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Behav Ecol Sociobiol (1998) 42: 107116

Springer-Verlag 1998

Jacobus C. Biesmeijer Mark G.L. van Nieuwstadt cs Marinus J. Sommeijer Saskia Luka

The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae)

Received: 16 April 1997 / Accepted after revision: 30 August 1997

Abstract Social insect foragers have to make foraging decisions based on information that may come from two dierent sources: information learned and memorised through their own experience (``internal'' information) and information communicated by nest mates or directly obtained from their environment (``external'' information). The role of these sources of information in decision-making by foragers was studied observationally and experimentally in stingless bees of the genus Melipona. Once a Melipona forager had started its foodcollecting career, its decisions to initiate, continue or stop its daily collecting activity were mainly based upon previous experience (activity on previous days, the time at which foraging was initiated the day(s) before, and, during the day, the success of the last foraging ights) and mediated through direct interaction with the food source (load size harvested and time to collect a load). External information provided by returning foragers advanced the start of foraging of experienced bees. Most inexperienced bees initiated their foraging day after successful foragers had returned to the hive. The start of foraging by other inexperienced bees was stimulated by high waste-removal activity of nest mates. By experimentally controlling the entries of foragers (hence external information input) it was shown that very low levels of external information input had large eect on the departure of experienced foragers. After the return of a single successful forager, or ve foragers together, the rate of forager exits increased dramatically for 15 min. Only the rst and second entry events had large

eect; later entries inuenced forager exit patterns only slightly. The results show that Melipona foragers make decisions based upon their own experience and that communication stimulates these foragers if it concerns the previously visited source. We discuss the organisation of individual foraging in Melipona and Apis mellifera and are led to the conclusion that these species behave very similarly and that an information-integration model (derived from Fig. 1) could be a starting point for future research on social insect foraging. Key words Decision-making Foraging Melipona Communication Learning

Introduction
Individual honeybees and stingless bees normally spend the last part of their life collecting food (Ro sch 1925; th, unpublished work). Each J.C. Biesmeijer and E. To individual has to decide when to start and whether to continue or stop its collecting activity. An individual's foraging career probably starts when its foraging motivation is above a certain threshold. At the start of a career, foraging motivation is largely related to genetic (Robinson and Page 1989) and physiological factors (van der Blom 1993; Robinson 1987). Once foraging has commenced motivation is continuously modied based upon accumulating experience (Dukas and Real 1993). The decisions on when to initiate foraging on the next day and whether to continue or stop foraging during the day may be based on internal information, previously obtained from the environment and now part of the bee's memory, and external information, the stimulus inputs obtained directly from the environment. Integration of internal and external information is an essential part of the decision-making process of foraging bees. This process will be represented here by the ow diagram in Fig. 1, based on work of Pasteels et al. (1987) and others (von Frisch 1967; Moritz and Southwick

J.C. Biesmeijer (&) M.G.L.v. Nieuwstadt1 cs M.J. Sommeijer S. Luka Ethology and Socio-Ecology Group, Department of Comparative Physiology, Utrecht University, PO Box 80.086, 3508 TB Utrecht, The Netherlands Fax: +30 2521105; e-mail: biesmeijer@neuretp.biol.ruu.nl Present address: Department of Botanical Ecology, Utrecht University, The Netherlands
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Information integration by honeybee foragers Little is known about the way in which experienced foragers integrate external and internal information. Karl von Frisch (1923) trained bees to a sugar-water feeder and observed that experienced foragers remained in the hive after food provisioning stopped and became active only when returnees indicated that their source has reopened. Meanwhile they neglect other external information. It has also been observed that foragers can be conditioned rapidly to almost any stimulus associated with food, and once conditioned are not receptive to information on other food sources (Wenner and Johnson 1966). Other authors, however, assume that after abandoning a source a bee instantly becomes available to the pool of recruitable foragers (Camazine and Sneyd 1991), whereas Free (1969) reported that experienced foragers tend to search for food sources that have the odour of the colony food stores even when it is dierent from the odour of the food source they have been visiting themselves. Information use by stingless bees How foragers of the other group of highly social bees, the stingless bees, make foraging decisions is still almost completely unknown. Most studies deal with their mechanisms of communication about food sources (Lindauer and Kerr 1958, 1960; Kerr 1994; Nieh and Roubik 1995). However, Raw and Passos de Freitas (in press) report on the perception and recording of time by workers of three species of stingless bees. Among the stingless bees a range of communication strategies are found, e.g. individual foraging, general arousal, sound communication and scent-trail communication (Lindauer and Kerr 1958, 1960). This makes this group of bees of special interest for studies on communication and learning in social foragers and may provide information on the functional signicance of the colonial and individual foraging strategies of the various species. In this paper we will study the role of internal and external information in decision-making of individual stingless bee foragers of Melipona beecheii and M. fasciata. The integration of information will receive special attention. Because the two species are closely related, it was assumed that their basic foraging mechanisms would not be essentially dierent.

