Abstract
Stingless bees (Hymenoptera: Apidae: Meliponini) are key pollinators of both cultivated and wild plants in tropical and subtropical areas of the world. While most species are found in lowland to mid-elevations, a few have adapted to high elevations, and their biology remains poorly understood. We assess the foraging pattern of Parapartamona zonata (Smith) in the central Andes of Colombia (2583 m.a.s.l.) and apply computer tomography to visualize and characterize its internal nest architecture. Bees foraged for pollen and nesting materials (resin and/or mud) from sunrise (5:40 h) to sunset (17:45), even at ambient temperatures as low as 11 °C. Foraging varied significantly throughout the day and temperature and sky condition explained 47% of its variance. Differences in the nest architecture, when compared with previous records, suggest that nesting behavior might be variable. These results are discussed in the context of behavioral adaptations in this unique environmental niche.
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1 Introduction
Bees play an essential role in ecosystem services and food security as primary pollinators of wild and cultivated plants (Klein et al. 2007; Michener 2007). They are also culturally important, with some species deeply ingrained in the social and biological histories of diverse human populations worldwide (Crittenden 2011; Ayala et al. 2013; Gonzalez et al. 2018). The economic, ecological, and cultural significance of bees is best exemplified by the stingless bees (Apidae: Meliponini), a group of social honey-making bees inhabiting tropical and subtropical regions. Stingless bees are the most common bees in these areas, pollinating a significant part of the native flora, including many important crops such as coffee and macadamia (Slaa et al. 2006; Souza et al. 2021; Bueno et al. 2023). Indigenous and non-indigenous populations rely on stingless bees for honey, pollen, wax, and other products, representing an integral part of their culture and cash economy. However, stingless bees are increasingly threatened by deforestation and other anthropogenic pressures, including the use of pesticides, pathogens, and climate change (Cortopassi-Laurino et al., 2006; Gonzalez et al. 2021; Fleites-Ayil et al. 2023).
Recent niche modelling studies predict significant changes in the geographical distribution of stingless bees under climate change scenarios. For example, reductions of up to 80% of the current distribution area of some South American stingless bees are expected, which might significantly impact pollination services, food security, and livelihoods (Marchioro et al. 2020; Giannini et al. 2020; Gonzalez et al. 2021). However, shifts in elevation are also predicted for some species in the Andes, suggesting differential levels of acclimation to low temperatures among species and that mountainous areas in the tropics might serve as important refuges during global warming for stingless bees (Prieto-Torres et al. 2020; Gonzalez et al. 2021).
Unlike honey bees and bumble bees, stingless bees have limited capabilities to thermoregulate their nests, potentially explaining their restricted distribution to warm climates in lowlands and mid elevations in tropical areas (Roubik 1989; Michener 2007). However, some species of a few genera reach elevations above 2000 m (Roubik et al. 1997; Gonzalez and Engel 2004; Camargo et al. 2023). Among these high-elevation stingless bees, there is a group of seven species found between 1400 and 3400 m from the Andes of Peru to Venezuela (Gonzalez and Nates-Parra 1999; Gonzalez and Smith−Pardo 2003). These species are closely related to the widespread neotropical genus Partamona Schwarz and have been separated into their own genus Parapartamona Schwarz or regarded as a subgenus of Partamona (Michener 2007; Engel et al. 2023; Camargo et al. 2023). The restricted distribution of Parapartamona to colder climates in the Andes suggests physiological or behavioral mechanisms at the individual or colony level to cope with low temperatures. Indeed, a recent study (Gonzalez et al. 2022) revealed that foragers of Parapartamona zonata (Smith) can tolerate temperatures varying from 2 to 4 °C lower than other stingless bee species and honey bees. Unfortunately, despite the small number of species and their presence across several countries in northern South America, the biology of Parapartamona remains poorly studied (Gonzalez and Nates-Parra 1999; Gonzalez and Smith-Pardo 2003).
To date, nests of Parapartamona are known to be partially exposed in different substrates with their entrances covered by vegetation, including moss. In particular, P. zonata nests in a variety of substrates, such as human constructions, soil, tree roots, cavities in tree trunks, and earth banks (Gonzalez and Nates-Parra, 1999). Bravo (1993) studied nests of P. zonata in Ecuador, which consisted of a dense batumen followed by an involucrum, a brood chamber arranged in a spiral, and a food storage area under the combs. Information on the other species remains unknown.
The purpose of this work is twofold: first, to document the foraging pattern and internal nest architecture of P. zonata in the Colombian Andes; second, to apply computer tomography (CT) as a non-invasive tool for the visualization and characterization of stingless bee nests (Greco et al. 2005). Understanding the biology of these high-elevation stingless bees will help us comprehend the traits favoring their adaptation to colder climates and predict which species might thrive in these mountain habitats under climate change. Additionally, knowledge of nesting architecture is crucial for their sustainable use, as many species are now being reared in meliponiculture without considering their basic biological needs, often resulting in colony death (Quezada-Euán et al. 2022).
2 Material and methods
2.1 Study area
We conducted this study from October to December 2021 in Pacho, Cundinamarca, a municipality located within the Andean cloud forest ecosystem in the oriental cordillera of Colombia (5°12′ 7.2″N, 74° 6′ 28.8″W, 2583 m.a.s.l.). The study area is characterized by patches of cloud forest in different successional stages, which are immersed within a matrix of grassland for cattle ranching and Eucalyptus plantations. Rainfall is bimodal, with the highest precipitation in April–May and October–November.
2.2 Foraging activity
We found four nests of P. zonata in the study area, but we chose only one of them that was in a soil bank with easy access to conduct observations on the foraging activity and to document its internal architecture. To assess bees’ daily foraging pattern, we used a cell phone (Motorola G20) mounted in a tripod next to the nest entrance to videorecord bee activity each hour, from 6:00 to 17:00 h, during a 10-min interval. We conducted observations for three consecutive days, each month, from October to December 2021, immediately after we discovered the nests. We used a personal computer to manually analyze each video and recorded the number of individuals arriving to the nest entrance, as well as the type of material they were carrying on their hind legs (corbiculae), such as pollen or material for nest construction (mud or resins). Bees without any load on their hind legs were scored as “empty,” but they might carry water or nectar. To determine the environmental conditions at which bees foraged, we measured ambient temperature and relative humidity with a HOBO datalogger every 15 min for the three consecutive days of our observations each month. We hung the datalogger about 1.5 m above ground from a tree branch that we found next to the nest entrance. In addition, we qualitatively recorded the sky condition as either cloudy and rainy or sunny and clear, serving as a proxy for high or low light intensity. These conditions were dummy coded as 0 or 1, respectively.
2.3 Nest architecture and computerized tomography
To document the internal nest architecture, we dissected the same nest used in the foraging activity analysis. We covered the nest entrance early in the morning before bees started foraging, and we used shovels and pocketknives to extract it from the ground. Then, we transported the nest to the Fundación Clínica Shaio, in Bogotá D.C., Colombia, where we conducted a high-resolution computed axial tomography (CANON Aquilion One). We used the IQ View v2.8 program to visualize and measure the internal structures and used 3D Slicer v4.11. to create a 3D model of the nest. Then, we dissected the nest and estimated the total adult population of the colony by dividing the weight of all individuals recovered from the nest over the average weight of a single individual. The terms used in the nest description follow those of Wille and Michener (1973).
2.4 Statistical analysis
We conducted statistical analyses in R (R Core Team 2018) and created bar graphs using GraphPad Prism, version 7.04 (GraphPad Software, San Diego, CA). To test for differences in the number of bees arriving at the nests at each hour of the day, we implemented a generalized linear mixed-effect model (GLMM) with Poisson distribution using the lmer function in the lme4 package (Bates et al. 2015), with hour and month as fixed factors and the day of observation as a random factor. To test for differences in the number of bees carrying different types of material, we also used a GLMM with a Poisson distribution. In this model, the type of material (pollen, resin/mud, or empty hind legs), hour, and month were considered fixed factors, and day of observation was considered a random factor. To assess the effect of abiotic factors on bee foraging, we conducted a multiple linear regression using the lmer function. The response variable was the number of bees per hour, and the predictors were temperature, relative humidity, and sky condition. Then, we used the function stepAIC from the MASS package (Venables and Ripley 2002) to select the model with the fewest predictors based on the Akaike Information Criterion (AIC) using both forward and backward predictor selection. We assessed the relative importance of each predictor with the package relaimpo (Gröemping 2007) and calculated 95% confidence intervals using a bootstrap with 1000 replicates to test their significance.
3 Results
3.1 Foraging activity
At the study site, air temperature ranged from 11.1 to 19.9 °C (14.6 ± 0.13, n = 174) while relative humidity from 63.8 to 100.0% (94.7 ± 0.63, n = 174). We observed bees leaving or returning to the nest as early as 5:40 h and as late as 17:45 h, when ambient air temperature was as low as 11.1 °C and relative humidity as high as 100%. The number of bees arriving to the nest varied significantly among times of the day (Wald χ2 = 3136.5, DF = 11, P < 0.001) and months (χ2 = 157.4, DF = 2, P < 0.001). The interaction between time of the day and month was also significant (χ2 = 2013.9, DF = 22, P < 0.001). Bees foraged throughout the day without displaying a clear pattern of activity; foraging was highest either in the morning or in the early afternoon (Figure 1a, c, e).
Similarly, the number of bees returning to the nest varied significantly with the type of material being carried (χ2 = 6171.9, DF = 2), time of the day (χ2 = 3136.5, DF = 11), and month (χ2 = 157.4, DF = 2). The interaction between time of the day and month was also significant (χ2 = 2013.9, DF = 22, P < 0.001 in all cases). Bees carried pollen throughout the day, with an average of 32.1% (0.0–50.1% ± 1.94, n = 55) of bees entering the nest each hour engaging in this activity. Resin or mud collection also occurred throughout the day, but the hourly percentage of bees dedicated to this activity accounted for less than 1% (0.0–1.7% ± 0.08, n = 55). The remaining percentage of bees returned to the nest with empty hind legs, probably carrying water or nectar (67.1 ± 2.0, 48.2–100%, n = 55; Figure 1b, d, f).
A multiple regression analysis utilizing the environmental variable temperature, relative humidity, and sky condition to predict the number of bees returning to the nest yielded a significant model, F(3, 28) = 10.24, P < 0.001, R2 = 0.472. Temperature (t = 3.49, P < 0.001) and sky condition (t = 552.7, P < 0.001) were significant predictors, while relative humidity was not (t = 1.0, P = 0.316). Based on Akaike’s information criterion, the best model excluded relative humidity and accounted for 47.1% of its variance. Between the two environmental variables, sky condition exhibited the highest relative importance (67.1%) for explaining the variance in the number of foraging bees.
Finally, as in other stingless bee species, P. zonata was moderately defensive, arriving in groups to the intruder’s head and face, biting the skin and sometimes regurgitating what appeared to be nectar.
3.2 Nest architecture and computerized tomography
We discovered four nests of P. zonata in the study area. Two were situated in cavities of dead tree trunks at about 1 m from the ground, while one (dissected) was in a natural cavity in a soil bank at 1.55 m from the ground, supported by a matrix of tree roots and soil. The last nest was in a ground-level cavity in a soil bank. None of the nests were exposed; all were immersed in the cavity, and only the entrance was visible (Figure 2). Vegetation, such as moss, was consistently found surrounding the nest entrances. We only studied the architecture of one nest, whose entrance consisted of a single funnel-shaped opening at the nest’s base with an approximate diameter of 5 cm, which allowed multiple individuals to enter simultaneously. The nest entrance was built with compact resin bordered by a mixture of mud and moss, displaying a hard consistency, dark gray color, and no ornamentation. Numerous distinctive small subspherical ventilation perforations were observed around the entrance. Typically, the entrance was guarded by 5 to 7 worker bees during the day, and there was no nightly closure. The access tunnel from the entrance to the storage area was straight, 25 cm in lenght, and covered by a hard layer of cerumen with a single curvature opening toward the bottom of the nest.
The nest was surrounded by a thick, hard, light brown batumen, an external wall made of a mixture of resin, mud, and other plant material, including roots and pollen (Figure 3a, b). The nest was oval with an approximate volume of 8 L. Internally, the nest contained the storage area inferior to the brood area, the latter of which was surrounded by five layers of dark brown involucrum (layers of wax mixed with resins) frequently traversed by small branches covered with cerumen (Figure 3c, d). The separation between each layer of involucrum was about 0.5 cm. In some areas, the outer layer of involucrum was attached to the inner wall of the batumen and was harder and more brittle than inner layers. The batumen was thicker superiorly, near the brood area (4.51 cm), and thinner inferiorly, near the storage area (0.45 cm) (Figure 3b).
The storage pots ranged from 1.21 to 2.07 mL in volume, were oval, dark brown like the involucrum, and contained either pollen or honey. Pollen pots were in the upper part of the storage area. The brood area was oval, 13 cm in diameter, 14 cm in height, and about 2 L in volume. Most brood cells were organized into 10 horizontal, spirally patterned combs, but some on top of the brood area were in 5 nearly vertical combs (Figures 3c, d and 4a). Combs ranged from 1.9 to 18.3 cm in diameter and were separated by cerumen pillars 0.39 cm long and 0.17 cm thick. The number of cells in the brood combs ranged from 8 to 11 per cm2. In the horizontal combs, eggs were found in the upper combs, larvae in the middle combs, and pupae in the bottom combs. Unlike the horizontal combs, the five nearly vertical combs contained immatures in different stages of development. No significant differences in the external color of brood combs related to the age of the brood were noted. Food provisions were viscous (Figure 4b–d). Nest measurements are summarized in Table I.
The colony of the excavated nest contained about 15,637 adult workers and 9072 brood cells. No virgin queens or males were observed inside the colony at the time of collection.
4 Discussion
Our observations indicate that Parapartamona zonata forages for both pollen and nesting materials (resin and/or mud) throughout the day, and these activities are positively associated and highly predicted by temperature and other weather conditions. Foraging activity increased with increasing temperature and was high during clear, sunny days. Thus, our results agree with other studies demonstrating that bee foraging is strongly influenced by these abiotic factors (Polatto et al. 2012, 2014; Nates-Parra and Rodríguez 2011). However, other abiotic and biotic factors not accounted for in our study might also influenced bee foraging, such as wind speed, food availability (Stone 1994; Polatto et al. 2014), population size, and colony condition, including foragers’ memory and response threshold (Biesmeijer et al. 1998, 1999; Biesmeijer and de Vries 2001). Relative humidity did not significantly predict the foraging activity of P. zonata, although it is a significant predictor in other bee species (Polatto et al. 2014; Gonzalez et al. 2020). However, relative humidity was relatively homogeneous during the study period. Future studies should assess the effect of this variable during both the dry and rainy seasons.
An interesting result in our study is that P. zonata collected pollen throughout the day. This activity is typically limited to the earlier, cooler hours of the day in colonies of stingless bees inhabiting warmer climates (e.g., de Bruijn and Sommeijer 1997; Hilário et al. 2003; Nates-Parra and Rodríguez 2011; Borges and Blochtein 2005; Souza et al. 2006). Such a pattern has been usually explained as a behavioral adjustment to avoid competitors, prevent water loss, save energy, or to synchronize with pollen release rhythms (e.g., Nates-Parra and Rodríguez 2011; Borges and Blochtein 2005; Souza et al. 2006), but it could also be related to thermal constraints because studies indicate that insect behavior changes at temperatures above 25 °C (Willmer and Stone 2004; Stoks et al., 2017; Speights et al. 2017), but in this case, temperature never exceeded 20 °C. Flying at elevated temperatures makes bees at risk of overheating, particularly if they are carrying pollen (Naumchik and Youngsteadt 2023), so pollen collection is restricted to cooler periods of the day. Bees may also reduce the number or duration of pollen foraging trips to avoid carrying heavy materials during the hotter periods of the day or they shift to nectar or water collection, which may be used in evaporative cooling (Souza-Junior et al. 2020; Maia-Silva et al. 2021). The risk of overheating during pollen collection may be low for stingless bees living in cooler, humid environments, as is the case with P. zonata. Thus, as the ambient temperature did not exceed 20 °C, pollen collection in P. zonata can be extended throughout the day. In colonies that experience seasons, pollen collection is extended during winter when compared to summer (Hilário et al. 2003; Borges and Blochtein 2005), which supports the idea that bees might experience thermal stress during pollen collection at elevated temperatures.
On average, 67.1% of foragers of P. zonata entering the nest had empty corbiculae (Figure 1b, d, f), which agrees with other studies on stingless bees showing a large number of bees returning without pollen loads to the nest (e.g., Nates-Parra and Rodríguez 2011; Borges and Blochtein 2005; Souza et al. 2006). It is often assumed that these foragers carry either water or nectar, which likely occurs during the warmer periods of the day to aid in thermoregulation or evaporative cooling (Souza-Junior et al. 2020; Maia-Silva et al. 2021). We did not examine foragers of P. zonata with empty corbiculae to determine the type of resource they were carrying, or if they were carrying anything at all, but given that foraging may not be limited by high ambient temperatures at these elevations in the Andes, foragers of P. zonata most likely were carrying nectar or water. Nectar is diluted at high elevations (Ornelas et al. 2007; Dalsgaard et al. 2009), which suggests a higher investment in collecting as well as in drying out nectar by high Andean bees when compared to bees from lowlands. Honey bees are known to fan their wings to help evaporate water from nectar as well as to thermoregulate their nest (Jones and Oldroyd 2006; Roubik 2006). We noticed a distinct fanning behavior during our studies, which was loud and constant throughout the day (Supplemental File 1). In addition, when foraging activity was high, we observed guards (5–7 individuals) fanning in front of the nest entrance. Thus, it is possible that foragers of P. zonata employ fanning for similar reasons like honey bees, including the removal of excess of CO2 (Roubik 2006). The ventilation ducts we observed around the entrance and upper part of the batumen might assist with gas exchange and temperature control, as suggested for other species (Wille and Michener 1973; Roubik 2006). Doubtless, further studies should address these questions regarding the collection of nectar as well as the fanning behavior of Parapartamona.
The nesting habits, locations, and substrates of the Colombian nests of P. zonata found in this study align with observations made by Bravo (1993) in Ecuador and anecdotal observations compiled by Gonzalez and Nates-Parra (1999) from labels of museum specimens. The presence of five nearly vertical combs on top of the horizonal combs (Figure 4a), housing immatures in various stages of development, is unusual and possibly indicates a significant shift in the overall position of the nest, which resulted in rebuilding the combs, but bees were unable to move them back to their original position. Stingless bee nests are perennial, and considering that the examined nest was inside a cavity in a soil bank, it seems reasonable to assume that erosion or a predator trying to reach the nest could have caused a shift in the nest’s position. However, the nests we found were all completely covered, unlike those previously reported, which were semi-exposed, as in some species of Partamona. Additionally, unlike the nests observed in Ecuador, the nest studied in Colombia did not have a space between the batumen and the surrounding soil. Instead, the batumen was continuous with the substrate, as reported in some ground-nesting species of Partamona (Camargo and Pedro 2003). Thus, our results suggest that nesting behavior in P. zonata might be variable. This variability is not surprising as stingless bees exhibit marked inter- and intraspecific variations in the external nest entrance, internal nest features, and nesting substrate. These variations might result from constraints imposed by nest site limitations and are often influenced by geographical, environmental, and phylogenetic factors (Camargo and Pedro 2003; Rasmussen and Camargo 2008; Roubik 2006).
The adult population estimate for the P. zonata nest revealed 15,637 individuals, a count falling within the range observed for various stingless bee species (Michener 2007). While some species of Partamona have reported a maximum of 3000 adult individuals (Camargo and Pedro 2003), P. zonata exhibited a notably larger population size. Stingless bees are thermoconforms at low elevations but display some thermoregulation abilities at mid-elevations (Gonzalez et al. 2022). Thus, a large population size in P. zonata might be advantageous for passively or actively thermoregulating the colony at high elevations in the Andes.
Finally, the use of X-ray computerized tomography to study stingless bee nests is rare, even though this technique has been more widely applied in other social insects such as ants and termites (e.g., Halley et al. 2005; Perna et al. 2008). To date, the only other study using X-ray computerized tomography on stingless bees is that of Greco et al. (2005), which monitored colony development of the Australian Tetragonula carbonaria (Smith) inside wooden hive boxes. We applied this technique to a subterranean nest, demonstrating its applicability to stingless bees with different nesting habits. Our study also illustrates that X-ray computerized tomography can accurately calculate nest volume as well as surface areas of the internal nest structure, which are typically challenging to determine using traditional methods. Additionally, 3D reconstruction of nests from CT-scan sections are powerful tool for scientific outreach, as they provide an immersive experience for the audience (see Supplemental File 2). Although promising, one of the main limitations of this technique is accessibility, as well as the cost of the equipment. This is particularly critical in tropical developing countries where stingless bees occur and need to be studied.
5 Conclusions
We assessed for the first time the daily foraging pattern of P. zonata, shedding light on its nesting habits and internal nest architecture in the Colombian Andes. Our findings revealed significant variations in foraging activity throughout the day, with temperature and sky condition as key predictors. Our work provides valuable insights into the species’ behavioral adaptations to the varying environmental conditions at high elevations in the Andes. We used computer tomography to visualize and characterize the internal nest architecture of P. zonata. This non-invasive approach allowed us to obtain informative images and measurements of the nest structure without direct manipulation, highlighting its potential for future research on stingless bee nests. This technique is promising, as it has also been applied to study the nest structure of solitary ground-nesting bees (Tschanz et al. 2023) as well as to detect parasitized cells of solitary cavity-nesting bees (Thomson et al. 2022). It is important to note that our study focused on a single nest from one population during the rainy season. Given the species’ extensive distribution, from Peru to Colombia between 1400 and 3400 m, and the potential variations in environmental conditions during the dry season (lower humidity and higher solar radiation), we anticipate changes in nesting and foraging behaviors. Future studies should consider collecting data during the dry season and examine nests at other locations to provide a more comprehensive understanding of the species’ biology at high elevations.
Data availability
The data is available in supplementary materials.
Code availability
Not applicable.
References
Ayala R, Gonzalez VH, Engel MS (2013) Mexican stingless bees (Hymenoptera: Apidae): diversity, distribution, and indigenous knowledge. Pot-Honey: A Legacy of Stingless Bees (ed. by P. Vit, S.R.M. Pedro & D. Roubik) 135–152. Springer Science, New York, NY
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Biesmeijer JC, de Vries H (2001) Exploration and exploitation of food sources by social insect colonies: a revision of the scout-recruit concept. Behav Ecol Sociobiol 49(2):89–99
Biesmeijer JC, van Nieuwstadt MG, Lukács S, Sommeijer MJ (1998) The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae). Behav Ecol Sociobiol 42(2):107–116
Biesmeijer JC, Born M, Lukács S, Sommeijer MJ (1999) The response of the stingless bee Melipona beecheii to experimental pollen stress, worker loss, and different levels of information input. J Apic Res 38(1–2):33–41
Borges FV, Blochtein B (2005) Actividades externas de Melipona marginata obscurior Moure (Hymenoptera, Apidae), em distintas épocas do ano, em Sao Francisco de Paula, Rio Grande do Sul. Brasil Rev Bras Zool 22(3):680–686
Bravo F (1993) Descriçao dos ninhos de Parapartamona zonata (Smith, 1854) e Parapartamona brevipilosa (Schwarz, 1948) (Hymenoptera, Apidae, Meliponinae) colectados nos Andes ecuatorianos. Rev Bras Entomol 37(4):779–785
Bueno FGB, Kendall L, Araujo D, Lequerica M, Heard T, Latty T, Gloag R (2023) Stingless bee floral visitation in the global tropics and subtropics. Glob Ecol Conserv 43:e02454
Camargo JMF, Pedro SRM, Melo GAR (2023) Meliponini Lepeletier, 1836. In Moure, J. S. Urban, D. & Melo, G. A. R. Orgs. Catalogue of Bees Hymenoptera, Apoidea in the Neotropical Region. http://www.moure.cria.org.br/catalogue
Camargo JMF, Pedro SRM (2003) Meliponini neotropicais: o gênero Partamona Schwarz, 1939 (Hymenoptera, Apidae, Apinae) — bionomia e biogeografia. Rev Bra Entomol 47(3):311–372
Cortopopassi-Laurino M, Imperatriz-Fonseca VL, