VARIATION IN PERCEPTION OF TASK INITIATION AND COMPLETION BETWEEN RUGATUL8US NESTMATES DRIVES DIVISION OF LABOR

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Authors Lynch, Colin Michael

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Link to Item http://hdl.handle.net/10150/631546 VARIATION IN PERCEPTION OF TASK INITIATION AND

COMPLETION BETWEEN TEMNOTHORAX RUGATUL8US NEST-

MATES DRIVES DIVISION OF LABOR

By COLIN MICHAEL LYNCH ______

A Thesis Submitted to the Honors College

In Partial Fulfillment of the minor with honors in Ecology and Evolutionary Biology THE UNIVERSITY OF ARIZONA DECEMBER 2018

Approved by: ______

Dr. Anna Dornhaus Ecology and Evolutionary Biology Variation in perception of task initiation and completion between Temnothorax rugatulus ​ ​ ​ nest-mates drives division of labor.

Abstract

Division of labor is one of the defining characteristics of social societies. It is thought that division of labor arises through simple logical rules and requires only that workers respond to environmental stimuli they encounter. It has been proposed that the response threshold is one of the primary rules that drives division of labor. We test this hypothesis by measuring response thresholds in the species Temnothorax rugatulus to different task-associated stimuli and see ​ ​ whether or not they can predict which tasks the ant takes on in the colony. We found that the response threshold hypothesis successfully predicts the relationship between the sensitivity to task-associated stimuli and performance of the task itself for one task, but it fails at predicting the relationship of the other task. In fact, the results were the opposite of what the response threshold predicted, suggesting that there may exist an alternative rule that functions in the opposite direction of the response threshold and yet may also be capable of allocating tasks. Here we coin the term “satisfaction threshold” as a name for this alternative mechanism.

Introduction

Social are among the most dominant organisms on the planet. The biomass of alone rivals that of humans and they are one of the main turners of earth, moving some 50 tons of soil every year in a single square mile of land (Holldobler and Wilson, 1990). Their ecological success is often attributed to their division of labor (Robinson, 1992), which can be understood as the partitioning of work between specialists in a system (Duarte et al, 2011). As these colonies are not centrally controlled, this emergent behavior of colonies arises from the actions and decisions of individuals. These decisions are made through simple logical rules which convert signals from the environment into behavioral responses.

While a number of different models have been proposed to explain the logic used by social insects (reviewed in Beshers and Fewell, 2001), one of the most widely used employs the use of innate response thresholds as a regulating mechanism of division of labor. Low threshold workers perform tasks at a lower level of stimulus than high threshold workers and are therefore specialists in a task, maintaining homeostasis in the task associated stimulus. High threshold workers for a particular task stimulus will perform a task only if the stimulus exceeds their higher thresholds. When the need for the task is kept low by the low threshold workers, then the high threshold workers will rarely be triggered.

It has been demonstrated that variation in sensitivity to sucrose in young honeybees correlates with their future foraging behavior (Pankiw and Page, 2000). Workers with the lowest response threshold became water foragers, followed with increasing response thresholds by pollen foragers, nectar foragers, bees collecting both pollen and nectar, and finally those returning to the colony empty. It has also been shown that bumblebees vary in their response thresholds for thermoregulatory fanning behavior, such that some nestmates consistently fan at lower temperatures and others at higher temperatures, suggesting that behavioral differences might emerge from differences in sensitivity to temperature (Weidenmuller, 2004). However, outside of this work with bees, few empirical studies been done to show whether or not response thresholds in fact exist and that they regulate division of labor in social insects.

To fill the knowledge gap, we measured the sensitivity Temnothorax rugatulus ants have to two ​ ​ different task-associated stimuli and tested whether or not this sensitivity was correlated to their behavior in the colony under normal circumstances. The response threshold hypothesis posits that the most sensitive individuals to a certain stimulus will be the individuals who specialize in the task associated with that stimulus. For example, the ants that respond low levels of brood pheromone should be more likely to be brood care workers. However, some preliminary experiments indicated that insensitive individuals may be the ones who specialize in a task. This was a wholly unexpected result, as there was no theoretical framework to understand why this would occur. Therefore the “satisfaction threshold” hypothesis was proposed to make sense of these results.

