeks of colony development, the queen must forage and care for her initial brood. This is a critical period as she assumes all duties at a time of the year where conditions are often suboptimal. Extrapolating from general information on bumblebee foragers, one may expect larger queens to provide more food to the nest and/or more efficiently by (i) collecting larger loads and, therefore spend relatively more time actually foraging and less in transit to and from the nest (Heinrich & Heinrich 1983), (ii) having access to nectar from deeper flowers due to their longer proboscis (Medler 1962; Heinrich 1976, 1979; Harder 1982), (iii) ingesting nectar faster (Harder 1983, 1986), (iv) being able to gather food even during cool and windy weather, in part due to more effective thermoregulation (Heinrich 1979; Heinrich & Heinrich 1983; Bishop and Armbruster 1999 for bees in general), and (v) being able to competitively displace smaller bees at nectar- and pollen-rich flowers (Morse 1982 and refs therein). Increased food provisioning, and possibly increased brood incubation, should increase larval growth rates (see Plowright and Pendrel 1977), ensuring the earlier emergence of workers to assist the queen.

Early colony development is also a critical period as many other bumblebee queens may then try to usurp the foundress queen instead of founding their own colony. Usurpation by other Bombus queens and by Psithyrus (a subgenus of bumblebees specializing in this strategy) is common (Hobbs 1965, 1966a,b, 1967, 1968; Richards 1978), and, when successful, jeopardizes the reproductive success of the foundress queen (Richards 1994). Larger foundress queens may be more apt at defending the colony against usurpers, as seen in dominance conflicts of polygynous colonies of certain social Hymenoptera (see references above).

In the subsequent growth phase of the colony, there is an exponential increase in worker numbers, and colonies of larger queens may grow faster if fecundity is a limiting factor and if, as for many insects (see references above), fecundity is positively related to size. During this period, the queen must also maintain dominance over workers, accomplished through pheromones and aggressive behaviour (Bloch and Hefetz 1999). Large queen body size may be helpful in these physical interactions, as in small queenless colonies large workers are more successful in gaining dominance (Van Doorn 1989). Once the colony switches from worker to sexual production, prolonged dominance by the queen could lengthen colony life and extend the period of gyne production by preventing or delaying egg laying by workers. If queen body size positively affects at least some of the factors mentioned above, then one may expect larger queens to have a higher reproductive success.

The primary goal of this study was to determine if, at the intraspecific level, the body size of foundress queens affected the reproductive success of bumblebee species under field conditions. We then explored some of the possible associations between body size and reproductive success by determining if larger foudresses i) started colonies sooner, ii) produced larger colonies (and this at a faster rate of development), and iii) were less susceptible to usurpations by Psithyrus and other Bombus queens.

Methods

Colonies

We followed the development of 185 bumblebee field colonies in the Quebec City area, Canada, in 1999 and 2000, consisting of (number of colonies, species code): B. bimaculatus (5, BIM), B. fervidus (34, FER), B. impatiens (45, IMP), B. perplexus (29, PER), B. rufocinctus (10, RUF), B. ternarius (33, TRN), B. terricola (19, TRC), and B. vagans vagans (10, VAG). Most B. impatiens , B. ternarius , and B. terricola were from laboratory colonies established using queens caught in the spring, and transferred to the field when the first brood of workers began emerging (about seven workers). All other colonies were naturally established by queens in above-ground nesting boxes in 2000. We marked each queen (foundresses and usurpers) with a coloured, numbered tag (Operlith®) on the thorax. We censused colonies every 12-15 days, and counted the numbers of workers, gynes, and males. We marked sexuals on the thorax with correction fluid (Liquid Paper®) to prevent double counting, and left them in the colony. We estimated the reproductive success of a colony, RS , using RS = M + bG , where M = number of males, G = number of gynes (young queens), and b = 3, a coefficient of differential per capita investment between the two sexes (see Beekman & van Stratum 1998). The maximal colony size (number of workers), Wmax , was used as an index of colony development.

For colonies established naturally, we estimated the date of nest establishment retroactively, by assessing the level of brood development upon discovery of a colony in a nest box, and by allowing 1 d for the build-up of the first wax cell, 5 d for egg hatch, and up to 10 d based on the degree of larval development.

