Our results show that harvester ant colonies vary in the regulation of collective behavior. Colonies differ in the baseline rate at which ants leave the nest, in foraging activity, and in how closely they adjust foraging to changes in the rate of forager return. This variation among colonies produces reaction norms that may influence the evolution of collective behavior (Dingemanse et al. 2009
). The regulation of foraging is ecologically important because it determines how a colony manages the trade-off between the risk of water loss when foraging and the risk of losing foraging area to a neighboring colony when not foraging (Adler and Gordon 2003
). However, in some conditions, competition among neighboring colonies is intense (Sanders and Gordon 2004
), and it may be worthwhile to scour the desert for any seed at all, despite the cost in desiccation.
We found that harvester ant colonies differ in the way that foraging activity responds to current conditions. First, some colonies are more likely than others to send out foragers. For example, the spread of points on the y
axis of shows the variation among 14 colonies in average rates of outgoing foragers. shows differences among 24 colonies in the average rates of returning foragers. It is well known that ants within colonies differ in activity level (e.g., Jaisson et al. 1988
); our results here show that colonies differ in activity level. Second, colonies also differ in the propensity to regulate foraging activity in response to a change in forager return rate (). This propensity is related to overall foraging level.
One source of colony differences in foraging activity appears to be a colony-specific trait that sets the interval that any ant waits before it goes out, independently of stimulation from returning ants. The association between the rate at which patrollers emerge, even when no ants return, in a given colony, and the average rate at which foragers leave the nest in the same colony, suggests that both patrollers and foragers have in common a baseline rate of activity. It is unlikely that the rate at which patrollers emerge depends on colony size; young colonies and mature ones, ranging in size by a factor of 5 from 2000 to 10
000 ants, have about the same numbers of patrollers, 30–50 (Gordon 1989
). Moreover, very small differences in the numbers of patrollers that emerge in each burst predict much larger differences in the numbers of ants foraging per minute (). It is also unlikely that the rate at which patrollers emerge directly determines the rate of foraging later on. Patrollers initiate foraging when they return to the nest (Greene and Gordon 2003
), and once foraging begins, the patrollers are no longer active. We do not know whether the number of patrollers active influences how many foragers first leave the nest. In any case, there is no evidence that the day’s foraging activity is determined by the initial number of foragers. Further work is needed to understand what produces colony differences in the activity of patrollers and foragers.
In many ant species, foraging is regulated by a nonlinear process that links numbers of foragers to the quality or quantity of food (Sumpter and Beekman 2003
; Detrain and Deneubourg 2008
). It seems that harvester ants, using encounter rate rather than pheromone trails, regulate foraging using a process that is also nonlinear. We found that a P. barbatus
colony is more likely to respond to a decrease in forager return rate when the initial rate of foraging is high. The following scenario might explain why. When the rate of foraging is low, foragers leave the nest at a rate set by a baseline probability that is independent of the rate of forager return. When food is abundant and the rate of forager return is high, foragers respond to returning foragers. Removing returning foragers artificially brings the rate of forager return down to the low rate at which outgoing foraging depends only on the baseline rate. When we stop preventing the return of foragers, the rate of forager return increases (see ) and inactive foragers begin to respond to returning foragers again, which brings the rate of outgoing foraging back up. However, on days when the foraging activity is initially very low, removals have no effect because the rate of outgoing foragers depends only on the baseline probability that is independent of the rate of foraging return.
It could be that foragers are less likely to respond to a change in the rate of forager return when rates are low because a change in a low rate is difficult to assess. The lower the rate of forager return, the fewer incoming ants each inactive forager encounters, and a small sample has a higher variance than a large one. Like the ants, it is difficult for us to detect a change in the rate of foraging when it is low (). The lower the rate of foraging, the higher the variation in the rate. This leads to a smaller apparent decrease in forager return rate, measured as the ratio of foraging rate after to rate before removals.
However, it is clear that the ants can respond to a change in forager return rate even when rates are low. The rate of outgoing foragers changed in response to removals at a wide range of levels of foraging activity, including some trials in which foraging rates were quite low. For example, shows that foraging changed in response to removals at low levels of foraging for colony 452 and foraging did not change in response to removals at high levels of foraging for colony 15. Thus, the association we found between response to removals and high foraging activity cannot be solely due either to the ants' difficulty in detecting a change in return rate or to our difficulty in detecting a relative change in the rate of outgoing foragers, when foraging activity is low.
In general, colonies are more likely to adjust to changes in forager return rate when foraging rate is high. Thus, colony differences in the level of foraging activity lead to variation in the propensity to regulate foraging. But even taking foraging rate into account, there were still differences among colonies in the probability that they responded to removals (). It appears that in addition to overall level of foraging activity, some other factors influence how closely a colony regulates foraging. These other factors may explain why, in a previous study with a much smaller sample of colonies (Gordon et al. 2008
), we did not find significant differences among colonies in response to removals. Some possibilities include the amount of stored food and the current need to feed larvae (Dussutour and Simpson 2009
; Mailleux et al. 2010
). Excavations show that colonies store food for many months (Gordon 1993
) and differ greatly in the amount of stored food (Gordon 1992
). We do not know how the amount of stored food influences the minute-to-minute regulation of foraging, and it is not possible to measure this amount directly in the field without destroying the nest.
We do not know what causes the differences among colonies in foraging behavior that we report here. Colony behavior depends on colony size in many ant species (e.g., Tschinkel 1993
; Bourke 1999
; Thomas and Elgar 2003
; Gordon 2010
). In P. barbatus
, task allocation (Gordon 1987
) and relations with neighbors (Gordon 1992
; Gordon and Kulig 1996
) change as a colony grows older and larger. However, although colony size influences colony behavior, it does not fully determine the numbers actively foraging at any moment. In P. barbatus
, as in many social insect species, the moment-to-moment rate of foraging depends on factors other than colony size, such as the rate of food intake (e.g., Fernandez et al. 2003
for honey bees; O'Donnell 2001
for wasps). At most about 20% of the workers in a mature colony engage in foraging at any time (Adler and Gordon 2003
), but on the year-to-year scale, the number that forage is not a simple linear function of colony size, as the numbers foraging change by a factor of 2 from ages 2 to 5 years (Gordon and Kulig 1996
; Adler and Gordon 2003
), while overall colony size changes by a factor of 5 during those years (Gordon 1992
). On the day-to-day scale, ants from all other exterior task groups switch tasks to foraging when more foragers are needed (Gordon 1989
), and foragers can be active on 1 day and revert to inactivity the next day (Gordon 1991
Colony differences in response to changing conditions provide the variation that underlies the evolution of collective behavior. Further work is needed to determine if the differences shown here account for the long-term year-to-year differences among colonies in foraging behavior observed previously (Gordon 1991
). Then, to investigate the evolution of the regulation of foraging, the next question is how variation among colonies in the regulation of foraging affects colony growth, survival, and reproductive success.