To illustrate the differences between the two hypotheses, consider the following thought experiments. In the first, imagine that there are two roommates sharing a kitchen. The dishwasher is broken, so the roommates agreed to wash the dishes in the sink. One of these roommates is very clean, so he or she washes the dishes when they just start piling up. The other roommate, who has a higher tolerance for dishes, never does the task, as it never reaches the point where he or she is concerned with them. In this colony of two individuals, the person with the lower response threshold (the number of dishes required to initiate a response) ends up becoming the specialist without ever needing to appeal to higher-level cognition.

For the second thought experiment, imagine that these two roommates are now working to fill the fridge with food. One of the roommates loves food, and is not satisfied with a fridge that is only partially filled. He or she will keep working until the fridge is completely filled. The other roommate, who is less fond of food, may be satisfied with a fridge that is only half full, and is therefore never inspired to work. Here again task specialization is achieved without higher-level cognition, as the person with the higher satisfaction threshold (the amount of food necessary to stop performing a task) ends up becoming the specialist.

These thought experiments illustrate that there are at least two different types of task-associated stimuli which have yet to be explored. The fullness of the sink, for example, is an indicator of how much work needs to be done. When the sink is full, this indicates that dishwashing absolutely needs to be done. This subcategory of the task-associated stimulus is called the task initiation stimulus (TIS). On the other hand, the fullness of the fridge is an indicator of how much work has already been performed. When the fridge is full, this indicates that food gathering no longer needs to be performed. This subcategory of the task-associated stimulus is called the task completion stimulus (TCS).

When a signal in the environment is perceived as a TIS, the response threshold hypothesis (or variations in the starting point of a task) is necessary to explain task allocation. When an individual is sensitive to this indicator that a job needs to be performed, they tend to overestimate how much of that signal is present in the environment, which means that they have a lower response threshold. This is akin to overestimating how many dishes are in the sink, which compels a person to start performing them sooner.

On the other hand, when a signal in the environment is perceived as a TCS, the satisfaction threshold hypothesis is necessary to explain task allocation. When an individual is insensitive to this indicator of how much work has already been performed, they tend to underestimate how much of that signal is present in the environment, which means that they have a higher satisfaction threshold. This is akin to underestimating how much food is in the fridge, which compels a person to continue foraging for food.

Sensitivity does not necessarily need to be addressed to create this variation in starting and stopping. It could very well be the case that each individual has a different cognitive rule that correlates with their thresholds. For example, a person may only start performing a task when they know they see 10 dishes in the sink, or they may stop filling the fridge when they see 10 food items. The purpose of this paper, then, is to demonstrate that sensitivity is associated with ​ task allocation, which seems to support the sensitivity-driven view of the thresholds rather than the cognitively-driven view. What is more, it seems that ants may use both response and satisfaction thresholds to organize labor, as for one task-associated stimulus, sensitive individuals performed the task in the colony under normal conditions, which supports the response threshold hypothesis. For the other task, it was the insensitive individuals who performed the task, which supports the satisfaction threshold hypothesis.

Methods

Ant collection, marking, behavior analysis

Colonies of T. rugatulus were collected from the Santa Catalina Mountains, Tucson, AZ at an ​ ​ altitude of about 2134 meters for these experiments. These colonies were housed in artificial nests designed to simulate the nest sites they choose in the wild. These ants live in the spaces in between rocks, so in the lab these colonies were housed in between two large microscope slides with a cardboard perimeter separating the two slides, creating a nest chamber (3.6 cm by 2.5 cm).These nests were set inside a foraging arena (11.5 cm by 11.5 cm) which has fluon painted on the inside of its walls, so as to prevent ants from escaping. They were fed once a week with Drosophila and diluted honey water (1:10). They were kept on a 12 hour life cycle at 21°C. This follows the protocol from Charbonneau et al. 2014.

To allow for identification of individual ants, each ant in these colonies were marked with a unique four-color code combination using Testor’s Pactra paint. To do this, ants were made ​®​ unconscious with a stream of carbon dioxide and were then restrained in a makeup sponge with a slit in it. Paint marks were placed on their head, thorax, and gaster under a dissecting microscope (Leica S6D).