Fig. 1 Flow diagram representing decision-making in Melipona foragers. External information is all information obtained directly from the environment (inside and outside the hive). Internal information is all information learned and stored in the bee's memory. Foraging success adds positively to internal information, indicated as +, whereas foraging failures add negatively to internal information, indicated as )

1992; Seeley 1995). The ow diagram does not predict how internal and external information are integrated. Information acquisition by honeybee foragers Decision-making processes play an important role in the regulation of food collecting by the honeybee, Apis mellifera (reviewed by Seeley 1995). The majority of the bees (so-called recruits) start foraging after having followed recruitment dances performed by returning foragers (von Frisch 1967) and only a few bees (so-called scouts) start searching for food independently (zu Oettingen-Spielberg 1949). Once started, bees continue to frequent a particular food source as long as it provides food (von Frisch 1967). During the rest of their foraging career both internal information and external information is available simultaneously. Internal information includes the time at which food was found (Beling 1929), and food source parameters such as protability (Raveret Richter and Waddington 1993), colour (Opnger 1931), odour (Opnger 1949), shape (Gould 1985) and position of the source (Ro sch 1925). External information is provided mostly by other bees. Returning foragers inform nest-mates about odour, location and protability of a range of food sources (von Frisch 1967; Farina and Nun ez 1995; Farina 1996). Nest mates provide foragers with information on the colony's nutritional status, e.g. nurse bees that trophallactically ``inform'' about pollen reserves (Camazine 1993), and nectar receivers that ``indicate'' the protability of the nectar source visited by a forager through the time the forager spends before unloading (Seeley 1989; Seeley and Towne 1992).

Material and methods


Study site and colonies The study was carried out in El Sur de Turrubares, San Jose Province (945N, 8435W; altitude 180 m), Costa Rica between April and July 1994. Three bee colonies were used: two of M. fasciata Lepeletier and one of M. beecheii Bennett. These were installed inside a house in a

