Role of Propagule Size in the Success of Incipient Colonies of the Invasive Argentine Ant

Abstract: Factors that contribute to the successful establishment of invasive species are often poorly understood. Propagule size is considered a key determinant of establishment success, but experimental tests of its importance are rare. We used experimental colonies of the invasive Argentine ant (   Linepithema humile ) that differed both in worker and queen number to test how these attributes influence the survivorship and growth of incipient colonies. All propagules without workers experienced queen mortality, in contrast to only 6% of propagules with workers. In small propagules (10–1,000 workers), brood production increased with worker number but not queen number. In contrast, per capita measures of colony growth decreased with worker number over these colony sizes. In larger propagules ( 1,000–11,000 workers), brood production also increased with increasing worker number, but per capita brood production appeared independent of colony size. Our results suggest that queens need workers to establish successfully but that propagules with as few as 10 workers can grow quickly. Given the requirements for propagule success in Argentine ants, it is not surprising how easily they spread via human commerce.     

Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality

Behavior in eusocial insects likely reflects a long history of selection imposed by parasites and pathogens because the conditions of group living often favor the transmission of infection among nestmates. Yet, relatively few studies have quantified the effects of parasites on both the level of individual colony members and of colony success, making it difficult to assess the relative importance of different parasites to the behavioral ecology of their social insect hosts. Colonies of Polybia occidentalis, a Neotropical social wasp, are commonly infected by gregarines (Phylum Apicomplexa; Order Eugregarinida) during the wet season in Guanacaste, Costa Rica. To determine the effect of gregarine infection on individual workers in P. occidentalis, we measured foraging rates of marked wasps from colonies comprising both infected and uninfected individuals. To assess the effect of gregarines on colony success, we measured productivity and adult mortality rates in colonies with different levels of infection prevalence (proportion of adults infected). Foraging rates in marked individuals were negatively correlated with the intensity of gregarine infection. Infected colonies with high gregarine prevalence constructed nests with fewer brood cells per capita, produced less brood biomass per capita, and, surprisingly, experienced lower adult mortality rates than did uninfected or lightly infected colonies. These data strongly suggest that gregarine infection lowers foraging rates, thus reducing risk to foragers and, consequently, reducing adult mortality rates, while at the same time lowering per-capita input of materials and colony productivity. In infected colonies, queen populations were infected with a lower prevalence than were workers. Intra-colony infection prevalence decreased dramatically in the P. occidentalis population during the wet season.An erratum to this article can be found at     

Constraints on foraging success due to resource ecology limit colony productivity in social insects

The benefit of group living is a fundamental question in social evolution. For sociality to evolve, each individual must gain in terms of some fitness component by living in larger groups. However, in social insects, a decrease in per capita success in brood production has been observed in larger groups. While it has been proposed that this decrease could be outweighed by an increase in the predictability of success, a functional basis to this hypothesis has so far never been demonstrated. In this paper, using foraging economics as a functional proxy to colony productivity, we construct a model to explore how number of foragers in the colony interacts with the ecology of resources to influence per capita foraging success and its predictability. The results of the model show that there is no increase in per capita foraging success in larger colonies under most circumstances, though there is an increase in its predictability. We then test the model with empirical data on the foraging behavior of the primitively eusocial wasp, Ropalidia marginata. The consistency between the data and the model suggests that foraging economics could provide a robust functional basis in explaining the relationship between colony size and productivity.     

Social influences on body size and developmental time in the bumblebee Bombus terrestris

In many social insects, including bumblebees, the division of labor between workers relates to body size, but little is known about the factors influencing larval development and final size. We confirmed and extend the evidence that in the bumblebee Bombus terrestris the adult bee body size is positively correlated with colony age. We next performed cross-fostering experiments in which eggs were switched between incipient (before worker emergence) and later stage colonies with workers. The introduced eggs developed into adults similar in size to their unrelated nestmates and not to their same-age full sisters developing in their mother colony. Detailed observations revealed that brood tending by the queen decreases, but does not cease, in young colonies with workers. We next showed that both worker number and the queen presence influenced the final size of the developing brood, but only the queen influence was mediated by shortening developmental time. In colonies separated by a queen excluder, brood developmental time was shorter in the queenright compartment. These findings suggest that differences in body size are regulated by the brood interactions with the queen and workers, and not by factors inside the eggs that could vary along with colony development. Finally, we developed a model showing that the typical increase in worker number and the decrease in brood contact with the queen can account for the typical increase in body size. Similar self-organized social regulation of brood development may contribute to the optimization of growth and reproduction in additional social insects.     