To identify each ant’s task specialization, baseline behavior of each individual ant was found . Their behavior was recorded for 10 minutes at random times between 8:00 AM and 5:00 PM on 3 non-consecutive days over a period of a week (over which behavior is consistent, Charbonneau and Dornhaus 2015). Video analysis tracked the behavior of every individual ant. For each second of the video, their behavior was placed into one of these categories: self grooming, grooming other, getting groomed by other, foraging, brood care, wandering inside, working outside, inactive, building, trophallaxis, and eating. The proportion of time they spent performing each task was calculated. Definitions for these tasks are provided in Table 1, which was adapted from Charbonneau et al, 2015.

Table 1 Task Definition Nest building Manipulating a stone in any way Brood care Manipulating brood (feeding, grooming, moving) Self-grooming Grooming itself Grooming other (giver) grooming another ant Grooming other (receiver) Be groomed by another ant Trophallaxis Receive or give trophallaxis Eating Feeding on drosophila inside nest Working outside Wandering outside nest (includes foraging behavior) Wandering inside nest Anytime an ant is mobile inside the nest wall but is not engaged in any task Inactive Immobile, not engaged in any tasks

Stand-alone Sucrose Assay

Three queen-right T. rugatulus colonies were collected September 2015 from the Catalina Mountains, Tucson, AZ at an elevation of 2134 meters. They were housed and painted as described above, and their behavior was analyzed using the above protocol.

To test response thresholds to different sucrose concentrations we secured each ant in a foam make-up sponge with its head sticking out and antennae accessible and allowed to acclimate for 5 minutes. Thresholds to sucrose were determined using the maxilla-labium extension response (Guerrieri and d’Ettore 2010). Each ant was then presented with a series of 8 linear logarithmic ascending concentrations of sucrose solution, similar to Page et al 1998 (0.1%, 0.3%, 1%, 3%, 10%, 30%, 50% w/v). Each stimulus was presented for a duration of 2 seconds by infusing a toothpick with the sucrose solution and then touching it to the right antenna. To prevent the accumulation of sugar on the antenna and to control for habituation to the increasing concentrations of sucrose we applied water to the antenna before each stimulus presentation, allowing us to also calculate a water responsiveness score. Ants were tested with each concentration in groups of six at a time to allow for an interval of ~ 5 minutes between concentrations. After stimulus presentation each ant was given 20 seconds to exhibit the extension response, after which time any response was not counted. If an ant responded, we recorded the latency of its response from the time of stimulus presentation. (Protocol adapted from Perez et al 2013 and Falibene and Josens 2012). Two of these sucrose trials were performed with an intertrial interval of 24 hours. Following the second trial ants were fixed in 4% formaldehyde and stored at -20 C for further processing.

Stand-alone brood assay

One queenright T. rugatulus colony was collected in March of 2016 from the Catalina ​ ​ Mountains, Tucson, AZ, at an elevation of 2134 meters. They were housed, painted, and their behavior analyzed as described in the portion of the methods section.

To perform the experiments, each ant was individually placed in arena made of a fluon-coated disposable medicine cup (10.64 cm^2 area, 3.8 cm tall) and was allowed to acclimate for 5 minutes. Ants were then presented with a “low” stimulus of one pupa, delivered to the area via a funnel that ensured delivery of the stimulus to the exact center of the arena. 15 minutes later a second (i.e. “high”) stimulus was presented to each ant by delivering a second pupa which had been starved (by secluding outside the natal nest) for three hours.

All pupae were obtained randomly from one of 8 “feeder” lab colonies *LOOK FOR EFFECT OF FEEDER COLONY IF YOU HAVE THAT DATA!, as we know that workers will accept intraspecific, nonnestmate brood (Forel 1874; Fielde 1903) and we did not want to disturb the experimental colony by removing its own brood. Pupae were not reused across trials. Between trials each arena was cleaned with 90% ethanol, rinsed with water and then dried to remove any residual odors/chemicals deposited by/from the previous ant.

We decided to use pupae because in social , larvae are generally the end-users of resources and the only brood developmental stage requiring food, and they are able to signal their hunger level to workers (Ulrich; Cassill and Tschinkel 1995; Creemers et al. 2003; den Boer and Duchateau 2006; Kawatsu 2013). The number, size, and hunger level of larvae can thus be expected to be major drivers of (sic) brood care.

