Behavioral Ecology Vol. 10 No. 5: 585-591
© 1999 International Society for Behavioral Ecology
Fitness consequences of cooperative colony founding in the desert leaf-cutter ant Acromyrmex versicolor
Social Insect Research Group, Department of Biology, Arizona State University, Tempe, AZ 85287-1501, USA
Address correspondence to S. Cahan. E-mail: azsic{at}asuvm.inre.asu.edu .
Received 18 August 1998; accepted 22 February 1999.
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ABSTRACT |
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The evolution of cooperative colony foundation (pleometrosis) in ants has been attributed to conversion of extra resources into increased competitive ability. Most cooperative founding species provide these additional resources from internal fat stores; however, in those species that forage for resources, the extent and type of individual investment in multiqueen colonies is not well understood. We compared singly- and group-founded laboratory colonies of the desert leaf-cutter ant Acromyrmex versicolor to investigate how cooperation affects colony survival, foraging success, and worker production. Under laboratory conditions, single foundresses were significantly less likely to initiate a successful symbiotic fungus garden, which inevitably led to colony starvation and death. If gardens were initiated successfully, however, there was no difference in the growth trajectories and foraging patterns between colony types. Cooperation in this species may more likely be maintained by survival benefits than by growth rate differences, which may be constrained in groups by individual and colony-level costs.
Key words: Acromyrmex versicolor, cooperation, division of labor, leaf-cutter ant, pleometrosis.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Cooperative nesting among females is an inherently costly strategy. Group-nesting females potentially lose their reproductive monopoly within the nest when other fertile individuals are present, and close contact with group members may increase competition for resources and increase risks of parasite or pathogen transmission. Despite these costs, however, cooperative breeding has evolved in a wide diversity of taxa, including fish (Taborsky, 1987
), birds
(Mumme et al., 1988;
Vehrencamp, 1977), mammals
(Packer et al., 1990), and
insects (Eggert and
Müller, 1992;
Wcislo, 1997). In some of
these taxa, associating females are closely related, offsetting costs through
kin selection (Hamilton,
1964). Not all cooperative groups contain close relatives,
however, and for these taxa cooperative nesting must have significant
ecological benefits in order to evolve.
In ants, cooperative nesting during colony founding has evolved a number of
times in different genera (Choe and
Perlman, 1997). Young queens of cooperative-founding species
associate with one another soon after mating and excavate or construct group
nests. Colony cofoundresses are usually all fertile and unrelated to one
another (Hagen et al., 1988;
Rissing and Pollock, 1988).
Brood produced by all females is kept together within the nest, and the
resulting workers apparently have no mechanism for distinguishing their own
mothers within the group (Bernasconi and
Keller, 1996).
Two main types of fitness benefits have been proposed to explain the
evolution of cooperative colony founding. First, cooperation may benefit
queens by reducing mortality during the founding period, increasing the
likelihood that they will live to produce reproductive offspring later
(Bartz and
Hölldobler, 1982;
Waloff, 1957). Nest joiners
may avoid high predation or desiccation risks associated with nest excavation
(Choe and Perlman, 1997;
Pfennig, 1995), or multiple
females may be better able to mitigate stressful ecological conditions such as
nest damage or extreme soil aridity
(Strassmann and Queller, 1989;
Cahan, in preparation). Group nesting may also reduce individual starvation
risks before the first workers begin to forage
(Rissing and Pollock,
1991).
The second potential benefit of cooperative colony founding is an increase
in total worker production. Previous studies of cooperative colony founding
suggest that initial worker number is an important determinant of colony
competitive ability, both against other starting nests and, later, against
nearby conspecific adult colonies (Bartz
and Hölldobler, 1982,
Rissing and Pollock, 1991;
Tschinkel and Howard, 1983).
Worker production in many species tends to increase with the number of
cofoundresses, presumably due to additional resource contributions from
joining queens (Bartz and
Hölldobler, 1982;
Rissing and Pollock,
1987).