Aging and demographic plasticity in response to experimental age structures in honeybees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L)

Honeybee colonies are highly integrated functional units characterized by a pronounced division of labor. Division of labor among workers is mainly age-based, with younger individuals focusing on in-hive tasks and older workers performing the more hazardous foraging activities. Thus, experimental disruption of the age composition of the worker hive population is expected to have profound consequences for colony function. Adaptive demography theory predicts that the natural hive age composition represents a colony-level adaptation and thus results in optimal hive performance. Alternatively, the hive age composition may be an epiphenomenon, resulting from individual life history optimization. We addressed these predictions by comparing individual worker longevity and brood production in hives that were composed of a single-age cohort, two distinct age cohorts, and hives that had a continuous, natural age distribution. Four experimental replicates showed that colonies with a natural age composition did not consistently have a higher life expectancy and/or brood production than the single-cohort or double-cohort hives. Instead, a complex interplay of age structure, environmental conditions, colony size, brood production, and individual mortality emerged. A general tradeoff between worker life expectancy and colony productivity was apparent, and the transition from in-hive tasks to foraging was the most significant predictor of worker lifespan irrespective of the colony age structure. We conclude that the natural age structure of honeybee hives is not a colony-level adaptation. Furthermore, our results show that honeybees exhibit pronounced demographic plasticity in addition to behavioral plasticity to react to demographic disturbances of their societies.     

Parental investment decision rules: a test in bluegill sunfish

Summary We review parental investment decision theory and provide an experimental test of the decision rule used by male bluegill sunfish (Lepomis macrochirus) in allocating parental investment to their young. The alternative decision rules tested are: (1) invest according to brood size (number) only; (2) invest according to past investment only; (3) invest according to both brood size and past investment; and (4) invest according to neither brood size nor past investment. By manipulating brood size independently of a male's cumulative investment in the brood, and by measuring each male's defensive behavior against a model predator, we found that male bluegill invest according to both brood size and past investment. This result is consistent with recent theory that past parental investment devalues adult future reproductive value, and that animals should therefore invest according to the value of their brood relative to that of their own expected future reproduction.     

Experimental analysis of worker division of labor in bumblebee nest thermoregulation (<Emphasis Type="Italic">Bombus huntii</Emphasis>, Hymenoptera: Apidae)

Bumblebee colonies experience daily and seasonal fluctuations in ambient temperature, but proper brood development requires a stable nest temperature. This study examined how adaptive colony responses to changing ambient temperature are achieved through the in-nest workers’ behavioral plasticity. We studied three Bombus huntii colonies in the laboratory. In the first experiment, we manipulated ambient temperature and recorded brood cell incubation and wing fanning by individually marked, known-age bees. The colonies maintained their nests closer to appropriate brood development temperatures (28 to 32°C) when exposed to a range of ambient temperatures from 10.3 to 38.6°C. Incubation activity was greater in cooler treatment conditions, whereas in the highest temperature treatment, some bees fanned and others moved off the brood. As the ambient temperature dropped, workers increased the duration of their incubating bouts, but, except at the highest temperature, the number of workers that incubated did not differ significantly among treatments. A subset of the bees incubated significantly more than their nest mates, some of which never incubated. Worker body size, but not age, was a good predictor of incubation rates, and smaller bees incubated at higher rates. In the second experiment, we removed the most actively incubating workers. Immediately after removals, the total colony incubation effort was lower than pre-removal levels, but incubation effort rebounded toward pre-removal levels after 24 h. The increased thermoregulatory demand after removals was met primarily by bees increasing their rates of incubation rather than by bees switching from a different task to incubation. We conclude that some B. huntii workers specialize on nest thermoregulation, and that changes in work rates are more important than task switching in meeting thermal challenges.     