A positive response was indicated by the focal ant grooming, feeding or picking up the brood (i.e. performing brood care) within the first 5 minutes of stimulus presentation. Latency to respond, duration of response, and number of “brood care” response bouts were also recorded. As with the sucrose assays, two trials were performed with an intertrial interval of 24 hours. Following the second trial all ants were fixed in fixed in 4% formaldehyde and stored at -20 C for further processing.

Colony context: increasing workload

Two queenright colonies of T. rugatulus were collected in October of 2016 from the Catalina ​ ​ Mountains, Tucson, AZ, at an elevation of 2134 m. They were housed, painted, and their behavior analyzed as described in the portion of the methods section. These colonies were used for the experiments described below.

After the behavioral analysis, large amounts of “work” were presented to each colony to see which ants responded to this increased workload. In one experiment, large amounts of brood from other colonies were introduced to the test colony. Previous studies have shown that brood items of some ant species are readily tolerated by non-nestmate workers and are reared to ​ adulthood (Krag et al, 2010). Preliminary experiments demonstrated that this also occurs in T. ​ ​ rugatulus as well. Therefore, in these workload experiments the ants should have only been able ​ to deduce that there was much more brood pheromone in the colony after the introduction of many new brood items. In the other experiment, filter paper, saturated with fungal spores, were introduced to the colony, which was a sign that much more cleaning needed to be done.

These experiments were done to determine which ants were responsive to this workload and to see if this activity correlated with their response thresholds. The results of this experiment are not reported here, however, it should be noted that these experiments took place. It has been hypothesized that exposure to task-associated stimuli can change response thresholds (Theraulaz et al, 1998), so it is possible that these experiments may have altered the results of the threshold assays. It is not clear, though, whether or not there was any such effect.

Brood care assay

Sensitivity to the task-associated stimulus brood pheromone was measured by placing each ant into an arena and presenting it with a low stimulus: a larva freshly picked from the ant’s colony. We then presented the ant with a high stimulus: a 3-hour starved brood larva taken from a separate “feeder colony.” The arena was made of a disposable medicine cup (10.64 cm^2 area, 3.8 cm tall) with the walls of the cup coated in fluon to prevent escape. Ants were placed into the bottom of the cup and were allowed to acclimate to the arena for five minutes. Brood was then added directly to the center of the arena by using a funneled lid. Their behavior was then recorded for 5 minutes. The high stimulus (starved larva) was then introduced to the arena and behavior was recorded for another five minutes. After the assay, ants were then moved to a new nest. To remove the scent of the previous brood item and ant, each arena was cleaned with 90% ethanol, rinsed with water and then dried to remove any residual odors/chemicals deposited by/from the previous ant between trials.

The behavior of the ants fell into one of two categories, either it was performing brood care or it was not performing brood care. Brood care was defined as any interaction that the ant had with the brood that lasted more than five seconds. This behavior includes antennation, active feeding, and moving of the brood.

Fungal grooming assay

Sensitivity to hygiene-related stimuli was measured by placing an ant into an arena (as described above) and then dusting it with fungal spores. Like in the previous experiment, ants were removed from their colony and placed individually into the arena for five minutes to allow for acclimation. As a low stimulus ants were first dusted with .005 grams (i need to check this--this isn’t right. I don’t remember the amount of the top of my head but I have it written down. Let me know if you need it) of the fungal spores were dusted onto them using a round nylon 25mm paint brush (give diameters of brush. Again, let me know if you need this). Their behavior was then recorded for 5 minutes. As a high stimulus another .01 grams of fungal spores were dusted onto them and behavior was recorded for another 5 minutes.

The behavior of the ant fell into one of two categories. The ant was either self-grooming to remove the spores from its antenna and body or it was not self-grooming. Self grooming was defined as any behavior where the ant extended its mouthparts to any part of its body for more than five seconds. The fungus in the genus Aspergillus flavus (what is the full scientific name?) ​ ​ was grown in culture grown in acidified potato dextrose agar at room temperature and 30% humidity in a climate-controlled room with a 16-hour cycle of fluorescent light, courtesy of Barry Pryor, University of Arizona) Sucrose assay

The third response threshold assay measured sensitivity to sucrose by exposing ants to two different concentrations of sucrose and recording whether or not they had a maxilla-labium response. It has been shown in Camponotus ants that when the ant detects sugar in the ​ ​ environment, they will extend their maxilla-labium in order to absorb the sugar (Fernando 2010). Preliminary experiments indicated that T. rugatulus have the same response. In this assay, ants ​ ​ were restrained in the slits of makeup sponges (as described for paint marking), allowed to acclimate to the sponge for five minutes and placed under a dissection microscope. As a low stimulus, 0.1% sucrose was applied to their antenna with a saturated toothpick. A response was indicated by the ant extending its mouthparts within 20 seconds of stimulus application. Following the low stimulus, a high stimulus of 50% sucrose (w/v) was applied to the antenna.

