Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective

Erhard Strohm strohm@biozentrum 0 1 Anita Bordon-Hauser 0 1 0 uni-wuerzburg. de . Received 14 December 2001; revised 16 September 2002; accepted 3 October 2002 1 Theodor-Boveri-Institut for Biosciences, University of W urzburg , Am Hubland, D-97074 W urzburg, Germany The size of the group of social species might influence basic aspects of productivity and social interactions. In many primitively social insects, foundress queens are basically in control of the number of workers in their first brood. We examined factors that might influence the optimal number of workers a queen should produce during the solitary founding phase in Lasioglossum malachurum (Hymenoptera, Halictidae). A priori, it seems plausible that she should produce as many workers as possible (1) to maximize colony productivity and (2) to minimize the impact of brood parasitoids. However, there might also be unfavorable consequences of a large colony size from the queen's perspective. First, the queen might incur disproportionately high costs that decrease her potential for subsequent reproduction. Second, the queen might not be able to suppress the development of ovaries in a large number of workers. As a clear advantage of a large colony size, we found an increased production of sexuals. Contrary to our expectation, in the first worker phase, nests that were parasitized by Sphecodes bees had more workers than did unparasitized nests. We found no evidence that the production of the first worker brood entailed costs to the queen. However, the degree of development of worker ovaries increased with colony size, and some degree of development was detectable with as few as four workers. This study shows that the number of workers a queen produces might depend on the interaction of several factors, some of which have not been considered in detail yet. Key words: cost of reproduction, group size, ovarian development, parasitism, productivity, trade-off. [Behav Ecol 14:546-553 (2003)] - T factors affecting the success of group members on any he size of a social group is one of the most important level of social organization (Emlen, 1991; Wilson, 1975). The optimal group size is hypothesized to balance opposing selection pressures (Wittenberger, 1981). This hypothesis is supported by many studies on vertebrates and social spiders (e.g., Clutton-Brock et al., 1999; Uetz and Hieber, 1997; Wiklund and Andersson, 1994). In a social spider, large group size has a positive effect on mean offspring survival but a negative effect on the incidence of egg parasitism and on the probability that a female will reproduce at all (Aviles and Tufino, 1998). In social insects, however, the significance of group size has not received as much attention (see Crozier and Pamilo, 1996). Recently, it has been suggested that colony size per se has considerable consequences for, e.g., the conflict over reproduction, morphological skew between queens and workers, colony efficiency, complexity of social interactions, and insurance-based direct fitness benefits (Anderson and Ratnieks, 1999; Bourke, 1999; Karsai and Wenzel, 1998; Shreeves and Field, 2002). These studies examined the importance of colony size primarily across different species. However, intraspecific variation in colony size might also affect social interactions and life-history traits (Field et al., 1999, 2000), as well as colony survival (Hogendoorn and Zammit, 2001; Strassmann et al., 1988). In this study, we tested the hypothesis that colony size has an effect on aspects of social interactions and colony success in the halictid bee, Lasioglossum (Evylaeus) malachurum (Kirby 1802). Because in halictids, the number of workers in the first brood isbesides exogenous factorsunder the control of the queen, we analyzed a number of factors that might select for an increase or decrease of colony size from the queens point of view. In the eusocial species of the genus Lasioglossum, a hibernated foundress usually raises a first brood that consists of workers only. These workers provision a second brood that consists of either sexuals or new workers, in which case the brood cycle continues. In L. malachurum, as well as in some other eusocial halictids, more worker generations are produced in warmer climates (Knerer, 1992; Miyanaga et al., 1999; Richards, 2000; Sakagami and Munakata, 1972). A priori, it appears to be advantageous for the foundress to produce as many workers in the first brood as possible because this might increase the number of sexuals produced (Michener, 1990; Oster and Wilson, 1978) and reduce parasitism (Abrams and Eickwort, 1981; Lin, 1964; Wcislo, 1997a) as well as predation (Strassmann et al., 1988; but see Shakarad and Gadagkar, 1995). However, the problem of optimal colony size might not be trivial because, from the queens perspective, a large number of workers might also have negative effects. First, it has been suggested that in L. malachurum, the risk of nest usurpation by floater females during the period of solitary foraging by the queen increases with the time a foundress forages by itself. The fact that foundresses stop provisioning at a certain time and close their nests and, thus, obviously do not produce the maximum number of workers possible has been interpreted as a means to counter the risk of usurpation (Kaitala et al., 1990; Smith and Weller, 1989). Second, the production of a large number of workers might entail costs (sensu Trivers, 1972) to the queen that disproportionately reduce her ability to reproduce in the future (Cant and Johnstone, 1999). The most severe form of such costs would be dying during foraging (e.g., owing to predation; Field et al., 2000; Ward and Kukuk, 1998). Third, the queen might not be able to suppress the ovarian development of a large number of workers. This is probably the case in species in which queen control is accomplished by aggression toward workers, as in halictids (for review, see Knerer, 1992; Michener, 1990; Richards, 2000). As a consequence, workers might reproduce and some resources might be allocated to the queens grandchildren to which she is less closely related than to her own offspring. Even if workers with developed ovaries do not actually oviposit, they might allocate some resources to ovarian development (see Inglesfield and Begon, 1983; Wheeler, 1996; Wheeler and Buck, 1996) to the detriment of colony productivity. We hypothesized an increase in colony productivity, as well as a decrease in parasitism, as possible advantages of a large number of workers in the first brood and trade-offs between the production of workers and subsequent production of sexuals, as well as an incomplete suppression of ovarian development in workers as possible disadvantages in L. malachurum. One probable advantage of large colony size is the often reported increase of colony productivity with worker number (Lee and Winston, 1987; for review, see Michener, 1990; see also Shakarad and Gadagkar, 1995; Shreeves (...truncated)