Assured fitness returns favor sociality in a mass-provisioning sweat bee,Megalopta genalis (Hymenoptera: Halictidae)

Assured fitness returns models for the evolution of sociality emphasize the selective value of ensuring that offspring receive adequate parental care to reach maturity. If a member of a social group dies, it can accrue returns on investment in offspring through the efforts of surviving social partners. We provide evidence that in the mass-provisioning, facultatively social sweat bee Megalopta genalis, adult presence in the nest throughout brood development provides protection from ant predation. Nests with adults present were well protected, and brood in nests with adults removed suffered higher predation. Females in observation nests showed effective defensive behavior against experimentally introduced ants, and bees in natural nests repulsed naturally occurring ant raids. Megalopta nest architecture and behavior are such that the brood of several cooperating females can be defended with little additional cost relative to solitary nesting. The benefits of cooperative defense may favor group living in mass provisioning bees. Our observations and experiments suggest that parental care throughout brood development can be adaptive in mass provisioning species, supporting the predictions of assured fitness returns models.     

Inbreeding in a lek-mating ant species, Pogonomyrmex occidentalis

In this paper we have two goals. First, we examine the effects of sample size on the statistical power to detect a given amount of inbreeding in social insect populations. The statistical power to detect a given level of inbreeding is largely a function of the number of colonies sampled. We explore two sampling schemes, one in which a single individual per colony is sampled for different sample sizes and a second sampling scheme in which constant sampling effort is maintained (the product of the number of colonies and the number of workers per colony is constant). We find that adding additional workers to a sample from a colony makes it easier to detect inbreeding in samples from given number of colonies; however, adding more colonies rather than more workers per colony always gives greater power to detect inbreeding. Because even relatively large amounts of sib-mating generate relatively small inbreeding coefficients, detection of even substantial deviations from random mating will require very large samples. Second, we look at the amount of inbreeding in a large population of the western harvest ant, Pogonomyrmex occidentalis. We find deviations from Hardy-Weinberg equilibrium equivalent to approximately 27% sib-mating in our population ( f = 0.09). Review of past studies on the population structure of other Pogonomyrmex species suggests that inbreeding may be a regular feature of the mating system of these ants. Although P. occidentalisis a swarm-mating species, there are a number of features of its population biology which suggest that the effective population size may be small. These include topographical variation that potentially breaks the population into demes, variation in the reproductive output of colonies, and variation in the size of reproductives produced by colonies. Received: 6 May 1996 / Accepted after revision: 6 October 1996     

Why do not all workers work? Colony size and workload during emigrations in the ant Temnothorax albipennis

Here, we study distribution of workload and its relationship to colony size among worker ants of Temnothorax albipennis, in the context of colony emigrations. We find that one major aspect of workload, number of items transported by each worker, was more evenly distributed in larger colonies. By contrast, in small colonies, a small number of individuals perform most of the work in this task (in one colony, a single ant transported 57% of all items moved in the emigration). Transporters in small colonies carried more items to the new nest per individual and achieved a higher overall efficiency in transport (more items moved per transporter and unit time). Our results suggest that small colonies may be extremely dependent on a few key individuals. In studying colony organisation and division of labour, the amount of work performed by each individual, not just task repertoire (which tasks are performed at all), should be taken into account.     

Production of sexuals in a fission-performing ant: dual effects of queen pheromones and colony size