Following the sucrose assay all ants were fixed in 4% formaldehyde and stored at -20 C.

Results

Variation in starting task performance and task allocation

The response threshold hypothesis posits that variation in the starting point of a task creates variation in task allocation. Therefore, the time it takes to start performing a task (latency) should correlate with the amount of time the ant spends doing that task under normal circumstances. Additionally, this relationship should be negative, as those with the smallest latency should be the ones who specialize in the task. Under the satisfaction threshold hypothesis, though, the starting point does not drive task allocation and is a random quantity, so there is no relationship between latency and the amount of time spent on the task.

In both assays, the relationship appears to be random. Figures 1 and 2 plot the amount of time it took for ants to react to the first stimulus against the proportion of time ants spent working on the respective task in the colony setting. A linear regression was performed on each plot, and both were insignificant.

Fig. 1: Linear regression between latency of brood pheromone assay and the proportion of time spent performing brood care. N = 116 and P = .059. This supports the satisfaction threshold hypothesis.

Fig. 2: Linear regression between latency of fungal spore assay and the proportion of time spent grooming. N = 122 and P = .171. This supports the satisfaction threshold hypothesis.

Variation in stopping task performance and task allocation

The satisfaction threshold hypothesis posits that variation in the end point of a task (duration) creates variation in task allocation. Therefore duration should correlate with the amount of time the ants spend doing the task under normal circumstances. What is more, this relationship should be positive, as those who have the highest duration should be those who specialize in the task. Under the response threshold hypothesis, though, the endpoint does not drive task allocation and is a random quantity, so there is no relationship between latency and the amount of time spent on the task.

In the brood care assay, there is a positive relationship between duration in the brood pheromone assay and the amount of time spent performing brood care, which satisfies the satisfaction threshold prediction. On the other hand, there is no relationship between the duration of self grooming in the fungal assay and the amount of time they spend grooming under normal circumstances, which satisfies the response threshold prediction. Figures 3 and 4 plot these relationships.

Fig. 3: Linear regression between duration of brood care in brood pheromone assay and the proportion of time spent performing brood care in the colony. N = 116 and P = .031. This supports the satisfaction threshold hypothesis.

Fig. 4: Linear regression between duration of brood care in brood pheromone assay and the proportion of time spent performing brood care in the colony. N = 122 and P = .487. This supports the response threshold hypothesis.

Brood pheromone thresholds and brood care

The first brood item in the assay represents the normal amount of stimulus the ant can expect to find when it is inside the colony, as this is the level of pheromone a brood releases when it is being cared for. Under the response threshold hypothesis, the ants that are sensitive to brood pheromone at this low level of stimulus are going to be the ants that respond to it the quickest and the most often, as the brood pheromone is a TIS. Individuals who are less sensitive to the stimulus shouldn’t be performing brood care when the stimulus level is so low. The second brood item, however, represents a much higher stimulus level. Ants who are moderately sensitive to brood pheromone, who may not have been responsive to the weaker stimulus, should be responsive to this higher stimulus. Ants who do not respond to either stimulus level are the least sensitive and should not be performing brood care in the colony. Therefore, the ants were categorized into three groups based on which stimuli, if any, they responded to within the first 3 minutes following presentation of the stimulus. In the first group, the low threshold group, individuals either responded to the low stimulus or to both the low and high stimuli. In the high threshold group, individuals only responded to the high stimulus. The third group was the non responsive group.

The opposite prediction is made with the satisfaction threshold hypothesis. There brood pheromone is a TCS, so the insensitive individuals should be the ones that specialize in a task. Figure 5 supports this prediction, as the no response workers are the ones who spend the most amount of time performing brood care, followed by the high threshold workers.

