Introduction

The aim of the present paper is to investigate the semiotically mediated human-bee communication in the practice of meliponiculture in Brazil.

Meliponini, most commonly known as stingless bees, are a diversified tribe, even more so than the Apini (honeybees), represented by numerous species and genera (Michener, 1974: 329; Frisch, 1967: 306). More than 600 species of Meliponini in over 55 genera have been categorized in tropical and subtropical regions (Cortopassi-Laurino et al., 2006: 275), being the most common pollinator bees in the American tropics, especially south of the equator (Michener, 1974: 346; Frisch, 1967: 306).

Before the Europeans colonized the Americas, the practice of rational kee** of stingless bees was already carried out (Barbieri & Francoy, 2020: 2) since the ancient Maya civilization, who acknowledged these bees as a vital part of social, economic, and religious life (Cortopassi-Laurino et al., 2006: 276). In Brazil, the largest country of South America, native indigenous societies such as the Kayapó have also been practicing beekee** for centuries, being aware of many details regarding Meliponini behaviour, characteristics of nests and nest types, as well as different species and their respective ecological zones (ibid.). Hence, it is possible to state that humans have not only been living along, but also actively interacting with stingless bees in a rational manner for eras.

In the 1950’s, researcher Paulo Nogueira Neto coined the term ‘meliponiculture’ (Nogueira-Neto, 1997) to designate this ancient practice of stingless bee beekee**, an activity which is still, to this day, undertaken by traditional and indigenous communities (Barbieri & Francoy, 2020: 2). This way, the characteristics of meliponiculture as an enterprise vary from region to region, being intrinsically tied to traditional knowledge (Cortopassi-Laurino et al., 2006: 275). Even though it might still be largely carried out by traditional communities, especially in Brazil, it is an activity constantly permeated by innovation. Meliponini beekeepers are not just appliers of traditional knowledge, but also developers of new tools and techniques, something which is needed in order to account for the enormous species diversity (Barbieri and Francoy 2020: 7–8).

As eusocial insects, Meliponini inhabit permanent colonies which are majorly comprised of thousands of individual bees (Michener 1974: 329). In a similar or parallel manner, meliponiculture is a highly social activity, where the innovation which occurs empirically is actively shared either through online social media or on meliponiculture-focused events (Barbieri & Francoy, 2020). As such, researchers consider meliponiculture as being a bridge that connects traditional knowledge to innovation and novelty, as well as a link “between basic education and scientific development” (ibid, 7).

Considering the importance of meliponiculture as a “significant activity that permits sustainable agricultural development and wildlife conservation” (Cortopassi-Laurino et al., 2006: 288), as well as the importance of Meliponini as being “among the major pollinators in the tropics” (Michener, 1974: 346), further studies surrounding this field are regarded as pertinent. More specifically, bearing in mind that humans have been dealing with Meliponini for more than four thousand years, it behoves the biosemiotician to study this relationship.

As put by Sebeok (1990:107),

How man and animals communicate with one another poses all sorts of interesting problems which require a great deal more study. Man may encounter animals under a wide variety of circumstances that make it necessary for each party to learn – even if never entirely master – the essential elements of the other’s code. (Sebeok, 1990: 107)

There are many studies on human-animal relations and communication, such as the long-established studies by Jared Diamond, focusing on domesticated animals (namely dog, sheep, cow, and horse). Parallelly, the content of bee intra-specific communication has been subject of great interest ever since the 1920’s with the Austrian ethologist Karl von Frisch. Nevertheless, there is a gap when it comes to studies that consider the communication and relationship between humans and bees, even though the two have, as stated in this introduction, a steady and ancient history together. Hence, this paper aims to start the investigation on this relation, which will by no means be finished here.

Hence, the general questions that drive the present research are:

  • Is it possible to state that there is a semiotically mediated intra-specific communication between humans and Meliponini?

  • If yes, how so?

To answer these, it is necessary to break down the first question into the following:

  1. a.

    In the context of the coexistence between humans and Meliponini, is there the possibility of a shared code?

  2. b.

    How do stingless bees sense the passage of time?

  3. c.

    Are stingless bees domesticated animals?

Accordingly, this paper is organized in the following manner: section 2 describes the materials and methods used in the research process. The next section (3.1) introduces some problems that may be encountered regarding inter-specific communication, mainly the matter of code, as well as some concepts that must be considered in this scenario. Subsequently, to try and identify what is meaningful for bees, or what is present in their umwelt that could be in common with their human handlers, section 3.2 offers a description of the biological makeup of stingless bees based on what is known of their inter-specific forms of communication. Still in search of the possibility of a shared code (question a. above) that would allow communication between humans and Meliponini to happen, section 3.3 investigates some aspects of chemical signals, and inquires on a bee’s the notion of time (question b.), as well as how that knowledge can be used in communication. Finally, section 3.4 presents a brief discussion on whether bees can or cannot be considered a domesticated species (question c.).

Methodology

Semiotics is, as has been pointed out by Sebeok (2001: 27–28), “classifiable as that pivotal branch of an integrated science of communication to which its character as a methodical inquiry into the nature and constitution of codes provides an indispensable counterpoint” (Sebeok, 2001: 27–28). Given the nature of the present study, the works of Sebeok (1967, 1990, 2001) were used as the main methodological guide. Therefore, the focus here is on codes, signs, and processes of signification that would underlie the possible communication between humans and stingless bees.