Models based on the kin selection theory predict that in social hymenopterans, queens may favor a lower investment in the production of sexuals than workers. However, in perennial colonies, this conflict may be tuned down by colony-level selection because of the trade off between colony survival and reproductive allocation. In this study, we present a survey of sexual production in colonies of Aphaenogaster senilis, a common species of ant in the Iberian Peninsula. Similar to most species that reproduce by fission, males were found in large excess compared to gynes (172:1). Sexuals were more likely to be found in queenless than in queenright (QR) field colonies. However, we also found a few gynes and numerous males in very large QR colonies. We compared these data with those available in the literature for A. rudis, a congeneric species from North America that has independent colony founding. The sex ratio in this species was only five males for each female, and sexuals were mostly found in QR nests, irrespective of colony size. We confirmed queen inhibition of sexual production in A. senilis in laboratory experiments and provide evidence that this inhibition is mediated by a nonvolatile pheromone. To seek the potential source of such a queen pheromone, we analyzed the secretions of two conspicuous exocrine glands, the Dufour’s and postpharyngeal glands (DG and PPG, respectively) in both queens and workers. Both secretions were composed of hydrocarbons, but that of DG also contained small quantities of tetradecanal and hexadecanal. The hydrocarbon profile of the DG and PPG showed notable caste specificity suggesting a role in caste-related behavior. The PPG secretions also differed between colonies suggesting its role in colony-level recognition. We suggest that in A. senilis, there are two modes of colony fission: First, in very large colonies, gynes are produced, probably because of the dilution of the queen pheromone, and consequently one or more gynes leave the mother colony with workers and brood to found a new nest. This is beneficial at the colony level because it avoids the production of costly sexuals in small colonies. However, because the queen and workers have different optima for sexual production, we hypothesize that queens tend to overproduce the pheromone to delay their production. This in turn may drive workers to leave the mother colony during nest relocation and to produce sexuals once they are away from the queen’s influence, creating a second mode of colony fission.     

Fire ant polymorphism: the ergonomics of brood production

Summary Social organization is generally assumed to increase colony efficiency and survival; however, little quantitative information is available to support this assumption. Polymorphism is an important aspect of labor division in colonies of the fire ant, Solenopsis invicta. Our objective was to investigate the effect of fire ant polymorphism on brood production efficiency. We set up standardized polymorphic colonies with a full range of worker sizes and artificial monomorphic colonies that contained only small, medium or large workers respectively. Polymorphic colonies produced brood at about the same rate as colonies composed of only small workers (Fig. 2A). Colonies composed of only medium workers produced about 30% less brood, and colonies composed of only large workers produced little or no brood at all. This pattern was independent of colony size; however, smaller colonies (0.75 g, live weight) produced almost twice as much brood per gram of workers as larger colonies (3.0g). Additional experiments revealed that the size of workers in the artificial monomorphic colonies affected all stages of brood rearing. Large workers not only inhibited the development of early and late instar larvae (Fig 4), but also reduced the queen's oviposition rate (Fig. 3). Brood production efficiency on an energetic basis was determined by dividing the grams of brood produced per unit time by the energetic costs expended for the maintenance and production of each worker size class. Worker maintenance costs were estimated from respiration while production costs were determined from the caloric content of worker tissue divided by their average longevity. Worker respiration per milligram body weight decreased about 40% as body size increased (Fig. 5). Large workers lived about 50% longer than small workers (Fig. 6) and contained 9% more energy per milligram of tissue (Fig. 7). Energetic efficiency in polymorphic colonies was approximately 10% higher than in colonies composed of only small workers (Fig. 9). In other words, when food supplies are limiting, polymorphism may offer a slight advantage in brood production.     

Sex allocation ratios in the facultatively polygynous ant, Leptothorax acervorum

We investigated sex allocation in a central European population of the facultatively polygynous ant Leptothorax acervorum. The population-wide sex ratio was found to be quite balanced, with a proportional investment in female sexuals of 0.49. Sex allocation varied considerably between colonies, resulting in split sex ratios. The productivity of colonies was negatively correlated with queen number and positively with colony size. In contrast, the sex ratio (proportional investment in female sexuals) was neither correlated with queen number, colony size, nor total sexual production, but with worker relatedness. The uncoupling of the genetic colony structure and queen number presumably results from frequent queen turnover and colony splitting.     

