James Nieh
Associate Professor of Biology, UCSD

e-mail: jnieh@ucsd.edu
Lab Home Page

Evolution of animal communication: functionally referential communication in highly social bees

Insect societies have evolved communication systems of remarkable complexity. Highly social bees (honeybees and stingless bees) use sophisticated methods to exploit resources such as pollen, nectar, water, resin, and nest sites. Social bees can recruit, increase the number of nestmates at a particular location or increase the number of nestmates searching for a particular resource at non-specific locations.

My research examines the mechanisms that allow highly social bees to communicate resource location and seeks to understand how these communication systems have evolved.

Honeybees use functionally referential communication, the transformation of environmental information into coded signals understood by a conspecific receiver. Such a system may be a sophisticated form of animal communication because of the cognitive complexities presumably involved in transforming sensory information into coded communication signals. However, the question of how referential communication has evolved remains relatively unexplored.

Stingless bees
Stingless bees are an excellent model for the evolution of animal language because they possess the widest diversity of species and communication strategies, including the ability to acoustically encode the distance and height of food sources. Moreover, some species may use functionally referential communication.


For example, Melipona panamica foragers can communicate the three-dimensional location of food sources. To achieve this, foragers use a combination of mechanisms. Results from a series of removal experiments (segregating all feeder-experienced foragers from potential recruits as they left the nest) suggest that direction is communicated outside the nest whereas height and distance are communicated inside the nest (Nieh & Roubik 1998).

A recruiting forager produces a series of pulsed sounds when she unloads her food to other bees and when she begins to make clockwise and counterclockwise dance movements (Nieh 1998B). During the food-unloading phase, she produces longer sound pulses for a food source on the canopy floor than for one 40 m up in the canopy. During the dance phase, sound pulse duration is positively correlated with increasing distance of the food source from the nest (Nieh & Roubik 1998). Thus M. panamica foragers appear to use sounds to communicate food height and distance. Several other Melipona species also produce sound pulses whose durations correlate with the distance to a food source. Direction may be communicated outside the nest through recruits initially following the recruiter for short distances. However, recruits can still find the food source at the correct height and distance even when they are prevented from following recruiters outside the hive.

When recruits are near the food source (within 6 to 12m), they can orient towards an odor beacon deposited by experienced foragers (Nieh 1998). Thus M. panamica's complete recruitment system uses visual, olfactory, and acoustic cues to both directly guide and to provide symbolic information.

Multi-modal communication
Recruiting foragers exploit several different information channels-sound, odor, vision, thermal sense, tactile sense. Such multi-modal communication is robust. It provides backups in case of information corruption or transmission failures. The lab therefore studies several modalities, focusing on acoustic, thermal, and chemical information.

Chemical Espionage
We have recently begun to focus on chemical espionage in stingless bees and the role this may have played in the evolution of potential "counter-espionage" strategies such as encoded communication inside the nest. All social bees have some form of odor marking at the food source, but only the stingless bees use odor trails. There is intriguing variation in the length of these odor trails, with some species producing complete odor trails that extend from the nest to the food source, others producing short odor trails that extend only a few meters away from the food source in the direction of the nest, and finally some that only odor mark the food source alone. Why does this variation exist? Some stingless bees, such as the aggressive species Trigona spinipes, can evidently eavesdrop and orient towards the odor marks deposited for good food sources by other species such as Melipona rufiventris. In experiments, this eavesdropping occurred when T. spinipes foragers were acting as scouts. Trigona spinipes foragers were also clearly able to distinguish between their own odor marks and those of M. rufiventris. After finding the food source marked by the "victim" species, T. spinipes attacked, drove away, and killed the M. rufiventris foragers, taking over their food. Limiting the conspicuousness of odor marks via strategies such as decreasing odor trail length could be an effective counter strategy to such eavesdropping. However, this would also decrease the amount of guidance information offered to recruits. Providing encoded location information, functionally referential communication, at the nest would replace such lost odor trail information. Interestingly, all bees for which there is some evidence for functionally referential communication, including honeybees, only use point-source odor marking,. Whether this is due to eavesdropping and aggressive competition remains to be determined. However, stingless bees and honeybees still aggressively compete in the environments and regions in which they evolved. Thus eavesdropping may have contributed to the evolution of functionally referential communication at the nest.

James Nieh Publication list    

    Contrera, F. A. L. and J. C. Nieh. (2006). The effect of ambient temperature on forager sound production and thoracic temperature in the stingless bee, Melipona panamica. Behavioral Ecology and Sociobiology (in press).

    Nieh, J. C., Leon, A., Cameron, S., and Vandame, R. (2006). Hot bumblebees at good food: thoracic temperature of feeding Bombus wilmattae foragers is tuned to sucrose concentration. Journal of Experimental Biology 209: 4185-4192.

    Wilson, E. S., Holway, D., & Nieh, J. C. Cold anesthesia decreases foraging recruitment in the New World bumblebee, Bombus occidentalis. Journal of Apicultural Research. (in press).