More specifically, this paper aims to develop a zoosemiotic model, meaning that it is among the objectives of this work to characterize not only what bees know, but how they know. As put by Kull (2014: 51), “zoosemiotic models […] characterize certain types of knowledge acquisition and knowledge application. These types can be related to different types of learning, inheritance (memory), and acting”.

At the same time, the works by Frisch (1950, 1967), Lindauer (1971), and Michener (1974) comprise the main theoretical framework regarding bee physiology, biology, and behaviour, both in the more general sense of the insect and, specifically, of Meliponini species. Besides these authors, this paper also draws on behavioural ecology literature, namely the works by Chittka (2017), Chittka and Rossi (2022), Hölldobler and Wilson (2009), and Jackson, Holcombe, and Ratnieks (2004).

As a means of complementation, an interview was carried out with a Brazilian researcher whose specialization is meliponiculture. Celso Barbieri is a Sustainability PhD researcher on the School of Arts, Sciences, and Humanities from the University of São Paulo. With a Bachelor’s in Environmental Management, Barbieri works in the areas of conservation of Brazilian native bees, citizen science, environmental education, as well as popularization and technification of meliponiculture, teaching various courses and workshops to the general public related to this activity. Barbieri also keeps three different Meliponini bee species at home (Tetragonisca angustula, Melipona quadrifasciata, and Plebeia droryana), and he has had these three hives for eight, seven, and four years, respectively. Hence, the information given by the researcher during the interview allowed for a better understanding of the behaviour of Meliponini and the development of this paper. The complete interview transcript, originally carried out in Portuguese, was translated into English by the author of this paper and is available as Supplementary Information (Online Resource).

Results and Discussion

Regarding Inter-Specific Communication; Concepts and Problems

According to Sebeok (2001: 28–29), “a variety of non-verbal and verbal messages conjoin organisms into a network of relations with each other as well as with the rest of their environment”. As such, living in total isolation is an impossibility since all species must coexist and share ecosystems on certain terms. For that, “animals must have additional codeswitching capabilities, an interspecific communication system” (Sebeok 1990: 106). By ‘codeswitching’, Sebeok is implying the capacity to change from one code to another, where ‘code’ means a set of rules through which messages can be converted from a given sort of representation to a different one. In any given message exchange, the two parties involved in communication should have, at least in part, a common code (Sebeok 2001: 31). Therefore, question a. needs to be asked: In the context of the coexistence between humans and Meliponini, is there possibility of a shared code?

To answer this question, some investigations are necessary. Regarding the study of animal communication, Sebeok (1967: 63–64) once wrote that one of the main problems faced by researchers in the biosemiotics field regards the fact that one is often unsure of the physical channel(s) through which a message is being transmitted. Thus, the first task of a researcher of animal communication “is to specify the sense or constellation of senses employed in the message-processing situations which he[/she] is observing” (ibid.).

The variety of channels used to transmit messages is constrained by environmental conditions and the adaptation context of a species, but perhaps even more importantly, it is also constrained by the specific sensorium of the animal (Sebeok 1990, 2001). The sensory apparatus is what dictates the shapes of signs that the biological makeup of an animal is able to interpret.

There is an array of sources where bees can retrieve information from. Biesmeijer and Slaa (2004: 144) distinguish five major types of information sources, namely: the individual bee, that is, its preferences and memory; the colony, including the physical state of the hive as well as the conditions of the hivemates; individuals from the same hive in the field, meaning hivemates that a bee might encounter outside of the hive; conspecifics, bees from the same species that might be encountered on the field and who are not from the same hive; and heterospecifics, that is, everyone else (as long as they are a part of the bee’s umwelt, naturally).

Thus, it is possible to recognize semiosis as a process of signal exchanges – between a bee and a flower; a bee and its hive; a bee and its nestmates; a bee and a heterospecific, etc – functioning as signs. Yet, for this communication to be truly understood, one must investigate how an emitting organism encodes messages in a channel that links it to the receiving organism and, so, one ought to investigate that organism’s effector and receptor organs.

Therefore, before trying to answer if there is a possibility of a shared code between humans and Meliponini, it is necessary to understand what is allowed by the biological makeup of stingless bees in terms of symbolic transmission of information between members of the same species.

Biological Makeup and Different Forms of Communication

Many consider the honeybee as being “the semiotic species par excellence, possessed, next to our own, of the most elaborate social communication system thus far recognized by ethologists” (Sebeok, 1995: 121). Nevertheless, little is discussed about stingless bees in the field of semiotics, probably due to the fact that Meliponini do not carry out the so-called Waggle Dance, which would be this elaborate communication system quoted by Sebeok in the aforementioned passage. In fact, the communication of Meliponini is entirely different from the famous “language of bees” described by Frisch (1950) regarding the rhythmic dances of the honeybees (Apis mellifera).

Besides, it is important to highlight that communication cannot be reduced to just transfer of information regarding location and quality of food sources (which is the purpose of the Waggle Dance). As eusocial insects, bees of any species need the ability to communicate in order to inform each other about many aspects of life, such as: stating that they belong to the same hive; informing what position one occupies in the social hierarchy; be given instructions of duties that need performing for the well-being of the colony (Lindauer, 1971; Chittka and Rossi, 2022), among others. Strictly speaking, communication as an interchange of signs serves also as a steering mechanism that guides social relations (Sebeok, 1967: 60).

