Robbing Behavior
Honey bee robbing behavior may take two different forms
Clarence Collison
Honey bee robbing behavior may take two different forms: stealing honey from hives that are unable to defend themselves during a nectar dearth, and collecting nectar from some flower species without making contact with the reproductive organs after carpenter bees have made slits in the flower petals (corolla). Robbing may also become involved in the transmission of Varroa mites and diseases between colonies. “When nectar sources are scarce or unavailable locally, honey bees are attracted by honey in neighboring hives. They make raids on hives that are unable to defend themselves and steal their honey or sugar syrup. Bees will never rob during a nectar flow as long as an abundance of nectar is available in the field. Robbing intensity depends upon the availability of natural sources of food, the more scarce or unavailable nectar becomes, the more the intensity of robbing increases. It is the strong colonies that make onslaughts on the weak ones or those that are poorly guarded (have few guards). The robber bees are the forager bees. They are after honey – they do not steal pollen. The tendency to rob varies with the race and strain. Italian bees are much more prone to rob than the brown or black races. Robbing may occur between colonies in one apiary or colonies of different apiaries. Sometimes it is possible to see several colonies in the apiary robbing one another simultaneously. Robbing behavior is usually more aggressive than normal and can develop into deadly fighting and the destruction of a hive. Robber bees are nervous, noisy, and fly timidly and shiftily. They alight cautiously on the alighting board at the entrance and dodge the guards that catch them. Robbing starts with the robbers forcing their way into a hive, taking their fill of honey/sugar syrup, and flying off. Upon returning to their hive, they alert their hive-mates to the honey source and taste and recruit a large number of bees to take advantage of this honey. The recruited bees are attracted to the scent of honey which is emitted from the entrance of the hive or any open spaces between supers. They frantically hover up and down before the entrance attempting to enter the hive. When robbers are about, the local bees will be actively on guard chasing away intruders who seek entrance. Combats will take place between the robbers and defenders of the hive leading to the death of a large number of bees from both colonies. Should the robbers succeed in overpowering a colony, they will strip it of all its honey; they rip the caps off the honey in the combs and sip the honey, leaving the surface torn and messy” (Hamdan 2010).
At the colony level, robbing is characterized by a conspicuous increase in foraging activity, requiring a concomitant increase in food storing abilities. Nectar foragers do not directly store their nectar load, but instead transfer it to receiver bees. The length of time a forager waits for a receiver affects the speed at which that forager leaves for another trip. During robbing, the rapid increase in foraging trip rate (Grume et al. 2021) likely requires rapid, increased recruitment of receiver bees (Seeley 1989), and possibly a change in the feedback mechanism that regulates foraging activity. The robbing colony’s defensive specialists also have been implicated in the syndrome (Grume et al. 2021). Guard bees are specialists who defend against invading robber honey bees. Guards smell odors on incoming foragers and chase away non-nestmates (Breed et al. 1995). Unsurprisingly, experiencing robber intrusion results in increase victim colony guard numbers and higher rates of non-nestmate rejection (Couvillon et al. 2008; Downs and Ratnieks 2000). However, guards from robbing colonies that have not experienced such intrusions can also elevate their defensiveness, even towards their own foragers (Grume et al. 2021), (Rittschof and Nieh 2021).
In honey bee colonies, foraging and nest defense behaviors are performed by similar-aged bees, and so hives must adjust their workforce investment to fulfil both tasks. Grume et al. (2021) investigated this balance in the context of honey robbing, a tactic in which foragers invade a victim hive, kill worker bees and steal honey stores. Robbing is highly beneficial because stored honey is a plentiful, concentrated food resource. However, robbing requires a large workforce to overwhelm the defenses of the victim hive; it is unknown how robbing hives adjust other behaviors to accommodate this demand. A method was developed to provoke a hive to engage in simulated robbing so rapid changes in foraging activity and nest defense could be measured. Surprisingly, robbing hives increased both behaviors. Guards, the individuals responsible for nest defense, specifically increased defensiveness towards their own nestmates as they returned from a robbing trip. They found that increased foraging activity and changes in forager odor profiles from prolonged exposure to victim hive honeycomb were insufficient to explain robbing-induced changes in guard defensiveness. However, brain gene expression profiles of robbing foragers suggest these bees are unusually aggressive, and thus more likely to provoke aggression from nestmate guards. Increased forager aggression occurred even in the absence of direct competition with victim bees. Thus, although increased guard defensiveness may be costly in terms of increased nestmate mortality because the ecological conditions that promote robbing simultaneously increase the likelihood a hive will become a robbing target, guards may use cues from returning nestmates to determine invasion risk and adjust their defensiveness accordingly. These results suggest that colonies use social information to dynamically optimize both foraging and defensiveness in order to maximize the benefits and minimize the costs of this high-risk tactic (Grume et al. 2021).