109 one-compartment hardwood box (60 20 20 cm; walls 2.5 cm thick). Each colony was connected to the outside through a transparent plastic tube and a glass-covered plywood walkway. To leave or enter, the bees had to walk 15 cm (including two curves to slow them down). This facilitated observation of individual bees. The entrance of each colony was colour-marked. One colony of M. fasciata (referred to as Mf I) contained about 500 bees, the other colony (referred to as Mf II) contained 800 1000 individuals. The M. beecheii colony consisted of 25003000 bees. All colonies contained an egg-laying queen, brood and stored food throughout the observations. Colony I was relatively weak and later killed by ants, so few results refer to this colony. Individual foraging behaviour Bees were colour-marked individually before (and during) the observations. A paper tag was glued to the thorax of a bee and painted after drying. Flight activity was recorded in all three colonies. Foragers of Mf I were observed on 9 and 10 May from 0500 to 1800 hours; foragers of Mf II between 15 June and 15 July from 0500 to 1100 hours (some days till 1600 hours); foragers of the M. beecheii colony between 6 June and 23 June from 0500 to 1200 hours (interrupted for marking bees from 0900 to 1000 hours). In all observations exits and entries of marked foragers were recorded and time, load type and load size were registered. Pollen loads were divided by sight into very large, large, normal, small and very small loads. Liquid loads are further referred to as nectar loads and were divided into large, normal and small loads based upon abdomen distension. Nectar loads could not be distinguished from other liquids carried in the honey stomach. Previous sampling of honey stomach loads indicated that M. beecheii foragers regularly carry water (less than 5% sugar), but M. fasciata very rarely. M. fasciata foragers occasionally carried a pollen-nectar mixture in their honey stomach, that may have been robbed from another M. fasciata colony nearby (J.C. Biesmeijer, Personal observations). Controlled-entry experiments Controlled-entry experiments analysed whether foragers used only internal information to start foraging or needed external information as well. To prevent the inuence of external information in decisionmaking for potentially outgoing foragers, all returning foragers were captured before entering the colony. This was achieved either by moving the colony 1 or 2 m overnight, leaving the coloured entrance intact, or by moving the entrance markings 1 m and connecting them to another entrance hole that was connected to a suction tube. All foragers ew out undisturbed following both methods of displacement and returned normally to the old entrance. When they entered the fake entrance, they were captured using a suction tube. Besides this no-entry treatment (all returnees captured), two controlled-entry treatments were applied in the trials. These treatments involved the entry of either 1 or 5 fully loaded foragers returning with pollen at four times during the trial and the entry of 15 fully loaded foragers returning with pollen at a fth time in all trials. Each moment of entry followed a 5- to 10min period in which on average less than 1 bee per minute left the hive. The controlled-entry experiments were performed (with unmarked bees of M. beecheii) to analyse colony level eects. The three dierent treatments were performed several times each on successive days, in such an order that the eect of dierent treatments and of pairs of successive treatments could be assessed. Similarly, individual-level controlled-entry experiments were performed with colony Mf 2. Three trials each involving 2 days of observation were carried out. The rst day of each trial consisted of recording normal foraging activity of all marked individuals (100 200 per trial) from 0500 to 1100 hours. Overnight the colony was moved 1 or 2 m. On the second day all returnees were captured as described before for several hours (till 0700 hours in trial 1; 0645 hours in trial 2; 1000 hours in trial 3) after which in trial 1 and 3 the colony was replaced in its old location and all captured foragers were released, making normal foraging possible. These two phases of the experiment will henceforth be referred to as the ``no-entry'' phase and the ``normal'' phase respectively. In trial 2, however, the normal phase was divided into three parts: (1) at 0645 hours two fully loaded pollen foragers were allowed to enter; (2) at 0700 hours four more foragers; (3) at 0730 hours the colony was replaced and all captured foragers released. In all trials observations of ight activity lasted till 1100 hours. Sugar water feeding experiment Fifteen foragers of a M. beecheii colony were trained to feed ad libitum from an 50% sucrose solution scented with peppermint oil placed 80 m from the hive. Food was provided for few hours only. Bees were observed on one day (after bees had foraged for more than 5 days), before (09401020 hours), during (10201130 hours) and after (11301210 hours) food was provided and all ight movements were recorded at the entrance of the colony.