With this broader understanding of the function of communication for bees, it is believed that Meliponini employ a combination of optical, olfactory (chemical), and mechanical signals for the symbolic transmission of information and mutual communication (Lindauer, 1971: 3).

Optical Signals and Visual Apparatus

According to Chittka (2017: R1052), “there is little direct evidence that bees actually perceive images — in the form of little virtual pictures somewhere in the bees’ brain”. Experiments with tethered bees led researchers to believe that their vision is somehow linked to motor patterns, since, when they are presented with an image, bees need to fly along its patterns in sequential scanning motions in order to be able to identify it. In other words, “[a] square could be distinguished from a circle by flying along any small subsection of the edge of the shape” (ibid.).

Further, “bees are faster than most other animals in learning to associate colours with rewards” (ibid.), seeing that colours are extremely meaningful for a species whose nutrition is primarily obtained from flowers. Additionally, bees “have trichromatic colour vision with UV-, blue- and green-receptors” (Chittka et al. 1994: 1489), something that is also reasonable, considering their umwelt. In the work by Chittka et al. (1994), a system was developed to categorize the bee colour space on the perceptual level, that is, the four colour sectors of bee colour vision: UV, UV-green, green, UV-blue. These four sectors do not point to a poor colour vision apparatus, but rather, they comprise “a physical continuum that covers all possibilities between two extreme curve shapes” (ibid.). Bees can perceive plenty of colours. They are only very different from the ones humans see.

There is also another matter when it comes to bee vision, one that is connected to the fact that the environment inside the hive has a lower intensity of light than the one outside. As put by Michener (1974: 60):

We ordinarily think of bees in the sunlit world of flowers in which they fly, generally isolated from one another and their nests, and in which vision is a major guide for orientation. The contrast of this picture with the conditions inside the nest could hardly be more striking. […] [The hive,] where bees spend most of their lives, is a dark place in which they move by walking. (Michener, 1974: 60)

Even though “the entrance to an ordinary hive is very small and virtually no light can penetrate into the labyrinthine recesses between multiple layers of honeycomb” (Griffin 1981: 22–23), one could still argue that ‘virtually no light’ still means some light, and that might just be enough not to render eyes useless. Rigosi et al. (2017:3–4), for instance, have shown how, for the compound eyes of bees, there are “differences in the photochemical and mechanical dynamics underlying the different adapted states of the eye”. These states can be understood as ‘dark-adapted’ (environment inside the hive) and ‘light-adapted’ (outside). This means that, even in the “dark”, bee eyes are still functional, for they are able to perceive even the lowest photon counting.

Lastly, there is something to be said regarding what sort of characteristic of a visual signal is the most meaningful to the bee: shape, size, colour, or a combination of all three? According to Chittka et al. (1994: 1505), the answer is contrast.

A bee that flies over a green meadow and seeks to detect a flower faces a signal-to-noise problem. […] The detectability of an object of a given size is dependent on the degree to which this object generates photoreceptor excitations whose differences from the mean background exceed the noisy fluctuations of the background signals significantly. […] In other words, the detectability of a signal is a function of the perceptual colour difference of this signal to the average background. (Chittka et al. 1994: 1505, my italics)

Therefore, bee vision is limited by this signal-to-noise ratio, not by eye resolution (Rigosi et al. 2017: 4). It was, thus, not by chance, that bee compound eyes evolved to be excellent in the “contrast transfer between the fine details of a visual scene and its retinal image” (ibid.), even increasing contrast gain when the situation requires it.

Mechanical Signals and Tactile Sense Organs

The role of tactile sense organs in communication between bees is extremely central, especially when it comes to the antennae and the joints of the exoskeleton (Griffin, 1981). Inside the hive, most “[a]ctivities are tactually, chemically, gravitationally, or sonically stimulated” (Michener, 1974: 60). In the case of Meliponini, who do not perform the rhythmic dances of the Apini, the energetic jostling of the hivemates (Frisch, 1967: 309) is particularly important in the communication process.

Besides the direct contact between individuals (jostling), tactile sense organs are also involved in how bees interpret sound. It is interesting to think that “the use of sound in the wider scheme of biological existence is rather uncommon” (Sebeok, 1990: 109). This way, for the bee, sound is not perceived as air-borne tones, it is not “heard” in the same way it is with humans, rather it is “felt” only as vibrations of the substrate (Frisch, 1967: 309–310). Similarly, Hölldobler and Wilson (2009: 234) write that, for Hymenoptera, “[m]ost vibrational signals are transmitted primarily through the soil, nest walls, leaves and twigs, and other solid surfaces, rather than through the air.” Therefore, the difference between how humans and bees perceive sound lies in the channel through which the signal is transmitted. For humans, the vibrations are transmitted through the air, whereas for Hymenoptera, they happen through surfaces.

Even though our perceptions of this particular signal (sound) may be intrinsically different given this disparity of channels (air vs. surface), it is still interesting to consider the possibility of phenomena such as cross-modal sensory perception (where a signal meant to be received by one sensory system is involuntarily perceived by another) and how this may provide for the merging of apparently separate umwelten. In other words, just because buzzing sounds are meant to be perceived as substrate vibrations by other bees, it does not mean it is not also received as air vibrations by the auditory apparatus of other species who may learn to recognize this signal as well as attribute meaning to it. Besides, the other way around may also be true. However, Hölldobler and Wilson (2009: 234) also point out that “acoustical communication (more accurately put, vibrational communication) is only weakly developed when compared with communication by pheromones”. The authors go even further stating that, when mechanical signals are employed, they are “usually combined in some manner or other with chemical signals” (ibid.).