In most ants, nutrition for the first workers comes exclusively from the
fat and muscle reserves of the attending queen
(Hölldobler
and Wilson, 1990). Thus, the presence of additional queens can
impact resource availability directly, provided they are willing to invest
their own stored material. One exception to this is the desert leaf-cutter
ant, Acromyrmex versicolor. Queens of this cooperative founding
species forage throughout the colony founding period to feed a symbiotic
fungus garden, which is in turn eaten by larvae. Nonclaustral species tend to
have lower fat stores than claustral species, reducing their ability to
influence resource availability through allocation of body reserves
(Keller and Passera, 1989). If
cooperative colony founding has evolved in A. versicolor because it
increases worker production, joining queens may be contributing through their
behavior within the colony in lieu of, or in addition to, stored resource
investment.
Starting colonies are complex environments, in which many tasks must be
completed simultaneously. This complexity provides several different routes by
which additional females could potentially affect worker production.
Individuals may interact with the offspring directly through additional
foraging, or by performing parental care behaviors in the nest, such as the
behavior of nest helpers in Mexican jays
(Brown, 1972) and subordinate
females in paper wasps (West-Eberhard,
1969). However, cofoundresses may also be able to impact offspring
production without directly feeding or caring for brood. Performance of tasks
unrelated to provisioning, such as group territory and resource defense, may
affect productivity by reducing resource constraints
(Brown, 1974). Division of
labor within the group may also be important. Group-founding colonies of
A. versicolor show strong asymmetries in task performance,
particularly in foraging behavior (Rissing
et al., 1989). In multiqueen colonies, one individual is free to
specialize on foraging and can therefore devote more effort toward food
provisioning for the young.
In this study, we investigated why A. versicolor queens participate in cooperative colonies and how additional queens contribute to colony survival and growth. To identify the benefits associated with cooperative colony founding, we manipulated the number of queens in laboratory colonies and followed their development until production of the first workers. We monitored queen and fungus survival to evaluate whether cooperation confers survival benefits at either the individual or the colony level. We also observed colony growth trajectories to evaluate whether additional queens affect colony worker production. To identify the mechanisms by which benefits are conferred, we monitored performance of several different tasks within the colony and used path analysis to isolate components of queen behavior that impact fungus and, ultimately, worker production.
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METHODS |
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Newly mated A. versicolor queens were collected on the ground at the Butcher Jones Recreation area, Maricopa County, Arizona, USA, on 23 August 1996. All queens had previously removed their wings but had not yet excavated a starting nest. Queens from this site generally form cooperative nests in the field (Cahan, personal observation).
We housed queens in the laboratory in circular, clear plastic dishes 9 cm
diam x 3.5 cm high. Each nest consisted of a single nest dish
one-quarter filled with pottery plaster, and an identical foraging chamber
without plaster attached by a 1-inch long piece of clear plastic tubing. Foil
was placed over the nest chambers for 2 weeks to promote fungus initiation,
then removed to facilitate nest observations. Twenty single-queen nests and
twenty three-queen nests were set up on 23 August and maintained until 22
November 1996. We used 3 queens in the multiqueen treatment to approximate the
average of 2.5 queens found in field starting nests
(Rissing et al., 1986). Nests
were kept at 25°C. We injected 2 ml of water into the pottery plaster at
weekly intervals to maintain high humidity in the nest chambers. Nests were
checked for mortality every 1-3 days. All dead individuals were removed from
nests. Total loss of the fungus garden was considered equivalent to queen
death and nests without fungus were excluded from later observations.
We checked colonies after 7 days to determine whether any fungus was present. After this, fungal growth was assessed once a week by placing an acetate sheet imprinted with a 0.1 in2 grid on the top of the nest and sketching the outline of the fungus garden. Fungus area was measured to the nearest 0.05 in2. We took measurements for 12 weeks. Only those nests that maintained a living fungus garden over at least 4 weeks were included in analyses.
