Corresponding author: Fábio Santos Nascimento (
Academic editor: Jack Neff
The nesting biology and social behavior of the euglossine bee species
The bees of the tribe
A diversity of nesting behavior is observed in the different species of
Observations of the intranidal behavior of
Similar social organization have been reported by
This long-term study presents new data on the nesting behavior of
The present study took place within the urban area of the town of Campo Formoso (
A total of eight
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N1 | 04/08/2008 | 16 OC; 3 UC; 2 PC; 2 F†; 2 F |
N2 | 15/08/2008 | 9 OC; 5 UC; 1 PC; 2 F |
N3 | 02/09/2008 | 11 OC; 1 F |
N4 | 17/09/2008 | 12 OC; 1 PC; 1 F†; 1 F |
N5 | 21/09/2008 | 8 OC; 5 UC; 1 PC; 3 F; 4 F† |
N6 | 24/09/2008 | 8 OC; 1 PC; 1 F |
N7 | 30/09/2008 | 11 OC; 1 F |
N8 | 30/09/2008 | 22 OC; 15 UC; 1 PC; 2 F†; 1 F |
The nests were observed under red light between 07:00 h and 18:00 h, with eight hours of observation being conducted three days per week. Nocturnal observations were made once a week between 19:00 and 23:00 h. Quantitative behavioral data were collected using two complementary procedures. All-events records (
Nest development was monitored for the collection of data on the following biological and behavioral parameters: (a) cell architecture; (b) nest reactivation and phenology; (c) female foraging behavior; (d) specific aspects of the activity of the females during construction, i.e. reuse of cells, supply, oviposition, cell closure, oophagy, cleaning the nest and the sealing of edges; (e) duration of the period of offspring development; (f) physiological condition of the females (relative fecundity).
Where appropriate, the results were presented as the mean ± standard deviation. The relationship between the number of cells with eggs and the duration of the female activity period was evaluated using Pearson’s correlation coefficient, while Mann-Whitney’s
Cells of
The emergence of 112 females was monitored. Of these, 90 (80.3%) returned to their natal nests, but only 35 (38.9%) remained and actively participated in nest re-use. The other 55 (49.1%) abandoned their natal nests a few days (1–3 days) after their return, without working in the nest. The younger females, more frequently (89.1%, n = 55), abandoned nests days after returning. The great majority (87.1%) of the 31 reactivations observed during the present study involved associations among females. 27 (87.1 %) of these reactivations were performed by more than one female and only four (12.9 %) by one female (
Number of reactivating females and function assumed in the reactivations occurred in
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N1/R1 | X | 54 | 2 | 1 | 1 | 11 | |
N1/R2 | X | 43 | 2 | 1 | 1 | 9 | |
N1/R3 | X | 41 | 2 | 1 | 1 | 13 | |
N1/R4 | X | 28 | 2 | 1 | 1 | 10 | |
N1/R5 | X | 38 | 2 | 1 | 1 | 13 | |
N2/R1 | X | 43 | 2 | 1 | 1 | 9 | |
N2/R2 | X | 52 | 3 | 1 | 2 | 11 | |
N2/R3 | X | 31 | 2 | 1 | 1 | 10 | |
N2/R4 | X | 42 | 1 | 1 | 0 | 13 | |
N2/R5 | X | 22 | 2 | 1 | 1 | 8 | |
N3/R1 | X | 51 | 1 | 1 | 0 | 10 | |
N3/R2 | X | 44 | 2 | 1 | 1 | 9 | |
N4/R1 | X | 53 | 1 | 1 | 0 | 10 | |
N4/R2 | X | 35 | 2 | 1 | 1 | 12 | |
N4/R3 | X | 24 | 2 | 1 | 1 | 8 | |
N4/R4 | X | 37 | 2 | 1 | 1 | 12 | |
N4/R5 | X | 13 | 2 | 1 | 1 | 5 | |
N5/R1 | X | 49 | 2 | 1 | 1 | 10 | |
N5/R2 | X | 10 | 3 | 1 | 2 | 4 | |
N5/R3 | X | 46 | 2 | 1 | 1 | 10 | |
N6/R1 | X | 51 | 1 | 1 | 0 | 10 | |
N6/R2 | X | 23 | 2 | 1 | 1 | 6 | |