Results
Foraging on successive days: start of foraging Observation of undisturbed ight activity of individual foragers of M. fasciata and M. beecheii showed that the time at which individuals started foraging was positively related to the time they started foraging on the day before (linear regression: M. fasciata P < 0:05 for 3 pairs of days, P = 0.14 for the 4th pair; M. beecheii P < 0:05 three pairs of days; nfasciata = 55 to 125, nbeecheii = 21 to 60). Moreover, foragers that were successful on the previous day started foraging earlier than previously unsuccessful foragers (data from M. fasciata; t-test; P < 0:05 for three out of four days; P = 0.09 on 4th day; nexp = 43 to 78, nunexp = 9 to 73). Foraging on successive days: foraging experience Three trials of the controlled-entry experiment were performed with M. fasciata and the summed results are presented in Table 1. We distinguished ``early'' foragers (bees that started foraging on day 1 in the period corresponding to the no-entry phase of day 2) and ``late'' foragers (bees that started foraging on day 1 in the period corresponding to the normal phase of day 2). Of the ``early'' foragers that were active on both days, 71% left the hive on day 2 in the no-entry phase, whereas only 18% of the late foragers went out in that phase. Whether bees started foraging in the no-entry or in the normal phase was not related to the number of ights (t-test: P > 0:1), the number of loads (t-test: P > 0:1) or the percentage of success (number of loads divided by number of ights) on the previous day (t-test: P > 0:1). Separate analysis of the dierent groups of foragers [pollen (n = 42), nectar (122), mud (6) and resin (24) collectors] showed that no signicant relation was

110 Table 1 Timing of foraging start by foragers of Melipona fasciata on two successive days. Day 1: normal foraging; day 2: no-entryphase (all returnees captured before entry) followed by a normal phase (unrestricted foraging). The numbers of foraging bees summed over three trials are given. The time of exit of an early forager or late forager on day 1 corresponds with the no-entry phase and normal phase of day 2 respectively (for details see Materials and methods section) Exit day 1 Exit day 2 No-entry phase Early forager Late forager 120 8 Normal phase 48 36 Not out 23 41 v2 = 75.15 P = 0.001 Signicance

successive days was recorded for four pairs of days of uninterrupted foraging activity and for three pairs of days on which no entry was allowed on the second day. The median dierence in time (the median appeared to be the best descriptive measure of the data) between the rst and second day of each pair showed that under normal foraging conditions bees tended to leave at about the same time, but that in absence of returnees they started signicantly later (Fig. 2; Mann-Whitney test: Z = )2.121, P = 0.04). The eect of activity of other foragers on unemployed foragers The ow-diagram that we adopted in this paper (Fig. 1) suggests that in the absence of positive internal information, bees would leave the colony only after having acquired external information about food sources. This would be the case for unemployed foragers, e.g. inexperienced bees and/or temporarily inactive bees. In the three trials in which normal activity was compared with a situation in which no entry of returnees was allowed, 42 of the 338 foragers (12%) were inactive on day 1 (day with normal foraging) but active on day 2 (no-entry and normal activity phase). Seventeen (40%) of them left the hive in the no-entry phase, before returning foragers had entered the hive. This indicates that the prediction from the model is not supported if only very recent experience is taken into account. If all previous foraging experience is considered, however, the prediction seems to hold. All 11 bees that were observed

present for any of the four groups between characteristics of previous foraging activity (number of ights performed, number of loads collected or percentage of successful loads) and the time they start foraging on the next day (linear regression: all P > 0:1). Successive ights during the day We analysed whether foraging success, as measured by load size, aected the probability of an individual stopping or continuing foraging. M. beecheii and M. fasciata bees hardly ever stopped foraging after having collected a full pollen load (Table 2), but usually did so after one or two unsuccessful ights (small pollen load or no load). If a bee's foraging day started with the collection of a small load (or no load), however, foraging continued. Pollen loads mostly decreased in size before a bee stopped foraging (comparing size of ultimate with penultimate load: M. fasciata 37 times decrease, 7 equal and 3 increase; M. beecheii: 23, 5, 1 respectively) Results are highly signicant for both species (binomial test of decreased load size against other transitions: P < 0:001). The eect of activity of other foragers on employed foragers The time at which employed foragers (bees that are presently engaged in foraging) started foraging on two
Table 2 The percentage of bees that stopped (stop) or continued foraging (go on) after having collected dierent-sized pollen loads. Load size categories were distinguished by sight Last load M. fasciata Stop % Go on % n Very large Large Average Small No load 1.8 8.1 5.9 17.8 30.3 98.2 91.9 94.1 82.2 69.7 336 74 68 45 76 M. beecheii Stop % Go on % n 0.0 6.9 28.6 59.3 100.0 93.1 71.4 40.7 113 102 21 27