Chemical Signals and Olfactory Communication

Olfactory signals take on a central role when communication serves the function of informing the hivemates of a food source. The way Meliponini convey location is, as it was already mentioned, not via Waggle Dance. What happens is that the foragers carry back to the hive the characteristic scent of the food source that was just visited. Newcomers are, then, aroused and induced to fly out by the buzzing sounds (vibrations) and energetic jostling coupled with the perception of the food scent that is distributed by the foragers through the act of jostling (Frisch, 1967: 309). According to Hölldobler and Wilson (2009: 232), vibrational signals “acting in concert with chemical recruitment signals”, can be seen as a “form of multimodal communication”. Furthermore,

Bees have a scent organ located on the abdomen in a pocket of skin lined with glands. Usually, the pocket is closed and cannot give out any scent. But bees returning to a rich source of food open the scent organ as they approach the feeding place and alight upon it. In doing this, they apparently apply to the food source a scent which is very attractive to other bees. It seems to carry the meaning “Come here; this way!“ (Frisch, 1950: 65–66)

The essential difference between Meliponini and other bee tribes lies in the fact that, since they do not practice the Waggle Dance, “Meliponini newcomers are not directed to their goal by information imparted exclusively in the hive (direction and distance information are not even incorporated in their alerting system)” (Sebeok, 1967: 71). Instead, after newcomers have been aroused by the returning forager through means of chemical and mechanical signs, it often so happens in Meliponini species that a guide bee will lead groups of newcomers back and forth from the hive to the food source for several trips (Michener, 1974: 157). Even further, guide bees not only lead the groups, but they also leave an odour trail for the newcomers to follow, in a way that neither optical, mechanical, or olfactory signals are sufficient by themselves, needing to be coupled for the newcomers to be able to locate the food source (ibid.).

It is also worth highlighting that, although the Meliponini guide bee and odour trail, when compared to the Waggle Dance, “may seem less elegant to us, it is just as successful […] and, in at least one respect, superior: communication fails when honeybees are required to report a feeding place much above or below the hive, but not so in the stingless bees” (Sebeok, 1967: 71). That happens since “the trail of odour spots and the guide bee can go up through vegetation as well as along the surface of the ground” (Michener, 1974: 158). Thus, even though the signs employed by Meliponini are less complex (or at least more indexical) than the ones used by the Apini (which are more symbolic), this mode of communication includes a whole axis of information (vertical) that the Waggle Dance fails to encompass, for all their encoding capacity.

Moreover, this type of chemical trail is not exclusive to stingless bees, but rather, it can also be found in other species of the Hymenoptera order. In a study on pharaoh ants (Monomorium pharaonis), Jackson, Holcombe, and Ratnieks (2004: 909) describe how pheromone trails “guide foragers between nest and food”, through “elaborate trail networks” produced by the species (ibid.). The authors show how these ants reorientate themselves within the network of trails by using information that is encoded in the geometry of the trail bifurcations. Through the bifurcation geometry, the ant knows which direction of the trail leads to the nest. This study reveals the great encoding capacity potential of odour trails as a type of communication.

Another very interesting fact regarding the chemical trail left by the guide bee is that the “odour deposited on objects is perceptible to the human nostril too and has the same definite smell as the mandibular gland, which is strikingly developed among the Meliponines” (Frisch, 1967: 311). Indeed, there are many accounts of Brazilian indigenous people, such as the previously mentioned Kayapó, who could also “follow the odour that bees used to mark nesting sites” (Cortopassi-Laurino et al., 2006: 276).

Additionally, regarding olfactory senses, during the interview with Celso Barbieri, one of the questions (Online Resource, question 4) asked the researcher if he thought his bees ‘knew’ him (that is, if they could distinguish him from other animals), to which his answer was: “Yes, they know us by smell”. Further along the interview (Online Resource, question 6), the researcher also pointed out that his bees do not present any risks to him, meaning that he doesn’t have to worry about using protective gear when dealing with the hives he keeps at home or the ones he cares for in the University of São Paulo campus. When asked why those bees do not bite him (Online Resource, question 7), Barbieri’s answer was: “As they get used to your presence and smell, they stop identifying you as a threat”.

Therefore, it is stated that bees can not only recognize humans based on scent, as well as profile that scent as ‘threat’ or ‘not a threat’. Meanwhile, it is known that humans are able to recognize the distinct smell from the mandibular gland of a Meliponini (as described by both Fisk, 1967 and Cortopassi-Laurino et al., 2006). All this leads to the conclusion that, if there is any possibility of a shared code between humans and bees, it can be through the use of olfactory signals.

Persistence of Chemical Signals, the Notion of time, Memory, and Learning

Scent is often considered as a primitive or particularly simple means of communication. For Frisch (1973: 77), olfactory signals only attain full significance for bees when coupled with buzzing and/or jostling, in the specific case of conveying information regarding food source location. Similarly, for Lindauer (1971: 2), scent as a method of communication offers no means of variation, contrary to optical or acoustical signals which are highly variable. That is because, “[t]o differentiate scent signals, different scents must be emitted from different scent glands” (Lindauer, 1971: 2), meaning that for there to be variation of messages, there must be variation in secreting organs, and there are only so many glands a living organism can have.