Fungus growth rate can be influenced by the type of leaf substrate provided (Weser J, in preparation). Thus, females may be able to distinguish between leaves upon which the fungus grows rapidly ("high quality") and those upon which the fungus grows slowly ("low quality") and may direct increased foraging effort toward selective searching for high-quality leaves. Previous research suggests that two trees found within the range of A. versicolor, blue palo verde and mesquite, differ in their suitability for fungus growth (Weser J, in preparation). We provided each nest with both high-quality (HQ) leaves (blue palo verde) and low-quality (LQ) leaves (mesquite). Twenty leaves of each type were offered for the first 9 days; however, because of low foraging rates across both treatments, 10 of each type were offered for the remaining 21 days of foraging observations. The number of each leaf type remaining was noted every 1-3 days, and new leaves were provided if fewer than three of either leaf type remained. All leaves were replaced each week. We monitored leaf intake for 4 weeks, after which all nests were given both leaf types ad libitum. To test whether foundresses selectively foraged for a certain leaf type, we compared the pooled number of HQ and LQ leaves collected to a 1:1 ratio with a G goodness-of-fit test.
Acromyrmex versicolor nests generally produce the first minim workers after 6-8 weeks (Julian, personal observation). The number of eclosed workers was censused weekly. The size of the first cohort of workers was quantified 2 weeks after eclosion of the first worker in each colony. It is at this age that workers first forage outside the nest and could constitute a competitive threat to neighboring colonies (Rissing SW, personal communication).
Because few single colonies survived to worker production (see Results), we conducted a second, smaller scale colony comparison in the summer of 1997. Single and three-queen colonies were housed in identical laboratory nests as in the main study. To increase survival, all nests without fungus after week 1 were provided with approximately 0.1 in2 of fungus from an adult colony. This addition was unlikely to bias later comparisons, as initial fungus inoculi did not appear to vary by more than 0.05 in2 across all colonies at this stage in either experiment. We gave starting nests HQ and LQ leaves ad libitum and checked them for mortality once weekly. After 6 weeks, nests were checked daily for workers. Two weeks after the first worker was seen in each colony, the total numbers of workers and pupae were counted.
Statistics
Survival of single versus multiqueen colonies over 8 weeks was compared
with a Peto and Peto log-rank test for censored survival data
(Peto and Pike, 1973;
Pyke and Thompson, 1986). This
test calculates a log-rank statistic comparing expected and observed deaths
over each time interval. Mortility due to failure to initiate fungus growth
was distinguished from foundress death or failure to maintain the fungus
garden by computing the log-rank statistic with and without colony survival
data from the first week.
Worker production may be influenced by queen number either directly or through a number of indirect routes. We have conceptualized these potential effects in a path diagram (Figure 1). Direct influence on worker number (A) could occur if starting colonies are brood limited, rather than resource limited, so additional egg contribution by cofoundresses could be translated into a larger worker population. Increased broodcare could also reduce offspring loss during development. If colonies are resource limited, however, queen effect should be mediated through increased fungus availability (B), as measured by the area of the fungus garden. Fungus growth could be influenced in three ways. First, group founding may directly increase fungus size (C) because groups process leaves and tend the fungus more efficiently than single queens. Alternatively, division of labor within the group may allow the forager to increase foraging effort, leading to higher total leaf intake (D) or higher quality leaf selection (E), and consequently to a larger fungus garden (F, G). High-quality leaves may also increase worker production (H) by raising fungal nutritional value for larvae.
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B), or by shifts in total
number of leaves collected (D
We tested these proposed relationships with a path analysis, which
statistically tests for direct and indirect causative relationships in
multifactor experiments (e.g., Herbers,
1990). The path analysis incorporated queen number, total leaf
intake, proportion of HQ leaves (arcsine transformed), fungus area during the
period of larval development, and worker production. All significance tests
are presented with F values for one-way regressions and T
values for multiple regressions performed as part of the path analysis.