N6/R3 | X | 36 | 2 | 1 | 1 | 12 | |
N6/R4 | X | 34 | 2 | 1 | 1 | 11 | |
N6/R5 | X | 26 | 2 | 1 | 1 | 9 | |
N7/R1 | X | 49 | 2 | 1 | 1 | 10 | |
N7/R2 | X | 51 | 2 | 1 | 1 | 11 | |
N8/R1 | X | 78 | 3 | 1 | 2 | 12 | |
N8/R2 | X | 50 | 3 | 1 | 2 | 13 | |
N8/R3 | X | 47 | 3 | 1 | 2 | 12 | |
N8/R4 | X | 38 | 2 | 1 | 1 | 12 |
During the intervals between reactivations or during periods of inactivity, the females spent more time inside the nests without engaging in cell construction or provisioning. The number of oviposited cells significantly positively correlated with the duration (in days) of the activity period of the females (
Subordinate females constructed or reutilized cells using resin deposited in small piles inside the nests. Of the 124 cells which were oviposited in, 92 cells (74.2%) were reutilized, while 32 cells (25.8%) were newly constructed. Females began to collect resin two (n = 39) or three (n = 67) days after emergence, and engaged in this activity throughout the day, but with a higher frequency between 14:00 h and 15:00 h (
Frequency of excursion from the nest by subordinate female
Females began to collect and to store food for the larvae four (n = 61) or five days (n = 65) after emergence. The mean duration of food-gathering excursions was 54.4±11.60 min (range: 33–81 min, n = 63), while food storage took 35.1±12.65 s (13–73s, n = 51). Food was gathered primarily in the morning, between 09:00 h and 11:00 h (
Females would occasionally return to the nest with neither food nor resin. These excursions were possibly for nectar collection and lasted 27.1±3.58 min (range: 7–68 minutes, n = 78) for dominant females, and 17.5±8.85 min (7–37 min, n = 37) for subordinates. While these trips occurred throughout the day, they were more frequent during the morning (n = 115), primarily between 07:00 h and 08:00 h (
Subordinate females prepared cells for oviposition by building the collar. Construction of the collar took 28.0±13.44 minutes (range: 11–65 min, n = 97) on average. Once they she had built the collar, a subordinate oviposited in the cell, but a dominant female almost always subsequently substituted her egg for that of the subordinate. The duration of bouts of this activity differed significantly (Z = 8.86; p <0.0001, n = 77) between subordinate (120.8±23.48 s, range: 68–155 s, n = 56) and dominant females (88.1±16.70 s, range: 61–125 s, n = 56). Oviposition (n = 97) took place between 09:00 h and 17:00 h, but was most frequent between 13:00 and 15:00 h (
Frequency of oviposition by female
The time spent on cell closure also differed significantly between subordinate and dominant females (Z = 6.08;
Dominant females spent most of their time inside the nests. This behavior was more frequent (70.4%, n = 366) when the subordinates were foraging The average duration of periods spent by dominant females in the nest guarding position was 13.2±6.13 min (range 6–30, n = 366).
Of the 31 processes reactivations observed, in 14 (45.1%) the dominant females disappeared, died or ceased ovipositing and were replaced by another female. In all cases, the substitute was another female that had emerged in the nest.
Following the emergence of a female and before the reutilization of a cell, the subordinate females cleaned the cell by removing the silk and pieces of the cell closure. This detritus was deposited on the bottom of the box. The mean duration of this behavior was 12.0±5.35 min (range: 2–27, n = 306).