In the case of Meliponini, a bee can either use its mandibular gland to secret its distinct smell or carry a small amount of the food from the food source back to the hive and distribute its scent to inform other bees of the quality of food that it has encountered. In the second case, the bee is not producing the chemical signals, it is carrying substances produced by another organism (for instance, a flower). Regarding the impossibility of secreting different scents, and so, the shortcomings of chemical communication when it comes to variability, Sebeok (1967: 65) poses the most interesting point:

In this very lack of flexibility, however, lies the one distinct advantage of chemical signals. By these means, an individual is capable of communicating with another in the future and, what is even more remarkable, an individual is also capable, by virtue of delayed feedback, of communicating with himself in the future. (Sebeok, 1967: 65)

Sebeok is speaking of the persistence of chemical signals in time, their endurance or longevity. Generally, in nature, optical or mechanical signals do not last much longer after the source has stopped emitting it. The same cannot be said about chemical signals, which can be received and interpreted long after the effector organ responsible stopped reproducing it. In other words, the odour trail of a guide bee will last longer than the act of laying the trail. When it comes to the honeybee’s Waggle Dance, for instance, the same cannot be affirmed. As soon as the dancer bee stops dancing, there will be no more information conveyanceFootnote 1. Ultimately, although optical and mechanical signals can be more variable, providing combinations and nuances, chemical signals present an advantage when it comes to time. This leads us to question b. How do stingless bees sense the passage of time?

According to Frisch (1973: 85), “[b]ees possess excellent timing, an inner clock, so to speak. During earlier experiments, by feeding at certain hours only they trained themselves to arrive promptly at the table at that time - even if the table was not set”.

Inspired by that passage, one of the interview questions (Online Resource, question 8) asked Barbieri if he maintains a routine with his bees. The researcher answered positively; he opens the hive boxes once a week to check for phorid invasions and also does a more thorough check-up every fortnight to see if the bees are laying new eggs or if there is anything that could be wrong with the hive. The subsequent question regarded if he thought the bees were aware of said routine, to which Barbieri once again answered “yes”. According to him, when it is time for the handling routine, the older bees leave the hive box and wait outside, while the younger ones retrieve deeper in the hive to hide from the light. As long as the routine is kept, and the bees have this constant contact with the human who is doing the handling, they do not present any sort of hostile behaviour, indicating that they are indeed used to the happenings.

Ethologist Lars Chittka (2017: R1049) writes that bees possess “a qualitatively different form of intelligence, tailored to the challenges of a profoundly different kind of society and lifestyle”. Since their umwelt is so different, it becomes challenging to investigate their perception of certain aspects of reality, such as time. Turning towards behavioural ecology is a possible way to shed some light into the matter. In this sense, the question of memory, as something intrinsically tied to time, is an issue that can be observed through experimentation.

Memory is understood as a “major source of intrinsic information and is used to decide when to start foraging, where to forage, and which flower to visit” (Biesmeijer & Slaa, 2004: 144). It also allows bees to inspect food sources that were known in the past, even after interruption. More than that, in the case of food foraging, the memory is associative, that is, “bees associate colour, shape, and scent with the rewarding nectar they collect in the flowers” (Hölldobler and Wilson 2009: 118), which facilitates their consistent “return to the same kind of flowers on subsequent trips” (ibid.).

Perhaps the most interesting aspect of memory, when it comes to eusocial insects, is that it has a highly collective character, in a way that up-to-date information is provided through a sort of ‘joint memory’, which forms the basis of the colony foraging (Biesmeijer & Slaa, 2004: 144). An additional way in which one may understand a colony can also be “as an information network” (Hölldobler and Wilson 2009: 309), where “patterns are built from many quite individual minds linked by a high degree of organization […] central to the colony’s survival and reproduction” (ibid.). Even though this collective aspect is the most fundamental, it is still important to understand that individual members are also in possession of “a cognitive consciousness built with a relatively complex brain that can store information from all its sensory modalities […] as well as some memory of the events it has experienced during its short life” (ibid.).

Yet another approach to characterizing the collective aspect of a colony can be with the term “superorganism”, as developed in the work by Hölldobler and Wilson (2009). A superorganism arises from the joined operation of various smaller, short-lived minds, arranged into “specialized castes that act together as a functional whole” (ibid, 6), as well as “self-organized by division of labour and united by a closed system of communication” (ibid, 84). This concept describes all eusocial colonies where “adult members are divided into reproductive castes and partially or wholly nonreproductive workers”, “adults of two or more generations coexist in the same nests”, and “nonreproductive or less reproductive workers care for the young” (ibid, 8–9). This functional whole that arises from self-organized smaller minds thus possess cognitive capacities that entail perception (of nest state, for instance), decision-making (what tasks need to be done), planning (i.e. in nest building), and last but not least, memory.