Relationships between variables were considered "direct" when the
variables were linked by a cause and effect arrow (see
Figure 1; e.g., fungus area and
worker number). A cause linked to an effect via a third variable (e.g., number
of leaves and worker number) was considered an "indirect" effect.
Most variables were joined by both direct and indirect routes. Because few
single nests produced workers, the direct effect of queen number on worker
production (path A in Figure 1)
could not be tested in this experiment. Instead, the total effect of queen
number on worker production was tested in the second experiment with a one-way
regression, and the significance of path A was inferred from the total effect
significance.
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RESULTS |
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Colony survival
Thirty-nine nests were used in the study, excluding one escaped group colony. Over 8 weeks, solitary nests suffered significantly higher mortality than group nests (LR1 = 15.29, p <.001, Peto and Peto log-rank test; Figure 2). However, this effect was due entirely to foundress death or fungus failure within the first week, as comparison of all subsequent mortality showed no significant differences (without week 1: LR1 = 1.01). Indeed, 9 of the 17 solitary queens surviving at week 1 failed to initiate a fungus garden. All 19 group nests successfully initiated a garden. After the first week, the most common cause of colony death was catastrophic fungus mortality and subsequent removal of the fungus garden from the nest.
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Worker production
Direct, indirect, and total effects generated by the path analysis are
summarized in Table 1 and
schematically presented in Figure
3. Three solitary colonies survived long enough to produce
workers. Fourteen multiqueen colonies produced workers. All surviving colonies
except one group colony produced workers over the 12 weeks of the experiment.
Worker emergence time was variable, ranging from 6 to 10 weeks. Worker number
was significantly positively affected by fungus area but not by leaf quality
(area: T = 2.36, p =.04;
Figure 3a). By the day of the
worker census, however, the relationship between worker number and fungus area
had become significantly negative (Figure
3b).
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In the 1997 experiment, seven single colonies and five multiqueen colonies produced workers. Colonies produced an average of 4.58±0.65 workers over a period of 2 weeks. Queen number had no significant effect on either worker or total brood number (F1,12 = 0.11, ns, linear regression).
Foraging effort
Few colonies foraged for the first 3 days of the experiment. Colonies took
in 0.56±0.10 leaves per day (l.p.d.) for the first week. Foraging
increased significantly in week 2 to 2.24±0.45 leaves per day
(p <.001, repeated-measures ANOVA). Foraging dropped by 50% during
week 3 (1.02±0.15 l.p.d.), then returned to week 2 levels for the final
week of observations (1.91±0.25 l.p.d.). Single and group nests did not
differ in total leaf intake over the 4 weeks (T = 0.54, ns).
There was no difference in the proportion of HQ leaves collected by single and multiqueen colonies (F1,20 = 0.04, ns). Overall, foragers showed a significant preference for HQ leaves, though all colonies but one collected some of each leaf type (Gpooled = 36.64, df = 1, p <.001). There was significant heterogeneity within the sample, with four multiqueen colonies showing significant deviation from HQ preference (Ghet = 66.81, df = 25, p <.001).
Fungus growth
Colony fungus gardens showed an initially high rate of growth, which
declined significantly over the 4 weeks of observation
(t19 = 2.63, p <.05; paired t test).
As the garden grew larger, a larger number of foraged leaves was used for
fungus maintenance, rather than for growth. To measure the number of leaves
needed for basic maintenance, we divided the number of leaves collected in
each 2-week period by the proportional growth of the fungus during the same
period. In the first 2 weeks of fungus growth, colonies required an average of
3.66 leaves to maintain the fungus without any additional growth. During the
second 2 weeks, the number of leaves required increased to 11.53
(t18 = -3.12, p <.01; paired t
test).