Fig 5. Ants were divided into three groups based on their sensitivity to brood stimulus. This is compared to the proportion of time each ant spent performing brood care in the nest under normal conditions. Kruskal-wallis test: P = .011

Fungal spore threshold and grooming

The logic of this experiment follows the logic of the first. The first dose of fungal spores represents a smaller stimulus level of some foreign body clogging the pores on its body. Preliminary experiments indicated that these grown under these conditions were not toxic to T. ​ rugatulus, so they act as a stand-in for any dirt-like substance that can coat an ant’s body. Under ​ the response threshold hypothesis, the ants that are sensitive to the presence of these foreign bodies should be the individuals who respond the quickest and the most often, and thus would become cleaning specialists in the colony. Individuals who are less sensitive to the stimulus shouldn’t be performing grooming at this stimulus level. The second dose of spores, however, represents a much higher stimulus level. Ants that are moderately sensitive to foreign bodies, who may not have been responsive to the weaker stimulus, should be responsive to this higher stimulus. Ants who do not respond to either stimulus level are the least sensitive and should not be performing grooming in the colony. Again, the opposite prediction is made by the satisfaction threshold hypothesis, where fungal spores would be a TCS rather than a TIS.

Like with the brood pheromone assay, the ants were separated into the high threshold, low threshold, and non responsive groups based on their response within the first 3 minutes of stimulus presentation. Figure 3 shows how these three groups compare in the proportion of time they spent grooming . “Grooming” here is defined as any grooming activity, which includes grooming themselves, grooming others, and getting groomed by others. As the low threshold workers are the ones who spend the most time performing the task, the response threshold hypothesis is supported.

Fig 6. Ants were divided into three groups based on their sensitivity to brood stimulus. This is compared to the proportion of time each ant spent grooming in the nest under normal conditions. Kruskal-wallis test: P = .041

Sucrose threshold and foraging

Sensitivity to sucrose has been shown to be a predictor of foraging behavior in other social insects (Page et al 1998), and it was the purpose of this assay to see if there were any similar links between T. rugatulus foraging behavior and their sensitivity to sucrose. Unfortunately, only ​ ​ 10 ants happened to forage during our video recordings, and only 2 survived long enough for their sensitivity to sucrose to be measured.

Discussion

This paper demonstrates that variation in the endpoints of a task and insensitivity to the task-associated stimulus drive task allocation for brood care. It is therefore reasonable to conclude that brood care is, in fact, driven by this new mechanism of satisfaction thresholds. Additionally, these results indicate that the traditional way of viewing brood pheromone is backwards, at least for T. rugatulus. Instead of being a signal that elicits behavioral responses ​ ​ from adults (Vander Meer et al, 1998), which is here classified as a task initiation stimulus, it could be a signal that stops a response after it has been initiated, or a task completion stimulus.

On the other hand, the response threshold hypothesis successfully predicts the results of two out of the three lines of investigation done with the fungal assay. This indicates that fungal spores are a traditional TIS. Task allocation in this domain, then, is driven by response thresholds.

Just as humans react to a full sink differently than they would a full refrigerator, ants too seem to be capable of processing multiple types of task-associated stimuli. To only refer to one type of signal or another would be to create an incomplete and somewhat confusing narrative of how division of labor can arise in social insects. For example, Pankiw and Page found that the response thresholds of preforaging bees to sucrose successfully predicted the type of foraging they would later perform, be it foraging for water, nectar, or pollen (Pankiw and Page, 2000). Here, individuals with the lowest response thresholds foraged for water, then the next highest group foraged for pollen, and the highest group foraged for pollen.

Pankiw and Page interpreted these results as supporting evidence for the response threshold hypothesis, however this does not quite seem to follow logically under the traditional paradigm of response thresholds. If sucrose is a TIS, or a signal for how much work needs to be done, then why would the insensitive workers be the ones who forage for nectar? This is like underestimating the number of dishes that are in the sink, but doing then them anyway. Instead, it seems more plausible to claim that sucrose is a TCS. The more of it that is present in the colony, the less work needs to be performed. If a bee underestimates how much sucrose is present in the colony, the more likely she is to go forage for nectar. This insensitivity to the task associated stimulus supports the satisfaction threshold hypothesis, although nothing definitive can be said until someone analyzes the starting and stopping points of foraging of bees.

Acknowledgements

Pryor lab, Bree Rodriguez, Alexis Morrison, NSF grant

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