In order to understand more about memory, the last of the interview questions (Online Resource, question 10) was about the period of lockdown during the beginning of the COVID-19 pandemic, in which the University of São Paulo campus was closed. During almost a year, Barbieri and his collaborators were not allowed to have contact with the on-campus hives. Thus, the interview inquired about whether the researcher noticed any unusual behaviour from the bees when he was allowed to return to campus. The response of the bees was indeed hostile, nibbling and swarming around to scare the intruder away. Barbieri explained: “If you go a couple of months without handling the hive, none of the workers will know you, because they all have lived for less time since emerging than the time you last did the handling. Essentially, there will be no workers left alive who have known you, all workers will be too young to know your smell. And because they don’t know you, they will consider you a threat” (Online Resource, reply to question 10).

Although Barbieri only mentioned his sent as a signal responsible for the activation of memory (recognition), Hölldobler and Wilson (2009) state that information received through all sensory modalities (that is, taste, smell, sight, and even sound/vibrations) can be temporarily stored in the bee brain. Surely, the persistence of chemical signals may be a characteristic that makes this type of signal more desirable when it comes to storing information over time. Nevertheless, the fact that bees are proven to be able to store information regarding other signals in both their individual and collective memory is also something important to consider. Bees were also shown to associate, at once, a given colour with a reward, being able to remember such association for up until 6 days (ibid, 119). Even further,

If given the experience three times in a row, they remember the colour for at least 2 weeks. The location of a food site in the field can be remembered for a period of 6 to 8 days after last visiting the location; on one occasion, worker bees were observed dancing out the location of a site after 2 months of winter confinement. (Hölldobler and Wilson 2009: 119)

Therefore, bees are able to not only recognize scent, but also colour, shape, sound, etc., in a way that the categories of ‘what is known and what is new, what is a threat and who is a friend’ can be multimodal. This way, it is not possible to affirm that, when it comes to associating a human to a non-threatening profile, scent is the only signal considered. Since they are able to memorize sound (vibrations), could they recognize voice? Since they are able to memorize patterns, could they recognize body or face features? These (and more) may be questions worth investigating through experimentation. Further, such categorization (known/new, friend/enemy, etc.) requires learning. On this subject, Kull (2014: 48–49) writes:

Organisms act on the basis of sign relations that have turned into habits, or codes. Sign relations depend on experience sensu lato, on learning. An organism’s experiences, embedded in sign relations, are also modelling relations. In this concrete sense, we can generalize the notion of “knowing” to any experience, covering all sign relations in which organisms are involved. Thus, in this context, the forms of knowing include both an instantaneous thought and a built-in adaptation, a conscious and an unconscious experience, a thoughtful and a quite automatic take, or stance. (Kull, 2014: 48–49)

Not too far from that, Chittka (2017: R1050) argues that “[t]here are interactions between instinct and learned behaviour at multiple levels, and complex instincts can facilitate advanced learning behaviour”. For instance, “[b]ees have innate predispositions to tell floral from nonfloral objects, and are more attracted to some flower colours than others”, yet, “because different flower species have different profitability in terms of nectar and pollen offerings”, it is necessary for bees to learn flower sensory signals “as predictors of rewards” (ibid.)., or in other words, bees need to learn how to attribute meaning to certain signs in order to efficiently forage for food.

Another example of the learning capacity of bees can be seen on the experiment by Loukola et al. (2017). The researchers engaged in training certain bees to transport a small ball to a defined location in exchange for a nutritive reward. The bees were trained in different ways, namely: they either watched the ball being moved to the defined location by a magnet or by a model demonstrator (meaning either a plastic model of a bee on a stick or a previously trained live bee). Their results showed that the bees learnt the task more efficiently by observing a demonstrator, than by watching the ball be moved ‘by itself’, that is, by the magnet (Loukola et al. 2017: 833). Chittka and Rossi (2022: 579) call this “social learning”, stating that “insects prioritise socially obtained versus individually acquired information”, being able to “learn from members of other species and robots”. An interpretation of this study shows that the ‘model demonstrator’ (be it a robot, plastic bee on a stick, or other unexplored possibilities) could be a mechanism for possible communication, at least in the sense of instructing a bee to perform a task.

The information storing and learning capacity of social insects can go even further:

Interestingly, when individual differences are highlighted with visible colour marks applied by experimenters, fruit flies and bumblebees (neither of which are known to recognise one another individually in nature) can learn to identify the bearers of reliable social information by visual cues. Thus, the cognitive capacities to recognize other individuals and store valuable information about them (including which individuals make for particularly valuable role models) certainly exist in the insects (Chittka and Rossi, 2022: 580)

In conclusion, recognition is fundamental to all social insect species, since they must be able to discriminate between colony members, alien species, co-specifics from different hives, as well as hivemates who belong to different layers of maturity and of the distinct hierarchical positions (Hölldobler and Wilson 2009: 275). Considering how chemical signals play a central role in such recognition, this might mean that, in an experiment similar to the one carried out by Loukola et al. (2017), a plastic model bee infused with certain characteristic odours may prove to be an even more efficient mechanism of communication, than the one relying solely on visual cues.

Coming back to the interview, it is possible to conclude that the bees Barbieri handles frequently indeed know him. Because, through their experience with him, sign relations were established – signals and cues emanating from Barbieri become meaningful, signifying ‘not a threat’, even though the act of barging in on the hive from the part of any other organism who is not recognized as a hivemate would have otherwise meant a definitive threat. Through past experiences with Barbieri, the bees have learnt to recognize and discriminate him as ‘not a threat’, and that in turn, has become a habit; a conditioned response that entails not swarming or biting the human, and accepting his intrusion on their space. For Kull (2014: 52), this type of learning is called ‘iconic learning’, and the knowledge associated with it is not conscious. Considering how important it is for human-animal relations the fact that one party must be able to recognize the other, even if the bees are not conscious of the fact that they know Barbieri, we can still state that they do.