Fungus area was significantly influenced by total foraging effort (T = 2.21, p <.05). Both queen number and leaf quality had marginal, but not quite significant, direct effects on fungus growth (queen number: F1,25 = 3.67, p <.10; leaf preference: T = 1.95, p =.06).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The formation of social groups is associated with a number of costs, such as increased competition and disease transmission. This suggests that sociality among nonrelatives must be accompanied by significant ecological benefits (Alexander, 1974
). The
results of this study point to increased success in fungus initiation as an
important benefit of cooperative colony founding. Even in the relatively
benign environment of the laboratory, jointly founded nests enjoyed
significantly higher success in initiating a fungus garden. Thus, queens may
benefit directly from associations by pairing with cofoundresses possessing
more viable or larger fungal inoculi. This difference in initiation success
may be even more pronounced in the field, where variation in moisture
availability and temperature could reduce the probability of successful fungus
growth. Fungus garden failure was found to be an important component of early
mortality in two other Acromyrmex species, A. niger and
A. balzani (Fowler,
1992).
Many of the species displaying cooperative colony founding, including
A. versicolor, start nests in specific microhabitats, resulting in
dense clumps of young queens which must compete for the territory
(Rissing et al., 1986,
Sommer and
Hölldobler, 1995;
Tschinkel and Howard, 1983).
The association between competitive environment and cooperative colony
foundation leads to the prediction that group nesting should increase
competitive ability against other young colonies through increased worker
production. Cooperative colony foundation is often associated with increased
total worker production (e.g., Bartz and
Hölldobler, 1982,
Rissing and Pollock, 1987;
Waloff, 1957). Whether this
increase provides a selective advantage is less certain, though some
laboratory and field studies suggest that, for large groups, high worker
numbers can provide enough competitive benefits to outweigh the costs of nest
sharing (Adams and Tschinkel,
1995; Bartz and
Hölldobler, 1982;
Choe and Perlman, 1997;
Rissing and Pollock, 1991).
Because of this body of research, cooperation in Acromyrmex
versicolor has been assumed to have similar fitness consequences
(Choe and Perlman, 1997;
Rissing and Pollock, 1988;
Rissing et al., 1989;
Seger, 1989).
We found that additional queens in laboratory colonies of A.
versicolor did not lead to an increase in worker production. When
controlled for early fungus mortality, starting colonies produced an average
of 4.58 workers per colony, regardless of queen number. This lack of
relationship remained even when worker pupae, which will become the second
cohort of workers, were included in the analysis. Without a larger worker
population, cooperative colony founding would have little effect on
intraspecific competitive ability, though it is possible that queens may
jointly defend their nest from usurpers or adult colonies, such as occurs in
the imported fire ant Solenopsis invicta
(Jerome et al., 1998).
Multiple queens may also be able to produce workers at a faster rate than
single queens; no clear trend was evident during this study, though the high
variance in emergence date made it impossible to test this directly with our
limited sample sizes.
Though these results suggest that A. versicolor queens may not
receive an important potential benefit of cooperative colony founding, it is
important to note that field conditions are quite different from laboratory
conditions, with potential consequences for the direction and strength of the
relationships considered in our model. Resource availability, in particular,
is likely to be lower and less predictable in the field, leading to higher
foraging costs in terms of both energy expenditure and search time. It is
possible that under these conditions, single queens may be more constrained by
within-nest tasks and be forced to restrict their foraging effort. However,
because A. versicolor starting nests occur beneath preferred food
plants (Rissing et al., 1986;
Weser J, unpublished data), resource availability may not be different enough
to affect our conclusions significantly. In addition, foraging in laboratory
nests was probably not cost-free, especially as the fungus garden grew larger,
because fungal growth trajectories declined over time in both treatments.
Other variables, such as temperature, moisture availability, and predation
pressure, may also have some effect on worker production and should be
investigated in the field.