    Nieh, J. C. & Sanchez, D*. (2005). Effect of food quality and location on thoracic temperature in the stingless bee, Melipona panamica. Journal of Experimental Biology 208:3933-3943.

    Saraiva, A., Nieh, J. C., & Cartolano E. A. Jr.* (2005). EthoLog: a tool for data acquisition on behavioral studies. 2005 EFITA/WCCA Joint Congress on Information Technology in Agriculture.

    Contrera, F. A. L., Imperatriz-Fonseca, V. L., Nieh, J. C. (2005). Temporal and climatological influences on flight activity in Trigona hyalinata (Apidae, Meliponini). Revista Tecnologia e Ambiente. 10:35-43.

    Nieh, J. C., Kruizinga, K.*, Contrera, F. A. L., Barreto, L. S.* & Imperatriz-Fonseca, V. L. (2005). Effect of group size on the aggression strategy of an extirpating stingless bee, Trigona spinipes. Insectes Sociaux. 52, 1-8.

    Nieh, J. C., Contrera, F. A. L., Yoon, R. R.*, Barreto, L. S.* & Imperatriz-Fonseca, V. L. (2004). Polarized short odor-trail recruitment communication by a stingless bee, Trigona spinipes. Behavioral Ecology and Sociobiology, 56, 435-448.

    Nieh, J. C., Barreto, L. S.*, Contrera, F. A. L. & Imperatriz-Fonseca, V. L. (2004). Olfactory eavesdropping by a competitively foraging stingless bee, Trigona spinipes. Proceedings of the Royal Society of London B, 271, 1633-1640.

    Nieh, J. C. (2004). Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie, 35, 159-182.

    Sanchez, D.*, Nieh, J. C., Henaut, Y., Cruz, L., & Vandame, R. (2004). High precision during food recruitment of experienced (reactivated) foragers in the stingless bee Scaptotrigona mexicana (Apidae, Meliponini). Naturwissenschaften. 91, 346-349.

    Nieh, J. C., Contrera, F. A. L. & Nogueira-Neto, P. (2003). Pulsed mass-recruitment by a stingless bee, Trigona hyalinata. Proceedings of the Royal Society of London B., 270, 2191-2196.

    Nieh, J. C., Contrera, F. A. L., Ramirez, S.* & Imperatriz-Fonseca, V. L. (2003). Variation in the ability to communicate 3-D resource location by stingless bees from different habitats. Animal Behaviour, 66, 1129-1139.

    Nieh, J. C., Contrera, F. A. L., Rangel, J.* & Imperatriz-Fonseca, V. L. (2003). Effect of food location and quality on recruitment sounds and success in two stingless bees, Melipona mandacaia and Melipona bicolor. Behavioral Ecology and Sociobiology, 55, 87-94.

    Nieh, J. C., Ramirez, S. & Nogueira-Neto, P. (2003). Multi-source odor-marking of food by a stingless bee, Melipona mandacaia. Behavioral Ecology and Sociobiology, 54, 578-586.

    Nieh, J. C. & Tautz, J. (2000). Behavior-locked signal analysis reveals weak 200-300 Hz comb vibrations during the honeybee waggle dance. Journal of Experimental Biology, 203, 1573-1579.

    Nieh, J. C., Tautz, J., Spaethe, J. & Bartareau, T. (2000). The communication of food location by a primitive stingless bee, Trigona carbonaria. Zoology, 102, 239-246.

    Nieh, J. C. (1999). Stingless-bee communication. American Scientist, 87, 428-435.

    Nieh, J. C. & Roubik, D. W. (1998). Potential mechanisms for the communication of height and distance by a stingless bee, Melipona panamica. Behavioral Ecology and Sociobiology, 43, 387-399.

    Nieh, J. C. (1998). The food recruitment dance of the stingless bee, Melipona panamica. Behavioral Ecology and Sociobiology, 43, 133-145.

    Nieh, J. C. (1998). The honey bee shaking signal: function and design of a modulatory communication signal. Behavioral Ecology and Sociobiology, 42, 23-36.

    Nieh, J. C. (1998). The role of a scent beacon in the communication of food location in the stingless bee, Melipona panamica. Behavioral Ecology and Sociobiology, 43, 47-58.

    Nieh, J. C. & Roubik, D. W. (1995). A stingless bee (Melipona panamica) indicates food location without using a scent trail. Behavioral Ecology and Sociobiology, 37, 63-70.

    Nieh, J. C. (1993). The stop signal of honey bees: Reconsidering its message. Behavioral Ecology and Sociobiology, 33, 51-56.

 Dr. Nieh received his BA from Harvard in 1991 and his Ph.D. from Cornell University in 1997. He completed a NSF-NATO postdoctoral fellowship at the University of Würzburg, Germany and was a Harvard Junior Fellow from 1998-2000.