On Domestication

According to Diamond (2012), humans started domesticating animals millennia ago. The author indicates that dogs were domesticated around the years of 15000 to 14000 BCE, while sheep, coats, and cows became domestic around 10000 to 8000 BCE, and horses, around 6000 to 5000 BCE (Diamond, 2012). Similarly, Frisch (1967: 306) wrote about how some bee species are cultured as ‘domestic’ in ancient South American societies, probably referring to the fact that, as it was already mentioned, native indigenous societies practiced beekee** centuries before Europeans arrived on the continent.

In recent times, Cortopassi-Laurino et al. (2006: 276) state that some species (such as Tetragonisca angustula, Trigona cilipes, and T. dallatorreana) are under ‘semi-domestication’ since they are often kept inside human houses, which leads us to question c. Are stingless bees domesticated animals?

Domestication can have a variety of definitions (Zeder, 2015). In the present article, four distinct but complementary definitions will be offered, each of which focusing on a different aspect: mutual advantages; incorporation into human culture; ability to communicate, and opening of semiotic relations.

The first possible way one can understand domestication is as a

[...] sustained multigenerational, mutualistic relationship in which one organism assumes a significant degree of influence over the reproduction and care of another organism in order to secure a more predictable supply of a resource of interest, and through which the partner organism gains advantage over individuals that remain outside this relationship, thereby benefitting and often increasing the fitness of both the domesticator and the target domesticate. (Zeder, 2015: 3191)

In this sense, it is easy to see how stingless bees fit the category of domesticated animals. After all, the practice of meliponiculture entails humans influencing the reproduction and caring for the safety and health of a beehive, in order to harvest products such as honey, beeswax, and propolis. Hives kept on especial meliponiculture wooden containers have an advantage over wild ones, since humans keep the hive safe from phorid invasion as well as protected from environmental factors (storms and such).

It is also worth mentioning that Brazilian legislation prohibits the removal of colonies from their natural habitat, with the exception of bait boxes, which capture colonies that are already looking for a new home (Venturieri 2008). Popular meliponiculture guides and manuals for the general public (aimed at popularization of stingless bee beekee**) describe varied colony multiplication techniques that configure efficient ways to obtain a hive from an already ‘domesticated’ one (ibid.). This means that, for more than a decade, Meliponini beekeepers have been breeding stingless bees apart from wild ones. In the grand scheme of nature, that is still little time. Nevertheless, it is interesting to account for the possibilities that this breeding can lead to in the future.

Moreover, as an extension to the definition proposed by Zeder (2015), domestication also “involves both culture and biology. The cultural process of domestication begins when animals are incorporated into the social structure of a human community and become objects of ownership, inheritance, purchase and exchange” (Clutton-Brock 1992: 79). Meliponiculture, as both an economic as well as cultural and scientific activity, is deeply related to this idea of domestication as incorporation of animals into human social structure.

For that to be possible, the beekeeper must possess deep knowledge of the biological needs of the bees, not only for the maintaining of the hive – so that it keeps being productive – but also to facilitate human-bee interaction. For instance, the popular guide on Indigenous Stingless Bee Beekee** written by Venturieri (2008: 59) states that honey harvest should be performed whenever the hive is almost or completely full and, for some species, this operation is facilitated when performed at night, since certain bee species are not so active during this time. From this guide, it is possible to see that, in meliponiculture, the obtention of deep knowledge about the lives of bees and how they understand the world is encouraged.

Still, when it comes to domestication, communication is a central aspect that has not been covered in any of the definitions mentioned until this point. Hence, from the point of view of biosemiotics, we turn once again to Sebeok, according to whom, domestication

[…] involves a crucial understanding on our part of the animals’ biologically-given communicative capacity. The success of processes like taming and training depends on our having mastered relevant elements of animals’ codes. In order to flourish in our company, each animal must be able to discern man’s verbal and/or nonverbal behaviour. (Sebeok 1990: 108)

One could argue that, in case of the study by Loukola et al. (2017), researchers succeeded in training bees to exert a task. The works by Hölldobler and Wilson (2009) and Chittka (2017) also mention other successful instances of bee training, namely: walking through mazes requiring recognition of colour cues, and pulling on a string to access an artificial flower kept under a barrier, respectively. Nevertheless, if bees need to actually understand man’s verbal and/or nonverbal behaviour in order for domestication to happen (as suggested by Sebeok) then, it becomes difficult to see how it would be possible to call bees ‘domestic’. Yet, if one is to interpret the passage above more loosely, it might be possible to recognize that we may communicate with bees even if they are not aware (conscious) that they are communicating with us. Otherwise, one could argue that Loukola et al. did not, in fact, train the bees to exert a task, but rather the plastic model bee was the one who did the training, since – as far as the bees were concerned – they were not dealing with a heterospecific, but with just another bee.

Even so, domestication, as delineated by Sebeok, can be even further interpreted as an opening of semiotic relations, that is, a widening of the concept of ‘group’ over the species limits, which may be a more useful definition for the present study. This opening requires a certain degree of freedom or flexibility for the determination of who does and who does not belong to a social group. So, maybe, the question regarding if stingless bees are a domestic species should revolve around whether humans can be considered as part of the hive or not.