Fig. 2 The median advance (positive) or delay (negative) in the time (min) at which foragers started foraging compared to the previous day. Values represent the median advance or delay of about 100 foragers. Each trial represents either a sequence of 2 days of normal foraging activity (light columns) or a day of normal foraging followed by a day on which no returnees were allowed to enter the hive, thus when no external information was available to the foragers (dark columns)

111 Fig. 3 Incidence of waste-carrying behaviour in relation to the exit of ve bees when no returnees were allowed to enter the hive. Arrows indicate exits of bees DY1 (0758 hours), BD3 (0932 hours), DB2, DO2 and OD1 (all 0937 hours)

to leave the hive during the no-entry phase of trial 1, and had been inactive on the previous day had been active on 1 or more days of the previous week. Thus, although they had not recently been foraging they were not inexperienced. Moreover, of the nine bees of trial 1 that were almost certainly without foraging experience and only active on the second day, only one started foraging during the no-entry phase, whereas the other eight bees were observed only after foragers had returned to the colony (v2-test: P = 0.02). This indicates that novice bees normally need stimuli from other foragers to initiate foraging. Another factor that stimulated the start of foraging (of four of the ve inexperienced bees that foraged in the no-entry phase of trial 3) seemed to be high activity of bees carrying waste pellets in the entrance area (Fig. 3). This correlation was not observed in the other two trials, because their no-entry phase was much shorter. The eect of external information on colony foraging To assess the eect of external information on colony foraging (both on the number of foragers and on the forager exit pattern) a controlled-entry experiment was set up with three treatments: entry of no foragers, one forager at a time or ve foragers at a time (all foragers used carried full pollen loads). Treatments performed on

Fig. 4 The eect of the number of returnees allowed to enter the hive on the number of outgoing foragers. Each column represents a series of two controlled-entry treatments performed on successive mornings. The percentage of change in the size of the forager force of day 2 compared to the number of outgoing foragers of day 1 is given. Dark columns indicate an increase in forager force, light columns a decrease. Numbers at column base indicate the sequence of treatments, e.g. 01 means rst day treatment 0 second day treatment 1 (treatments: 0 no entry, 1 1 bee entered per event, 5 5 bees entered per event)

two successive days were compared (Figs. 4 and 5). Entry of 1 forager per event resulted in a 1520% larger forager force than the no-entry treatment, whereas a higher number of entries resulted in a 20120% increase. Two successive days of no-entry treatment resulted in a 20% decrease in forager force, whereas 2 days with 5 entries per event resulted in an increase of about 20%. The shapes of the curves in Fig. 5 show that after the rst or the rst two entry events many foragers go out (1st event: 3 outgoing foragers per minute, 2nd event 2 per minute), but that the next entry events have little or no eect. Even the fth event in which 15 foragers were allowed to enter the hive did not result in a strong increase of outgoing foragers, whether the previous entries were low (1 entry per event) or high (5 entries per event). Only in one case (Fig. 5e, black line) did a later entry have a large eect (in this case after less eective rst and second entry events). An entry event resulted in an

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Fig. 5 Eect of forager entry during early morning foraging of M. beecheii. Six of nine pairs of comparisons involving 2 successive days with the same or dierent entry patterns of returning foragers are shown. The three treatments are: no entry (no foragers allowed to enter the hive), 1 entry per event (1 successful pollen forager entered at the rst four moments indicated by an arrow), 5 entries per event (5 successful pollen foragers entered at the rst four moments indicated by an arrow). The last arrow of each trial marks the entry of 1015 successful pollen foragers. The trends in treatments (day 1 vs. day 2) shown are a no entries at all on day 1 and 2; b increase in number of entries from no entry to 1 entry; c, d from 1 entry to 5 entries; e high number of entries on both days, and f high number of entries followed by no entry