Body size measurements

Queens were held steady in a clear sandwich plastic bag (without anasthesizing or chilling them to prevent deleterious effects, see Kukuk et al. 1997) and measured with an electronic caliper (precision of instrument = ± 0.01 mm, but reproducibility = ± 0.1 mm). Due to wear, absolute wing length could not always be obtained. Therefore, as an estimate of body size we measured the length from the anterior end of the tegula (the point of articulation with the thorax) to the distal end of the median cell, at the junction of the basal and costal veins on the right forewing. The advantage of these two points is that the tip of a caliper can be slightly pressed on the tegula, and that the basal vein is thick and visible. There was a strong correlation between the mid and total lengths of the forewing (Pearson’s r = 0.92, P < 0.0001, n = 216 queens). Thirty-four of 298 queens could never be measured.

Statistical analyses

Only colonies that had not been subjected to major disturbances (e.g., by floods, theft, vandalism, predation, abandoned by the queen during the early stage of colony development) during the period of interest were included in analyses; for example, a colony that was flooded in late summer could be used for an analysis on early colony development but was obviously excluded from the analysis on reproductive success. We only used foundresses of naturally established colonies to test if body size influenced (i) the time of establishment (ii) the rate of growth of colonies, using only those that were not usurped, and (iii) the probability of being usurped by other Bombus queens, as this occurs early in colony development. We used all colonies to determine whether the foundress body size affected i) the probability of being usurped by Psithyrus, as this occurred later in overall colony development, and ii) the maximum size of colonies, using only those that were not usurped. To determine if the difference of size between resident and usurper Bombus queens affected the outcome of usurpation encounters, we only used those in which one queen survived and the outcome was not affected by other Bombus or Psithyrus usurpers. We considered two queens to differ in size only when their forewing measurements differed by > 0.2 mm.

Since colonies grow exponentially (at least in the ergonomic part of colony development), we modelled colony growth over the first 65 days with the one-parameter exponiential model p = e kt , where p = number of pupae (pupae of gynes are given a weight of 3 compared to pupae of workers and males, see Beekman & van Stratum 1998), k = constant of growth, and t = time in days since nest establishment. We estimated k by using the regression wizard of SigmaPlot 2000 ver 6.00 (SPSS Inc. 2000). It should be noted that modeling the growth of the colony using the number of pupae provides similar results to using the mass of the brood (e.g., strong correlation between values of k , n = 7 colonies of B. fervidus , Pearson’s r = 0.98, P < 0.0001,). We conducted all of the other statistical analyses using SAS for Windows, version 8.0 (SAS Institute Inc. 1999). For logistic models, we used the logit link function. We started with the models including all main effects and, if significant, added interactions significant at α = 0.15. Most interactions in logistic regressions could not be tested because they caused quasicomplete separation of data (no frequency counts in some cells). In the general linear models, we transformed the values of reproductive successes and maximal colony sizes by the square-root to comply with assumptions of homoscedasticity. All analyses contained species as an obligatory factor to account for the inherent interspecific body size differences, and we required a minimum of three valid colonies to include a species in an analysis. All trends presented are at the intraspecific level, unless noted otherwise. Tests on the effect of body size were unilateral, whereas tests for all other effects were bilateral.

Results

When examining the outcome of usurpation fights between pairs of Bombus queens, there was no indication that resident queens benefited from being larger than usurpers as resident queens had about the same probability of winning the combat (57 – 67%), independently of size differences between the two protagonists (Table 6).

Discussion

Our results demonstrate the intraspecific importance of the body size of foundress Bombus queens on their reproductive success under field conditions (Figures 1 and 2, Tables 2 and 3). The effect was clear despite the large variability caused by many other important factors, such as ecto- and endo-parasites (Müller & Schmid-Hempel 1992; Imhoof & Schmid-Hempel 1999), brood parasites, usurpations, food availability (Schmid-Hempel & Schmid-Hempel 1998; Goulson et al. 2002; Pelletier & McNeil, in press), microclimate, and predation. Thus, queen body size may explain part of the variability in reproductive success observed among laboratory colonies, reared with ample food and in the absence of enemies (e.g., Duchateau & Velthuis 1988; Müller et al. 1992; Beekman & van Stratum 1998).