For that, it is worth recalling that communication doesn’t happen just to inform food location. It can also be frequently used to inform on the division of labour. According to Lindauer (1971: 16–19),

[…] even under normal conditions the division of labour was not quite so rigid as had previously been supposed. On the whole, the bee does adhere to her schedule; but this can be readjusted to a large extent, and every bee can engage in other tasks in her spare time, depending on whether a working place happens to be vacant. It is this flexibility that guarantees the full harmony of the social life. (Lindauer 1971: 16–19)

For Lindauer, the individual bee becomes informed of the tasks which need to be executed either through specific orders passed down from one bee to another, or the individual “[…] gathers on her own the necessary information about the current necessities within the hive” (ibid.).

She does this by extensive patrolling around. Cells are inspected to see whether they are clean and prepared for egg laying; larvae are inspected to see if they are ready to be fed, other cells whether they are ready to be sealed. Seams and corners are searched for wastes, or the building areas are surveyed for needed construction work. (Lindauer, 1971: 19)

Here, the final point of this paper shall be argued: if communication regarding division of labour can happen mediated by the physical properties of the nest, it should be possible to state that the beekeeper, attuned to these properties, takes part in this communication process. It is among the tasks of a beekeeper to observe the hive and take actions to help, either by assisting in cleaning or even defending the nest against phorid invasion. As it was discussed on previous sections, bees are able to learn to recognize humans as their handling of the hive becomes a habit. In the interview (Online Resource) with Barbieri, the researcher states that, during their handling routine, the more experienced (older) bees wait outside the box until the cleaning is done. The fact that bees will not consider their keeper an invader when opening the hive boxes, and will even patiently cooperatively wait outside during the handling of the hive (as the keeper carries on with his/her tasks of cleaning and caring for the nest) may be interpreted as a sign that the bees do consider this human part of their social group, in some sort of manner.

Today, biologists know that eusocial insect hives are much more complex than previously thought. According to Chittka and Rossi (2022: 580), “[t]he historic notion that complex colony function emerges only from simple, hardwired behaviour routines, which govern local interactions between anonymous individuals, is no longer tenable”. Their research on how stingless bees showcase culture-like processes in the wild demonstrates how these insects are much more than the sum of their genotypes, a view which is consistent with biosemiotics. Such understanding of the complexity of bee behaviour and communication may be a doorway to further studies on the human-bee relations.

Conclusion

This paper discussed the possibilities of semiotically mediated communication between humans and stingless bees. First, it was stated that, for there to be inter-specific communication, there has to be a shared code, and that this depends on the biological makeup and sensory apparatus of both animals involved in the communication process.

When trying to identify what is meaningful for the bees, it became clear that one way to communicate with the insects is through the use of a guide bee model (as described by Loukola et al., 2017). Additionally, it is possible to conclude that the use of olfactory (chemical) signals can also be a feasible channel through which to exchange signs with stingless bees. It is possible that the coupling of the model bee with the knowledge of chemical communication may configure an even more effective mechanism with which to train Meliponini to exert certain tasks, even though it is still not clear precisely what kinds of signals take on a more meaningful role when it comes to social learning. Because bees have the capacity to store information in their memory regarding all stimuli that they are able to perceive, there still needs to be more experimentation in order to determine exactly what are the most important aspects that should compose this model bee (colour, shape, pattern, dimensionality) in order for there to be effective communication (other than the very clearly relevant olfactory/ chemical signals).

Besides, given its specific characteristics, chemical signals present the possibility to endure time to a certain degree, opening possibilities of investigation on how certain species that use those signals perceive the passage of time and keep memory of past events, something which is important for human-animal relations, considering that one party has to be able to recognize the other (iconic learning).

Further, when it comes to the memory of a hive, it is important to understand that, given the lifespan of individual bees, human handlers cannot go more than a few months without coming into contact with the insects at the risk of having his/her scent forgotten and subsequently deemed as a threat over the course of the next encounter. A way to potentially mitigate this problem could be to present the odour of the beekeeper in their absence in an effort to prolong the memory, however, since bee memory is associative and multimodal, we cannot be sure that scent is the only sign bees interpret in recognizing and profiling their human handlers.

Finally, on the topic of domestication, it is understood that bees can be deemed ‘domestic’ under many definitions of the concept. In summary, meliponiculture is an activity which entails multigenerational mutualistic relationships between humans and bees, as well as deep understanding of bee biology, life, and communicative capacity from the part of the beekeeper. The most relevant characteristic of human-bee relationship in this sense might be the fact that beekeepers are attuned to the necessities of the hive much similarly to how a bee might be, even taking action to protect and maintain the nest safe and healthy. Also, the fact that bees are able to recognize and react to the beekeeper in cooperative ways during nest maintenance can be interpreted as the bees deeming the beekeeper as part of their social group, in some sort of way.

Conclusively, as stated by Frisch (1973: 86), “[a] question answered usually raises new problems, and it would be presumptuous to assume that an end is ever achieved”. Accordingly, this research suggests that this topic is deserving of more studies to further develop the notion of human-bee communication. Zoosemiotics, as a field of studies which considers animal views of the world, how they experience life, and what is meaningful for them, is the ideal modelling system for the complete investigation of all possibilities of mutual understanding between these two species.