been informed about their food sources (Fig. 5f) and advanced the start of their foraging considerably. The mechanism involved in the organisation of individual foraging The median time that pollen foragers of M. fasciata stayed in the nest after having returned from a foraging ight was negatively related to the size of the load (Fig. 6). After an unsuccessful ight a forager stayed up to 6 times longer in the nest than after having collected a very large pollen load. Foragers of M. beecheii that frequented a sugar-water feeder (Fig. 7) performed ``checking'' ights before food was provided. Such ights were slightly longer than foraging ights (t-test: P = 0.001) and were performed at about 10 times longer intervals (t-test: P = 0.0001). After food supply stopped, two to four progressively longer ights were performed with a corresponding in-

elevated rate of departures for about 15 min (range 626 min). This rate was not dierent for the treatment that involved 1 or 5 foragers entering per event (MannWhitney test: P = 0.77). The cumulative number of foragers that had left the hive during each trial (measured after 90 min of foraging) was not dierent for the three treatments (Kruskal-Wallis test: P = 0.41). In one case many foragers initiated foraging without having

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source (Tables 1 and 2; Fig. 6 and 7). The timing of the rst foraging was inuenced by their experience of the previous day and by the arrival of foragers back in the hive (Figs. 2, 4 and 5). Novice bees started foraging after having been stimulated by nest mates (no-entry experiments and Fig. 3). Thus, both learning and communication are important in the regulation of individual foraging in Melipona. Integration of external and internal information: the feedback model It seems that the ow-diagram depicted in Fig. 1 provides a good starting point for the analysis of decisionmaking by Melipona foragers. We could not measure the state of internal and external information of the foragers directly, but approached it by performing the controlledentry experiment. It followed from the feedback model that if external information were cut o, only experienced bees would go out, and inexperienced foragers and foragers that usually went out late would not go out early in absence of external information. Of the foragers 71% (176 individuals) behaved according to the model, whereas 29% (73 individuals) behaved otherwise. Of the latter group, 48 bees went out later than expected and only 25 went out earlier than expected. The bees that went out later than expected were all experienced bees that apparently needed external information to start foraging or otherwise postponed their foraging. Of the 25 bees that went out earlier than expected only 213 could have been novice bees (i.e. 15% of all recordings). The remaining bees were experienced foragers that for unknown reasons did not forage consistently in the period prior to the test day. The feedback model does not predict the outcome of the three possible cases in which conicting information is available (Tables 3 and 4). It is known that experienced honeybee foragers use learned information and conrming external information rather than external
Table 3 Expectations for individual foraging behaviour based on work on honeybees, ants and bumblebees as depicted in Fig. 1. According to the ow diagram at least one information source must be positive for foraging to start (+), if not bees stay in the hive ()). If both internal and external information are positive a forager is expected to start foraging when both refer to the same source. The outcome of the other situations (one type of information positive and the other negative, or both positive, but referring to dierent food sources) are not predicted by the ow diagram (indicated as ?) External information Internal information Pos. Pos. None Neg. +a + ? None + ) ) Neg. ? ) )

Fig. 6 The eect of pollen load size on the duration that a forager stays in the nest after having collected the respective load. The average of the medians of 9 and 10 May 1994 from M. fasciata 1 is shown. Sample sizes were (from very large load to no load): 217, 61, 52, 23, 30 on 9 May; and 159, 32, 34, 32, 71 on 10 May

Fig. 7 Nest time (dark columns) and foraging time (light columns) of Melipona beecheii foragers before (09401020 hours), during (10201130 hours) and after (11301210 hours) food was provided at a sugar-water feeder: mean + SE with sample size in each bar

crease in the time they stayed in the nest after each ight (Fig. 7).

Discussion
The observations and experiments presented in this paper revealed that most experienced Melipona foragers decided to initiate, continue, or stop their daily foraging activity based upon direct experiences with the food

a A forager is expected to go out, but it is not predicted which information source will be used

114 Table 4 Decisions made by individual foragers of M. fasciata for situations that dier in the type and message of information that is available (see Table 3) External information Internal information Pos. Pos. None Neg.
a

information and individual dierences in communication thresholds (Seeley 1994) will inuence colony foraging in Melipona, as it does in honeybees. External information used by Melipona foragers Melipona foragers clearly used information about food sources that they obtained from their nest mates, but what type of information did they use? A returning Melipona may provide nest mates with information on the odour of the food or the taste of the sugar solution and may produce a sound that relates to the distance of the food source (Esch et al. 1965). Moreover, a recruit may follow an outgoing forager and thus be guided to the food (Esch 1967). For experienced foragers of Melipona scent information that matches their experience is sucient to make them return to the feeder they frequented previously (J.C. Biesmeijer, personal observations), as it is for honeybee foragers (von Frisch 1923). Although inexperienced bees may obtain information on quality, direction and distance of the food, they do not nd the food source rapidly (Nieh and Roubik 1995; see next section). This may indicate that location information is not very precise or not used by novices. Preliminary observations on recruitment by M. fasciata and M. beecheii in Costa Rica revealed that novices locate a food source, even when sound is not produced by any of th and J.C. Biesmeijer, unpublished the returnees (E. To work). Inexperienced bees may thus search for a food source of which they know the odour, while they may have only a slight idea of its position. Once arrived near the source, olfactory information, e.g. scent of food or foragers and deposits left by foragers (Kerr 1994; Kerr and Rocha 1988), and visual information, e.g. presence of other foragers at a source further guide a searching bee (J.C. Biesmeijer and W.E.C. Vork, unpublished work). Colony foraging: the eect of information exchange The foraging eciency of a Melipona colony increased through communication between its workers. Information exchange produced an increase of about 25% in the size of the forager force at the short term. Normally most of the foragers of a colony will be employed, and consequently most of the eect of information exchange will be to advance foraging of employed bees. The stimulation of unemployed bees through information exchange seems to have a quantitatively much smaller eect on a Melipona colony's foraging eciency as a result of the low percentage of novice foragers (at least in this study). This observation seems to be conrmed by the study of Nieh and Roubik (1995). They trained ten Melipona panamica (=M. fasciata) foragers to a sugarwater feeder 100 m from the nest and it frequently took them 2 or more days to record the ve to ten recruits they needed to obtain a signicant recruitment eect.

None + ) )

Neg. +/) ) )

+a + +b

A forager will decide according to its internal information or advance its decision if the external information conrms the internal information b It is assumed that a forager will follow its internal information and neglect the external information; +/) indicates that a forager will go out if the external information is about its own source, but will not go out if it informs about another source

information on competing food sources (von Frisch 1923; Seeley et al. 1991; Wenner and Johnson 1966). Von Frisch (1923, p.10) summarised the behaviour of such conditioned bees in the hive after their food source ceased providing food as follows:
``Es unterliegt kein Zweifel, dass sie ruhig im Stocke bleiben, wenn Tausende von Sammlerinnen mit Blu tenstaub und Nektar beladen vom Blumenbesuch heimkehren'' ``There is no doubt that they stay in the hive quietly, when thousands of foragers loaded with pollen and nectar come back in the hive''

Our observations seem to indicate that employed Melipona foragers also neglect external information, except for positive information concerning their own food source. Positive external information about the same food source can stimulate an individual to restart foraging if internal information is negative, e.g. after repeated failures, and to advance the start of its daily foraging. Positive information about another source seems to be neglected by many foragers that stop foraging although nest mates continue to collect food from other sources. The reverse situation, in which a bee is foraging successfully but receives negative external information about its source, may be rare, but a forager will probably ignore the external information and continue foraging. This remains untested however. The results suggest that successful Melipona foragers, like honeybee foragers, rely on the memorised and directly perceived food-source characteristics and are receptive only to communicated information that matches these characteristics. The validation of the feedback model outlined here may be obscured by variation in the quality of information. We tried to diminish the inuence of information quality by using only fully-loaded pollen foragers in our controlled-entry experiment. The observations that the number of bees (1 or 5) that entered per event did not inuence the colony output, and that in the majority of these cases the colony response pattern was similar (high to the rst and second entries and low to subsequent ones) indicate that information quality did not interfere with our results. Under normal conditions the quality of

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Few other food sources were available during the experiments. This low rate of recruitment may, however, be a result of low numbers of recruitable bees present in their colony. Nieh and Roubik (1995) used a colony that consisted of 500800 bees which seems relatively small compared to the colonies in our area, which contain 500 3000 individuals. Daily monitoring of Melipona colonies during other observations (J.C. Biesmeijer, unpublished work) revealed that a M. beecheii colony of 500 bees produced 6 4 brood cells per day (n = 56 days) and a M. beecheii colony of approximately 1000 bees 9 6 cells (n = 58). Thus about half of the six to nine novices that would have been recruitable daily in the small colony of Nieh and Roubik arrived at the experimental feeder, which seems quite ecient. However, if 10 foragers frequent a feeder located 100 m from the hive, as in their experiments, with a typical round-trip time of 24 min (depending on the sugar concentration), about 3 feeder-frequenting foragers will enter the hive per minute, which is 150 per hour. The 5 successful recruits that located the experimental feeder during a complete day of observation were thus the result of about 10001500 forager returns. This seems to demonstrate a low eciency of recruitment of novice bees compared to the very high eciency of information exchange between returning and experienced foragers [even if the percentage of Melipona returnees that actively recruit nest mates is as low as Apis, about 10% (Seeley 1994)]. Moreover, Esch (1967) states that novice Melipona bees did not locate a food source at 300 m distance from the colony within 2030 ights in which they were guided by experienced foragers for the rst 3050 m. In Apis mellifera recruitment eciency also seems low. To locate a food source indicated by a dancer, honeybee recruits need much longer (about 2 h) than the few minutes that direct ight would require (Seeley and Visscher 1988). Experienced honeybees, however, revisit their food source a few minutes after a returning forager has informed them about its reopening (von Frisch 1923). Also, the ecient switching by a honeybee colony from one nectar source to a better source, as shown in the experiments of Seeley et al. (1991) is not a result of individual foragers that switch nectar sources, but of one group of foragers that abandons the deteriorated source and another group (experienced and novice bees) that are recruited to the better food source. An identical experiment with M. fasciata revealed that the colony performed a similar switch to the better source, and that only a few percent of the individuals switched food sources (J.C. Biesmeijer and M.W.C. Ermers, unpublished work). Thus communication is not the only regulatory force in colony foraging, but is complemented by learning. A Melipona colony thus seems to forage as a selforganised superorganism in which individuals make decisions by following simple rules. The mechanisms involved seem to correspond at least partly with those reported for Apis mellifera (Moritz and Southwick 1992; Seeley 1995) and show similarities with decision-making

in foraging ants and bumblebees (Pasteels et al. 1987). Our results suggest that the use of one and the same model of individual foraging may serve as a basis for future studies on social foraging in insects.
Acknowledgements This study would not have been possible without the assistance provided by many people in many ways. Miguel Soto and ARBOFILIA (an NGO from Costa Rica) allowed us to use their bees and provided logistic support. The people of El Sur and ARBOFILIA made our stay very pleasant, and motivated us in our work. Hans van der Pluym assisted in data collection. Laboratory facilities of CINAT and PRAM were available for communication and data analysis thanks to Henry Arce Arce and Johan van Veen. Judith Slaa, Han de Vries, Hayo Velthuis, Marcel Ermers and two anonymous referees improved the manuscript through many corrections and suggestions, for which we are very grateful. This study was supported by The Netherlands foundation for research in the tropics (WOTRO) (grant W84-357 to M.J.S.), the Uyttenboogaart-Elliasen Foundation (J.C.B.), the STIR-programme of Utrecht University (S.L.) and NUFFIC (M.v.N.).

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Communicated by R.F.A. Moritz

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