The mean duration of resin work bouts was 10.3±5.0 min (range: 2–29, n = 256) for subordinates, and 9.6±4.18 min (range: 2.5–19.8, n = 126) for dominant females. This difference was not significant (Z = 1.04;
Dominant females opened the closed cells in which subordinates had oviposited after an interval of between 31 and 240.3 min (i.e., more than four hours) after cell closure. Prior to reopening the cells, the dominant females behaved aggressively towards subordinates by biting and pulling them from the closed cell. Opening a cell took an average of 16.7±2.34 min (range: 12.6–21.68 min, n = 62). Following more than half (61% of 141 observed acts) of the subordinate ovipositions, the dominant female ingested the subordinate’s egg. Oophagy took between 96 and 248 s (mean = 158.4±45.65 s, n = 86). Oophagy (86 events) occurred between 10:00h and 18:00h, and was most frequent (n = 61) between 14:00h and 18:00h (
Frequency of oophagy by dominant female
The length of brood development was compared between the rainy and dry seasons. The period was significantly longer during the rainy season (rainy season – males: 75.7 ± 3.55 days and females: 82.3 ± 1.92 days; dry season – males: 56.2 ± 0.86 days and females: 61.7 ± 2.44 days;
Duration in days of the development period (egg-adult) of the brood (male and female) of
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N1 | 55.2 | 62.3 | 77.6 | 79.5 |
N2 | 55.6 | 59.3 | 75.4 | 84.3 |
N3 | 56.1 | 58.9 | - | - |
N4 | 57.3 | 63.8 | 69.8 | 81.5 |
N5 | 55.8 | 63.5 | - | - |
N6 | 57.5 | 58.4 | 76.4 | 82.2 |
N7 | 55.4 | 64.7 | - | - |
N8 | 56.6 | 62.4 | 79.1 | 83.8 |
The spermathecae of two dominant and three subordinate females were dissected for the analysis of possible differences related to social rank. The analysis revealed long ovarioles with mature or maturing oocytes and all females were inseminated.
The exploitation of pre-existing cavities for the construction of nests observed in
The replacement of the dominant female by a subordinate female is consistent with the hypothesis of an age-based dominance hierarchy, as occurs in other primitively eusocial bee species (
The reactivation and abandoning of nests by
Larval provisioning requires large expenditures of time and energy for
In associations of
The high rates of return (80%) and effective reactivation (39%) recorded in
Because all nest-mates have developed ovaries, have mated, and do not differ in size, dominant and subordinate females are recognized by their behavioral characteristics. Dominant females exhibited agonistic behaviors towards subordinates and the intensities of these aggressive behaviors where the dominant female had already participated in a reactivation process.
The agonistic interactions observed in
Although the agonistic behaviors displayed by dominant females do not prevent oviposition by subordinate females, reproductive dominance, reflected in the monopolization of offspring production, is achieved by the dominant female through the replacement of subordinate female eggs with her own. The monopolization of offspring production leads to the highest reproductive skew, as predicted by the concession-based transactional skew model (
If the dominant female of
In
Oophagy of some dominant’s eggs by subordinates was also observed in
The oophagy of subordinate’s eggs preceding oviposition by the dominant was also observed in reactivated nests of
As emphasized by Zimmerman et al. (2009), detailed behavioral observations together with the genetic analysis of brood can help clarify the relationships among all females of an association and the real contribution of each one to the social context of the nest.
Oophagy may have a nutritional function (
The females of
The development period was similar for males and females, although seasonal variation was influenced by environmental factors, such as the temperature. Higher temperatures may contribute to increased metabolic rates, which may reduce development time considerably (
Presumably single females can establish a new nest. Their subordinate status is determined only by the presence of a dominant.These females may be in a state of “sit and waiting” (
The nesting behavior of
We are grateful to the beekeepers Fred and Marcos Rogério for their help with the localization and transfer of the nests, and to Manoel Joaquim and Ana Maria for authorizing access to the nests and to Dr. Stephen Francis Ferrari and two anonymous reviewers for their critical analysis and suggestions for improvement of the text.The Brazilian National Research Council (CNPq) and Fapesp (2010/10027-5) provided graduate stipends to the first author and a productivity grant to F.S.N.