Offspring protection by merlin Falco columbarius females; the importance of brood size and expected offspring survival for defense of young

Summary Nest predation was simulated by presenting a stuffed raven close to nests of merlins. This was done to examine the influence of brood size related factors on female defence intensity. The original clutch size did not affect nest defense after hatching, but brood size was important. It determined the attack frequency and, for each brood size level, the proportion of attacking females. When brood sizes were manipulated, the defense intensity increased and decreased, respectively, in relation to the size of the brood. In addition, broods with high future survival (first broods) were defended more vigorously than broods with low future survival (replacement broods). Hence, expected benefits in terms of fledgling production and chick survival seem to be important determinants of female investment in offspring protection. The lower predation rate among females responding with overt aggression to the raven compared to that of less aggressive females suggests that defence of young is beneficial.     

Brood size manipulation affects frequency of second clutches in the blue tit

The reproductive trade-off hypothesis predicts that the investment made in current reproduction determines the breeders’ future fitness as a consequence of intra-or inter-generational reproductive costs. Long-lived species are expected to favour their own reproductive value at the expense of their offspring, hence incurring in inter-generational costs, whereas short-lived species are expected to invest in the current breeding attempt even at the expense of their own survival, thus incurring in intra-generational costs. We tested whether intensity of current reproductive effort has intra-or inter-generational costs in a short-lived bird, the blue tit Parus caeruleus, with a brood size manipulation experiment. We expected more intra-generational (parental reproduction and/or survival) than inter-generational (offspring quality and survival) reproductive costs. We found that parental effort, measured as the hourly rate of parental visits to nests, increased gradually with experimental manipulation. Brood size manipulation resulted in a gradual increase in the number of fledglings per nest from reduced to increased treatments. We found an effect of the manipulation on the probability of making a second clutch, with adults rearing enlarged broods being less likely to undertake such a second reproduction during the season compared to those rearing control or decreased broods. We found no evidence of other reproductive costs; neither as adult weight after manipulation, apparent parental local survival, apparent offspring local survival or local recruitment. Although the results seem to support the a priori expectations, alternative explanations are discussed.Communicated by M. Soler     

Common goldeneyes adjust maternal effort in relation to prior brood success and not current brood size

Parental investment theory predicts that parental effort should be related to the reproductive value of the current brood. This depends on both the number of young and the survival prospects of each of them. Thus parents may provide more care to larger broods either because of (1) the direct effect of brood size per se on reproductive value (the “brood size” hypothesis) or because (2) past mortality, reflected in current brood size, predicts future mortality of the brood and hence its reproductive value (the “brood success” hypothesis). Earlier studies have not attempted to distinguish between these alternatives. We tested the hypotheses in the precocial, nidifugous common goldeneye Bucephala clangula, a species with uniparental female care. Maternal effort was measured as the time spent by the female in rearing the brood. We found that brood size itself is not associated with maternal effort, but that females modify their maternal effort according to the mortality already experienced by the brood, supporting the prediction of the brood success hypothesis. We also found that brood mortality varied considerably between broods and that previous mortality predicts future mortality within broods, basic assumptions of the brood success hypothesis. Received: 30 January 1996 / Accepted after revision: 27 October 1996     

Worker drift and egg dumping by queens in wild Bombus terrestris colonies

Wild bumblebee colonies are hard to find and often inaccessible, so there have been few studies of the genetic structure of bumblebees within natural colonies, and hence, it is not clear how frequently events such as worker reproduction, worker drift and queen usurpation take place. This study aimed to quantify the occurrence of natal-worker reproduction, worker drift and drifter reproduction within 14 wild colonies of Bombus terrestris in Central Scotland. Four unlinked microsatellites were used to identify patterns of relatedness of the colonies’ adults and broods. In colonies with queens (queenright colonies), worker reproduction accounted for just 0.83 % of males, increasing to 12.11 % in queenless colonies. Four colonies contained a total of six workers which were not daughters of the queen, and were assumed to be drifters, and four male offspring of drifters. Drifting is clearly not common and results in few drifter offspring overall, although drifters produced approximately seven times more offspring per capita than workers that remained in their natal colony. Unexpectedly, two colonies contained clusters of sister workers and juvenile offspring that were not sisters to the rest of the adults or brood found in the colonies, demonstrating probable egg dumping by queens. A third colony contained a queen which was not a sister or daughter to the other bees in the colony. Although usurping of bumblebee colonies by queens in early season is well documented, this appears to be the first record of egg dumping, and it remains unclear whether it is being carried out by old queens or newly mated young queens.     

Helpers in colonial cooperatively breeding sociable weavers <Emphasis Type="Italic">Philetairus socius</Emphasis> contribute to buffer the effects of adverse breeding conditions

Some studies on the effects of helpers in cooperatively breeding vertebrates show a positive effect of helper presence on reproductive output whereas others find no effect. One possibility for this discrepancy is that helpers may have a positive effect when breeding conditions are adverse, while their effect might go unnoticed under good conditions. We investigate this hypothesis on sociable weavers Philetairus socius, a colonial cooperatively breeding passerine that inhabits a semi-arid region where breeding conditions vary markedly. We used multivariate mixed models to analyse the effect of helpers on reproduction under contrasting environmental and social conditions while controlling for parental and colony identity. We found that reproductive success in sociable weavers was primarily influenced by nest predation and rainfall. In addition, colony size was negatively associated with hatching and fledging success and number of young fledged per season. Helpers had a less prominent but significant influence on feeding rates and reproductive outcome. In agreement with expectations, the presence of helpers counteracted some of the negative effects of breeding in periods of low rainfall or in large colonies and was also associated with an increased number of young fledged per season. Our results illustrate that the effect of helpers might be detectable mostly under unfavourable conditions, but can contribute to improve reproductive performance in those situations.     

Resource allocation,brood production and cannibalism during colony founding in the fire ant,Solenopsis invicta

Summary The colony founding characteristics of newly mated fire ant queens from monogyne colonies were studied in the field and in the laboratory under haplo- and pleometrotic conditions. Initial queen weight (live) was not correlated with subsequent progeny production. During founding, queens lost a mean of 54% of their lean weight, 73% of their fat weight and 67% of their energy content. The percentage of fat decreased from 44% to 33%. Queens lost weight or energy in relation to the amount of progeny they produced (Figs. 1, 2). The efficiency of the conversion of queen to progeny increased as more progeny were produced, leading to a decline in the unit cost of progeny (Fig. 3). The more minims a queen produced, the lower the mean weight of these minims and the faster they developed (Fig. 4). In a field experiment on pleometrotic founding, total brood increased with queen number, peaked between four and seven queens and declined with 10 queens (Fig. 5). Brood developed faster at the sunny, warmer site, but total production and queen survival was higher at the shady site. As queen density increased, production per queen decreased as a negative exponential in which the exponent estimated sensitivity of brood production to queen-crowding and the constant estimated the production by solo queens (Fig. 9). These effects of queen number were confirmed in laboratory experiments. The decrease of production per queen was small and not always detectable during the egg-laying phase, but brood attrition was always strong during the larval period and increased with queen number (Figs. 8, 10). While airborne factors may have contributed to this inhibition, most of the brood reduction was due to other causes, probably cannibalism. For a given number of minims, increased queen number increased the mean weight of these minims, an effect that resulted both from a lower minim production per queen and from cannibalism of dead queens by survivors (Fig. 11). Cannibal queens lost much less weight to produce a given number of minims than unfed control queens, and these minims were heavier (Fig. 12).     

Decentralized control of drone comb construction in honey bee colonies

Honey bee colonies furnish their nests with two types of comb distinguished by cell size: large cells for rearing males (drone comb) and small cells for rearing workers (worker comb). The bees actively regulate the relative quantity of each type, a behavior likely to be important in setting a colony's sex ratio. Experimental analysis of the information pathways and control mechanisms responsible for this regulation found the following results. The amount of drone comb in a nest is governed by negative feedback from drone comb already constructed. This feedback depends on the workers having direct contact with the drone comb in their nest, but does not depend on the queen's contact with the comb. The comb itself, rather than the brood within it, is sufficient to provide the negative feedback, although the brood may also contribute to the effect. These findings show that drone comb regulation does not depend on the queen acting as a centralized information gatherer and behavioral controller. Instead, the evidence points to a decision-making process distributed across the population of worker bees, a control architecture typical of colony organization in honey bees and other large-colony insect societies. Received: 24 May 1997 / Accepted after revision: 30 August 1997