Lack of a relationship between queen and worker number may in part be
explained by the unique combination of fungal symbiosis and nonclaustral
colony foundation in the desert leaf-cutter ant that alters the mechanisms of
queen input into the colony. The presence of the fungus garden alone does not
appear to limit queens' abilities to influence worker number, as group colony
founding in a claustral leaf-cutter, Atta texana, does result in an
increase in both fungus size and worker number
(Mintzer, 1987). Because they
are nonclaustral, however, A. versicolor queens have little to
contribute to colony growth at the outset of colony founding. The only type of
offspring investment possible for cofoundresses is performance of colony
tasks; however, there was no evidence from this study that any of the
behaviors undertaken by additional queens affected total food availability for
worker production. The reasons for this lack of effect probably vary for the
different pathways considered in our colony model.
Leaf collection by more than one cofoundress has not been observed in
A. versicolor, which restricts their ability to influence worker
production directly (path A in Figure
1; Rissing et al.,
1989). It is unclear why multiqueen colonies have a single
foraging specialist. Because A. versicolor queens are not related
(Hagen et al., 1988), we would
expect a shift away from strict division of labor in order to equalize costs
to co-operating queens (Reeve and
Ratnieks, 1993; Vehrencamp,
1983). Perhaps other ecological factors, such as desiccation
stress, contribute to this phenomenon by selecting to minimize the number of
foragers. Alternatively, queen behavior in the colony-founding context may be
constrained by selection acting on division of labor in the worker population.
A. versicolor colonies show pronounced division of labor from an
early age (Julian, unpublished data;
Julian and Cahan, in press).
If foraging propensity is determined by the same genes in both queens and
workers, selection against foraging specialization during the founding stage
may be balanced by selection for specialization in the adult colony.
Experiments are currently underway to address this possibility.
Division of labor among queens may also have an indirect effect on brood production. Because cofoundresses are available to care for the nest, the foraging specialist in multiqueen colonies is potentially free to increase her foraging effort, which we would detect as an increase in the quantity and/or quality of leaves collected over the founding period (paths D and E in Figure 1). We found no evidence that such an increase occurs. Queen type had no effect on either the total number or species composition of foraged material, indicating that the foraging specialist was expending the same effort into foraging as she would as a solitary foundress.
Why don't specialists increase their foraging effort? Unlike within-nest
task performance, increased foraging effort does significantly increase colony
worker production, making allocation toward leaf collection appear to be an
advantageous strategy. Lowered group efficiency occurs in some cooperative
breeding systems due to intranest competition for genetic representation in
the brood. Groove-billed anis, for example, regularly engage in egg dumping
within the group nest, severely reducing egg-laying efficiency
(Vehrencamp, 1977). This
situation may also occur in some ants, which invest fewer fat stores to
offspring when in groups to bias later queen conflicts in their favor
(Bernasconi and Keller, 1996;
Tschinkel, 1993). Retention of
energy for direct competition within A. versicolor colonies is
unlikely because multiple foundresses apparently do not fight after worker
eclosion, instead cohabiting jointly founded nests long after the founding
stage (Julian, personal observation). However, queens may be competing for
future reproductive success by attempting to minimize their risk of
foraging-associated mortality.
We can think of three additional hypotheses to explain why foraging investment does not increase in multiqueen colonies: constraints on fungal growth, increased cost asymmetry among cofounding queens, and negative effects of increased worker number.
Fungal growth constraints
The path diagram that we constructed assumes that foraging behavior has a
direct causal relationship to fungus growth. However, the significant
correlation between leaf input and fungal growth may also be generated if the
causal relationship were reversed; that is, if fungal growth capacity
determines the number of leaves collected. Fungal area available for new leaf
placement is probably limited during colony initiation, when queens build up a
garden from extremely small inoculi. It appeared in this study that foragers
were willing to collect more leaves than can be used by the fungus garden, as
most piled leaves outside the nest entrance and brought them in as old leaves
were used. If excess leaves are experimentally provided to starting colonies,
they are either removed or they rot within the nest, exposing the colony to
undesirable pathogens and foreign fungi (Cahan, personal observation). This
suggests that at the initial stage, growth rate is limited not by queen
behavior but by the growth capabilities of the fungus itself. Later in the
founding period, however, fungus growth rate tends to decline from its
original trajectory, suggesting that at this point growth may be driven more
by behavioral constraints than by the growth potential of the fungus.
Cost asymmetry
Foraging behavior is rarely seen in starting ant colonies, suggesting that
such activity is risky. Because the fungus garden grows volumetrically, the
costs of foraging enough to maintain a constant growth rate increase
exponentially throughout the colony-founding period. Inevitably, the increased
cost falls on the foraging specialist, though the worker production benefits
of her efforts are evenly distributed to all queens in the colony. This
produces an increasing fitness skew among cofoundresses, with nonforagers
benefiting at the expense of the foraging specialist. In response, the
specialist should refuse to increase her foraging effort at the point in
colony development when she no longer receives net benefits from enlarging the
fungus. Leaf intake did not increase after the second week, and colonies
showed a significant decline in fungus growth rate over the 8-week study.
Negative effects of workers
Studies in other ant species have demonstrated that larger numbers of
workers allow colonies to be more competitive and outgrow the vulnerable
founding stage more quickly (Rissing and
Pollock, 1991; Tschinkel,
1992; Vargo, 198).
Worker number has been shown to have a positive effect on colony growth rate
in young A. versicolor colonies as well (Cisneros R, and Fewell JH,
unpublished data). However, when colonies produce the first minim workers, the
sudden addition of nonforaging consumers within the colony may be more of an
ergonomic burden than a benefit. Though the largest broods in this study
produced twice the average number of workers (experiment 1: 6 versus 2.69;
experiment 2: 9 versus 4.64), these productive colonies tended to outstrip
their fungal resources in the weeks after worker emergence. This can be seen
most clearly in the fungus—worker relationship over time. At week 3,
when the first larvae are feeding, fungus area is a good predictor of worker
production (Figure 3a). By 2
weeks after workers emerge, however, this relationship has changed from
positive to negative, with the most productive colonies suffering major fungus
losses (Figure 3b). This
suggests that adult ants actively consume the fungus, as has previously been
found in this and other leaf-cutter species
(Bass and Cherrett, 1995;
Tibbets and Faeth, 1999;
Quinlan and Cherrett, 1979).
Because fungus growth costs increase exponentially, even three queens may not
be able to provide enough fungus for each new worker to prevent excess
consumption, leading to a maximum possible number of workers that can be
safely produced regardless of colony type.
Colony growth in A. versicolor may be limited by any or all of these factors. The unique relationship between queens and their symbiotic fungus fundamentally alters how queens interact with their offspring, making a full understanding of colony function much less straightforward than in other species. The fungal garden may control numerous components of colony development: initial survival, foraging rate and selectivity, worker production, and probably other aspects such as nest site selection, which we did not examine in this study. Because of the strong relationship between the fungal garden and workers, and the weak relationship between queen number and fungal growth, queens may be constrained in the types of fitness contributions they can make in the starting colony context. Thus, what appears to be a selfish reduction in colony investment by cofounding queens may in fact be determined by the colony environment, rather than intranest competition. Further work on the role of the fungus in colony function should help to resolve how task performance is controlled in the desert leaf-cutter ant.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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We thank Susan Bertram, Jennifer Drnevich, and the members of the Social Insect Research Group at Arizona State University for helpful suggestions on experimental design and the manuscript. Jennifer Fewell provided laboratory space for the colonies. Funding for this study was provided by a grant from the Zoology Department of Arizona State University to G.E.J., and by National Science Foundation grant DEB-9623487 to S.C. and S.W. Rissing.
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