The higher success of larger queens can be related to the fact they developed larger colonies (Figure 4, Table 4). A larger worker force may benefit colonies by increasing food provisioning, the quality of brood care, and thermoregulatory capabilities of the nest during the production of sexuals; and by lengthening the duration of sexual production. Furthermore, a larger number of workers provides a better protection against Psithyrus usurpations (Fisher 1984, 1985). Psithyrus usually prevent their hosts from reproducing altogether (Küpper & Schwammberger 1995 and refs therein; pers. obs.), so preventing their establishment in colonies increases the chances of colony success. It should be noted that a larger maximal colony size cannot confer a better protection against Bombus usurpers because these usurpations usually occur in the early stage of colony development, before the emergence of the first workers. Finally, a larger colony size may increase protection against some brood parasites, but this remains to be explored.

How can larger queens obtain larger colonies, and thus ensure higher success? First, larger queens may nest earlier to increase the length of colony ergonomic development, but this was not the case in the present study (Figure 3, Table 4). Furthermore, regardless of body size, we found no evidence that nesting earlier increased reproductive success. If nesting earlier was beneficial, then one would expect nest establishment to occur over a brief period, as in subarctic species where the summer is short (see Vogt et al. 1994). However, not only do temperate species establish nest over many weeks (Richards 1978; pers. observ.), but certain species such as B. fervidus do not start until June (pers. obs.). Hence, other factors, such as finding a suitable nest site close to abundant food, may be of greater importance for temperate species than nesting as early as possible.

Second, larger queens may delay the onset of sexual production to increase the length of colony ergonomic development. However, this strategy seems unlikely as a delay could (i) increase the risks of colony failure because brood parasites such as wax moths ( Vitula edmandsae in North America and Aphomia sociella in Europe) can destroy the whole comb in late summer, and (ii) the late emergence of sexuals could decrease their probability of finding suitable mates. While our census schedule did not permit us to determine the precise moment when sexual production occurred, there does appear to be selection against extending ergonomic colony development in our area as most species (except B. impatiens ) begin producing sexuals well before the end of summer (Macfarlane et al. 1994; pers. obs.).

Third, colonies of larger queens may develop faster. Fast rates of colony development are useful, and even a necessity, where summers are very short (e.g., in the Arctic), but the importance of maintaining a fast rate of development decreases with warmer temperatures and longer summers (Laverty & Plowright 1985). This does not mean that a relationship between queen body sizes and rates of colony development do not exist in temperate areas, such as in our study site, but this remains to be verified with larger sample sizes of naturally-established colonies.

Fourth, larger queens may be able to dominate workers longer; thereby preventing or retarding selfish behaviour from workers (e.g., oophagy, egg laying, matricide; see Bourke 1994; Bloch 1999; Bloch & Hefetz 1999; Bourke 2001). This issue also remains to be explored.

Queens did not benefit from being larger than Bombus usurpers in usurpation fights (Table 6). This is in opposition to suggestions currently in the literature (Plowright & Laverty 1984; Owen 1988; Sutcliffe & Plowright 1988), which are based on data in which the status (resident or usurper) of competitors was unknown (Richards 1978). Our finding is similar to that reported on the outcome of dominance contests during temporary polygynous phases in B. atratus , a Neotropical bumblebee (Cameron & Jost 1998). Other factors must, thus, determine the outcome of such fights. In the sweat bee Lasioglossum figueresis , it is the level of ovarian development rather than body size that appears to determine the outcome of encounters between reproductively active females (Wcislo 1997).

We have provided evidence that body size significantly affects the reproductive success of queens of many species of bumblebees under field conditions. Additional research is required to obtain a clearer understanding of the mechanisms involved, including the effect of queen size on the growth rates of colonies and dominance over workers. Another challenge will be to explain, especially with regard to life history strategies, what makes queens of species such as B. vagans vagans successful despite their smaller size. Finally, since larger queens have a higher reproductive potential and that their body size appears to be determined by the amount of food received during larval growth (Plowright & Jay 1977; Sutcliffe & Plowright 1988, 1990), there should be a colony trade-off, depending on prevailing ecological conditions, between producing a large number of smaller gynes and a smaller number of larger gynes with greater reproductive potential. This colony trade-off to balance the costs and benefits of gyne production also merits further attention.

Acknowledgements

We thank E. Plamondon, Dr. M. Roy, J. Duchesneau, A. Labrecque, J. Senécal, and A. Bélanger for technical assistance; J. Gervais (APIPOL) and M. Hardy for advise on rearing; F. Boulay (Société Immobilière Irving) for permission to work on private land, and Dr. J. Régnière for comments on the manuscript. This project was funded by a FCAR graduate scholarship to L. P. and by a NSERC research grant to J. N. M.

References

Abell, A.J., Cole, B.J., Reyes, R., and Wiernasz, D.C. 1999. Sexual selection on body size and shape in the western harvester ant, Pogonomyrmex occidentalis Cresson. Evolution 53: 535-545.

Andersen, A. and McNeil, J.N. 2001. Size influences male mating success in the alfalfa blotch leafminer (Diptera: Agromyzidae). Canadian Entomologist 133: 717-719.

Beekman, M. and van Stratum, P. 1998. Bumblebee sex ratios: why do bumblebees produce so many males? Proceedings of the Royal Society of London 265: 1535-1543.

Bernasconi, G. and Keller, L. 1998. Phenotype and individual investment in cooperative foundress associations of the fire ant, Solenopsis invicta. Behavioral Ecology 9: 478-485.

Bishop, J.A. and Armbruster, W.S. 1999. Thermoregulatory abilities of Alaskan bees: Effects of size, phylogeny and ecology. Functional Ecology 13: 711-724.

Bloch, G. 1999. Regulation of queen-worker conflict in bumble-bee ( Bombus terrestris ) colonies. Proceedings of the Royal Society of London B 266: 2465-2469.

Bloch, G. and Hefez, A. 1999. Regulation of reproduction by dominant workers in bumblebee ( Bombus terrestris ) queenright colonies. Behavioral Ecology and Sociobiology 45: 125-135.

Bourke, A.F.G. 1994. Worker matricide in social bees and wasps. Journal of Theoretical Biology 167: 283-192.

Bourke, A.F.G. and Ratnieks, F.L.W. 2001. Kin-selected conflict in the bumble-bee Bombus terrestris (Hymenoptera: Apidae). Proceedings of the Royal Society Biological Sciences Series B 268: 347-355.

Cameron, S.A. and Jost, M.C. 1998. Mediators of dominance and reproductive success among queens in the cyclically polygynous Neotropical bumble bee Bombus atratus Franklin. Insectes Sociaux 45: 135-149.

Cnaani, J., Robinson, G.E., Bloch, G., Borst, D., and Hefetz, A. 2000. The effect of queen-worker conflict on caste determination in the bumblebee Bombus terrestris. Behavioural Ecology and Sociobiology 47: 3467-352.

Coelho, J.R. and Holliday, C.W. 2001. Effects of size and flight performance on intermale mate competition in the cicada killer, Sphecius speciosus Drury (Hymenoptera: Sphecidae) . Journal of Insect Behavior 14: 345-351.

del Castillo, R.C., Nunez, F.J., and Cano, S.Z. 1999. The role of body size in mating success of Sphenarium purpurascens in Central Mexico. Ecological Entomology 24: 146-155.

Duchateau, M.J. and Velthuis, H.H.W. 1988. Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107: 186-207.

Fisher, R.M. 1984. Evolution and host specificity: a study of the invasion success of a specialized bumble bee social parasite. Canadian Journal of Zoology 62: 1641-1644.

Fisher, R.M. 1985. Evolution and host specificity: dichotomous invasion success of Psithyrus citrinus (Hymenoptera: Apidae), a bumble bee social parasite in colonies of its two hosts. Canadian Journal of Zoology 63: 977-981.

Goulson, D., Hughes, W.O.H., Derwent, L.C., and Stout, J.C. 2002. Colony growth of the bumblebee, Bombus terrestris , in improved and conventional agricultural and suburban habitats . Oecologia 130: 267-273.

Harari, A.R., Handler, A.M., and Landolt, P.J. 1999. Size-assortative mating, male choice and female choice in the curculionid beetle Diaprepes abbreviatus . Animal Behaviour 58: 1191-1200.

Harder, L.D. 1982. Measurement and estimation of functional proboscis length in bumblebees (Hymenoptera: Apidae). Canadian Journal of Zoology 60: 1073-1079.

Harder, L.D. 1983. Functional differences of the proboscides of short- and long-tongued bees (Hymenoptera: Apidae). Canadian Journal of Zoology 61: 1580-1586.

Harder, L.D. 1986. Effects of nectar concentration and flower depth on flower handling efficiency of bumble bees. Oecologia 69: 309-315.

Heinrich, B. 1976. The foraging specializations of individual bumblebees. Ecological Monographs 46: 105-128.

Heinrich, B. 1979. Bumblebee economics. Harvard University Press, Cambridge, Massachusetts.

Heinrich, B. and Heinrich, M.J.E. 1983. Size and caste in temperature regulation by bumblebees. Physiological Zoology 56: 552-562.

Hobbs, G.A. 1965. Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. II. Subgenus Bombias Robt. Canadian Entomologist 97: 120-128.

Hobbs, G.A. 1966a. Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. IV. Subgenus Fervidobombus Skorikov. Canadian Entomologist 98: 33-39.

Hobbs, G.A. 1966b. Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. V. Subgenus Subterraneobombus Vogt. Canadian Entomologist 98: 288-294.

Hobbs, G.A. 1967. Ecology of species of Bombus (Hymenoptera: Apidae) in southern Alberta. VI. Subgenus Pyrobombus . Canadian Entomologist 99: 1271-1292.

Hobbs, G.A. 1968. Ecology of species of Bombus Latr. (Hymenoptera: Apidae) in southern Alberta. VII. Subgenus Bombus . Canadian Entomologist 100: 156-164.

Hölldobler, B. and Wilson, E.O. 1990. The ants. The Belknap Press of Harvard University Press, Cambridge, Massachusetts.

Honek, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66: 483-492.

Imhoof, B. and Schmid-Hempel, P. 1999. Colony success of the bumble bee, Bombus terrestris , in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi . Insectes Sociaux 46: 233-238.

Jamieson, I.G. 2002. The relationship between male head size and harem size in the sexually dimorphic mountain stone weta Hemideina maori . Ecological Entomology 27: 41-48.

Keeping, M.G. 2000. Morpho-physiological variability and differentiation of reproductive roles among foundresses of the primitively eusocial wasp, Belonogaster petiolata (Degeer) (Hymenoptera, Vespidae). Insectes Sociaux 47: 147-154.

Kukuk, P.F., Kilgore, D.L., and Frappell, P.B. 1997. Larval ejection behavior in Bombus occidentalis in response to CO2- or N2-induced narcosis. Journal of the Kansas Entomological Society 70: 359-361.

Küpper, G. and Schwammberger, K.H. 1995. Social parasitism in bumble bees (Hymenoptera, Apidae): Observations of Psithyrus sylvestris in Bombus pratorum nests. Apidologie 26: 245-254.

Lachaud, J.P., Cadena, A., Schatz, B., Perez-Lachaud, G., and Ibarra-Nunez, G. 1999. Queen dimorphism and reproductive capacity in the ponerine ant, Ectatomma ruidum Roger. Oecologia 120: 515-523.

Laverty, T.M. and Plowright, R.C. 1985. Comparative bionomics of temperate and tropical bumble bees with special reference to Bombus ephippiatus (Hymenoptera: Apidae). Canadian Entomologist 117: 467-474.

Macfarlane, R.P., Patten, K.D., Royce, L.A., Wyatt, B.K.W., and Mayer, D.F. 1994. Management potential of sixteen North American bumble bee species. Melanderia 50: 1-12.

Medler, J.T. 1962. Morphometric studies on bumble bees. Annals of the Entomological Society of America 55: 212-218.

Michener, C.D. 2000. The bees of the world. Johns Hopkins University, Baltimore, MD.

Morse, D.H. 1982. Foraging relationships within a guild of bumble bees. Insectes Sociaux 29: 445-454.

Müller, C.B. and Schmid-Hempel, P. 1992. Correlates of reproductive success among field colonies of Bombus lucorum : the importance of growth and parasites. Ecological Entomology 17: 343-353.

Müller, C.B., Shykoff, J.A., and Sutcliffe, G.H. 1992. Life history patterns and opportunities for queen-worker conflict in bumblebees (Hymenoptera: Apidae). Oikos 65: 242-248.

Owen, R.E. 1988. Body size variation and optimal body size of bumble bee queens (Hymenoptera: Apidae). Canadian Entomologist 120: 19-27.

Pelletier, L. and McNeil, J.N. The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos (in press).

Plowright, R.C. and Jay, S.C. 1977. On the size determination of bumble bee castes (Hymenoptera: Apidae). Canadian Journal of Zoology 55: 1133-1138.

Plowright, R.C. and Laverty, T.M. 1984. The ecology and sociobiology of bumble bees. Annual Review of Entomology 29: 175-199.

Plowright, R.C. and Pendrel, B.A. 1977. Larval growth in bumble bees (Hymenoptera: Apidae). Canadian Entomologist 109: 967-973.

Rhainds, M., Gries, G., and Min, M.M. 1999. Size- and density-dependent reproductive success of bagworms, Metisa plana . Entomologia Experimentalis et Applicata 91: 375-383.

Richards, K.W. 1978. Nest site selection by bumble bees (Hymenoptera: Apidae) in southern Alberta. Canadian Entomologist 110: 301-318.

Richards, K.W. 1994. Ovarian development, ovariole number, and relationship to body size in Psithyrus spp. (Hymenoptera: Apidae) in southern Alberta. Journal of the Kansas Entomological Society 67: 156-168.

Richards, M.H. and Packer, L. 1998. Demography and relatedness in multiple-foundress nests of the social sweat bee, Halictus ligatus. Insectes Sociaux 45: 97-109.

SAS Institute Inc. 1999. The SAS system for Windows, ver 8.0. Cary, North Carolina.

Schmid-Hempel, R. and Schmid-Hempel, P. 1998. Colony performance and immunocompetence of a social insect, Bombus terrestris , in poor and variable environments. Functional Ecology 12: 22-30.

Sokolovska, N., Rowe, L., and Johansson, F. 2000. Fitness and body size in mature odonates. Ecological Entomology 25: 239-248.

SPSS Inc. 2000. SigmaPlot 2000 for Windows, ver 6.00.

Starks, P.T. and Reeve, H.K. 1999. Condition-based alternative reproductive tactics in the wool-carder bee, Anthidium manicatum . Ethology Ecology and Evolution 11: 71-75.

Sutcliffe, G.H. and Plowright, R.C. 1988. The effects of food supply on adult size in the bumble bee Bombus terricola Kirby (Hymenoptera: Apidae). Canadian Entomologist 120: 1051-1058.

Sutcliffe, G.H. and Plowright, R.C. 1990. The effects of pollen availability on development time in the bumble bee Bombus terricola K. (Hymenoptera: Apidae). Canadian Journal of Zoology 68: 1120-1123.

Van Dongen, S., Sprengers, E., Lofstedt, C., and Matthysen, E. 1999. Fitness components of male and female winter moths ( Operophtera brumata L.) relative to measures of body size and asymmetry. Behavioral Ecology 10: 659-665.

Van Doorn, A. 1989. Factors influencing dominance behaviour in queenless bumblebee workers ( Bombus terrestris ). Physiological Entomology 14: 211-221.

Vogt, F.D., Heinrich, B., Dabolt, T.O., and McBath, H.L. 1994. Ovary development and colony founding in subarctic and temperate-zone bumblebee queens. Canadian Journal of Zoology 72: 1551-1556.

Wcislo, W.T. 1997. Social interactions and behavioral context in a largely solitary bee, Lasioglossum (Dialictus) figueresis (Hymenoptera, Halictidae). Insectes Sociaux 44: 199-208.

Table 3.1 Queen body size (mid-length of the fore wing in mm; mean ± variance, range) of eight Bombus species in the Quebec City area in 1999 and 2000, for foundresses of naturally established colonies, usurpers, and the pool of all queens (including foundresses of laboratory established colonies and queens whose role (foundress or usurper) was not established).

Species	Foundresses of naturally established colonies					Usurper queens					All queens
	n	mean	var	min	max	n	mean	var	min	max	n	mean	var	min	max
B. impatiens	2	10.2	0.1	10.0	10.3	11	10.0	0.2	9.3	10.6	57	10.1	0.2	8.9	10.8	A
B. fervidus	28	9.6	0.1	8.7	10.4	37	9.7	0.1	8.9	10.5	73	9.7	0.1	8.7	10.5	B
B. perplexus	26	9.3	0.4	7.1	10.4	11	9.6	0.4	8.6	10.2	46	9.3	0.4	7.1	10.4	C
B. terricola	1	9.0				1	8.2				14	8.9	0.3	7.8	9.8	D
B. bimaculatus	4	8.8	0.5	7.8	9.4						7	8.6	0.3	7.8	9.4	D	E
B. ternarius											27	8.4	0.1	7.7	9.1		E
B. rufocinctus	13	8.4	0.1	7.8	8.7	7	8.2	0.1	7.8	8.7	22	8.3	0.1	7.6	8.7		E
B. vagans vagans	11	7.8	0.7	6.0	8.6	2	7.4	1.6	6.5	8.3	14	7.8	0.7	6.0	8.6	F

Species with the same letter are not significantly different (least-squares means, Tukey-Kramer adjustment, α = 0.05).

Table 3.2 Logistic regression testing for the effect of foundress Bombus queen body size (mid-length of the fore wing) on the probability of producing sexuals (n = 100; all eight species).

Source	χ2	df	P
Model	15.08	8	0.029
Species	12.25	7	0.093
Body size	5.90	1	0.008

Table 3.3 ANCOVA testing for the effect of Bombus queen body size (mid-length of fore wing) on the index of reproductive success for foundress queens that successfully produced sexuals (n = 56 ; species: FER, IMP, PER, RUF, TRN, TRC), r2 = 0.33. The interaction was not kept in the final model because P > 0.50.

Source	F	df	P
Model	4.08	6, 49	0.0021
Species	4.47	5, 49	0.0019
Body size	5.45	1, 49	0.012

Table 3.4 ANCOVAs testing for the effect of the foundress Bombus queen body size on the timing of nest establishment (n = 68; species: BIM, FER, PER, RUF, VAG), r2 = 0.58, and maximal colony size (n = 88; all eight species), r2 = 0.23. The interactions were not kept in the final model because P > 0.50.

Parameter	Source	F	df	P
Nest establishment	Model	17.20	5, 62	< 0.0001
	Species	19.56	4, 62	< 0.0001
	Body size	1.39	1, 62	0.12 a

Maximal colony size	Model	2.98	8, 79	0.0057
	Species	2.97	7, 79	0.0081
	Body size	4.26	1, 79	0.021

a Power = 0.318, more than 200 queens would be required to obtain a power of 0.60

Table 3.5 Logistic regressions testing for the effect of Bombus queen body size (mid-length of the fore wing) on the incidence of usurpations by other Bombus queens (n = 50 contests; host species: FER, PER, RUF, VAG), or Psithyrus females (n = 49 contests; host species: IMP, TRN, TRC).

Usurper subgenus	Source	χ2	df	P
Bombus	Model	4.86	4	0.30
	Host species	1.85	5	0.60
	Body size	0.48	1	0.25

Psithyrus	Model	5.85	3	0.12
	Host species	4.87	2	0.09
	Body size	2.27	1	0.07

Table 3.6 Observed probabilities of winning a usurpation contest for resident Bombus queens when fighting against another Bombus queen, by differences of size between the resident and usurper queens. A queen is considered larger when the mid-length of the fore wing is longer by more than 0.2 mm.

	All contests	Intraspecific contests only
Resident queen larger	10/15	7/11
Same size	2/3	1/2
Resident queen smaller	8/14	6/10
Total	20/32	14/23

Legends of figures

Figure 3. 1 Positive relationship between the predicted probability of producing sexuals and the body size (mid-length of fore-wing in mm) of foundress queens for eight Bombus species (n=100) in the Quebec City area, Canada, in 1999 and 2000. The logistic regression model is presented in Table 2.

Figure 3. 2 Predicted reproductive success of foundress queens as a function of body size (mid-length of fore wing in mm) in six Bombus species that reproduced successfully (n = 59) in the Quebec City area, Canada, in 1999 and 2000. Based on the ANCOVA presented in Table 3.

Figure 3. 3 Julian date of nest establishments as a function of the body size (mid-length of fore wing in mm) of foundress queens in four Bombus species nesting in the Quebec City area, Canada, in 2000.

Figure 3. 4 Predicted maximum colony size (in number of workers) as a function of the foundress queen body size (mid-length of fore wing in mm) in eight Bombus species in the Quebec City area, Canada, in 1999 and 2000. Based on the ANCOVA presented in Table 4.


Chapitre 2 Field techniques for the study of bumblebee colonies		Chapitre 4 The effect of food supplementation on reproductive success in bumblebee field colonies.