Guard bees are primarily responsible for preventing robbing. Previous research has shown that the probability of both nest-mate and non-nest mate workers being accepted by guards at the nest entrance increases as nectar availability increases. The mechanism responsible for this change in guard acceptance may be explained by two competing hypotheses: Odor Convergence and Adaptive Threshold Shift. In this study the Odor Convergence hypothesis was tested. The acceptance by guards at the nest entrance of workers transferred between four colonies that had been fed either odorless sucrose syrup (two colonies) or diluted heather honey (Calluna vulgaris) (two colonies) was measured for three days before feeding and during two weeks of feeding. Despite the large sample sizes, the probability of guards accepting non-nest mates was not affected by the similarities or dissimilarities in food odor between guards’ and non-nest mates’ colonies. This finding contrasts with the accepted wisdom that food odors are important in nest mate recognition and the data, therefore, strongly reject the Odor Convergence hypothesis (Downs et al. 2001).
In the colony, entrance guards distinguish between nestmates and intruders. Those below a threshold of dissimilarity are accepted. However, the threshold is dependent on ecological conditions and may shift to become either restrictive or permissive, depending on the frequency of intrusion and cost of admitting an intruder. Previous research has shown that both the number of guards and their acceptance threshold to conspecific non-nestmates can change dramatically over weeks owing to changing nectar availability and robbing intensity. Couvillon et al. (2008) investigated whether these changes could also occur rapidly, over minutes, in response to sudden increases in conspecific intruders (robber bees). They induced high levels of intrusion at nest entrances and determined changes in the number of guards, the number of fights per guard, and the acceptance thresholds of guards. Their results showed a rapid response within 15 minutes. At the level of individual guards, acceptance declined from 83 to 55% for nestmates and 67 to 43% for conspecific non-nestmates. Also, per individual guard, mean fights increased from 0.005 to 0.06 fights/guard. At the colony level, the mean number of guards at the entrance rose from 1.9 to 2.3, and overall acceptance in a three minute trial declined from 74 to 52% for nestmates and 59 to 30% for conspecific non-nestmates. These results show that honeybees can make rapid behavioral shifts at both the colony and the individual levels.
When honey bee colonies collapse from high infestations of Varroa mites, neighboring colonies often experience surges in their mite populations. Collapsing colonies, often called “mite bombs,” seem to pass their mites to neighboring colonies. This can happen by mite-infested workers from the collapsing colonies drifting into the neighboring colonies, or by mite-free workers from the neighboring colonies robbing out the collapsing colonies, or both. To study inter-colony mite transmission, six nearly mite-free colonies of black-colored bees were positioned around a cluster of three mite-laden colonies of yellow-colored bees. The movement of bees between the black-bee and yellow-bee colonies before, during, and after mite-induced collapse of the yellow-bee colonies was monitored. Throughout the experiment, they monitored each colony’s mite level. They found that large numbers of mites spread to the black-bee colonies (in both nearby and distant hives) when the yellow-bee colonies collapsed from the high mite infestations and became targets of robbing by the black-bee colonies. They concluded that “robber lures” is a better term than “mite bombs” for describing colonies that are succumbing to high mite loads and are exuding mites to neighboring colonies (Peck and Seeley 2019).
Robbing is a route of disease transmission that probably occurs at significant levels both under managed and natural conditions. However, bees generally rob only when there is little available foraging opportunities in the field, and they are only able to invade weak colonies. When outside food sources become scarce, guard bees in strong colonies usually detect and repel intruding bees from other colonies. On the other hand, when colonies become diseased and weakened, guarding becomes ineffective and robbing bees easily enter a sick colony where they may encounter pathogens. A robber bee brings pathogens back to its own nest on the surface of its body, or in robbed honey stored in its crop. An infected robber could also infect the visited colony with pathogens on its body, although this route of infection seems less likely (Fries and Camazine 2001).”
Surprisingly little is known about transmission rates between honey bee colonies of Paenibacillus larvae, the causative agent of American foulbrood. Lindström et al. (2008) studied the rate of horizontal transmission of P. larvae spores between colonies as a function of physical distance between colonies by culturing for the spores from sequential samples of adult bees. The results demonstrate a direct effect of distance to clinically diseased colonies on the probability of contracting high spore levels, as well as on the probability of developing clinically visible disease symptoms. The results also demonstrate that colonies may develop considerable spore densities on adult bees without exhibiting visible symptoms of disease. Furthermore, the data suggest that transmission of AFB between apiaries occur within a one km distance from clinically diseased colonies but is significantly lower at two km distance or longer when colonies dead from AFB are allowed to be robbed out (Lindström et al. 2008).
Nectar robbing is also a problem in the pollination of some plant species. “In Hawaii, a carpenter bee (Xylocopa sonorina) and the honey bee use floral perforations to obtain nectar. With its maxillae, X. sonorina perforates corollas and calyces of introduced plant species; in corollas of different lengths and diameters, the perforations made are significantly different in length. Through these perforations, X. sonorina imbibes nectar without pollinating the flowers. Old and New World Xylocopa spp. perforate the flowers of at least 22 families. Honey bees obtain nectar through these perforations made by X. sonorina. Elsewhere in the world, honey bees use previously made perforations in flowers to obtain nectar from at least 10 plant families. These bees are “robbers” of some plants in that they take floral provisions in ways that are unlikely to effect pollination” (Barrows 1980).
Honey bees probe for nectar from robbery slits previously made by male carpenter bees, Xylocopa virginica (L), at the flowers of rabbiteye blueberry, Vaccinium ashei Reade. This relationship between primary nectar robbers (carpenter bees) and secondary nectar thieves (honey bees) is poorly understood but seemingly unfavorable for V. ashei pollination. Two studies were designed to measure the impact of nectar robbers on V. ashei pollination. First, counting the amount of pollen on stigmas (stigmatic pollen loading) showed that nectar robbers delivered fewer blueberry tetrads per stigma after single floral visits than did the benchmark pollinator, the southeastern blueberry bee, Habropoda laboriosa (F.), a recognized effective pollinator of blueberries. Increasing numbers of floral visits by carpenter bee and honey bee robbers yielded larger stigmatic loads. As few as three robbery visits were equivalent to one legitimate visit by a pollen-collecting H. laboriosa female. More than three robbery visits per flower slightly depressed stigmatic pollen loads. In a second study, a survey of 10 commercial blueberry farms demonstrated that corolla slitting by carpenter bees (i.e., robbery) has no appreciable affect on overall V. ashei fruit set. Their observations demonstrate male carpenter bees are benign or even potentially beneficial floral visitors of V. ashei. Their robbery of blueberry flowers in the southeast may attract more honey bee pollinators to the crop (Sampson et al. 2004).
Carpenter bees (Xylocopa spp.) act as primary nectar thieves in rabbiteye blueberry (Vaccinium ashei Reade), piercing corollas laterally to imbibe nectar at basal nectaries. Honey bees learn to visit these perforations and thus become secondary nectar thieves. Dedej and Delaplane (2005) tested the hypothesis that honey bees make this behavioral switch in response to an energetic advantage realized by nectar-robbing flower visits. Nectar volume and sugar quantity were higher in intact than perforated flowers, but bees (robbers) visiting perforated flowers were able to extract a higher percentage of available nectar and sugar so that absolute amount of sugar (mg) removed by one bee visit is the same for each flower type. However, because perforated flowers facilitate higher rates of bee flower visitation and the same or higher rates of nectar ingestion, they are rendered more profitable than intact flowers in temporal terms. Accordingly, net energy (J) gain per second flower handling time was higher for robbers on most days sampled. They concluded that the majority evidence indicates an energetic advantage for honey bees that engage in secondary nectar thievery in V. ashei.
A two year study was conducted to assess how nectar robbing in honey bees affects fruit production in rabbiteye blueberry. Various harvest parameters were measured from fruit collected from plants tented with honey bees and carpenter bees (AX), carpenter bees (X), honey bees (A), no bees (0), or in open plots (open). In open plots, rates of illegitimate honey bee flower visitation increased from initial lows to fixation at > 95%. Fruit set is higher in open, A, and AX plots than in X and 0 plots. Even though fruit set is similar in A and AX plots, seed numbers are significantly reduced in AX plots in which X. virginica-induced illegitimate honey bee flower visitation approaches 40%. Open-pollinated berries were larger than berries from all other treatments in 2001, whereas in 2002 berry weight followed the pattern A > open > AX > (X≈0). Sucrose content of juice and speed of ripening were unaffected by treatments (Dedej and Delaplane 2004).
References
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Clarence Collison is an Emeritus Professor of Entomology and Department Head Emeritus of Entomology and Plant Pathology at Mississippi State University, Mississippi State, MS.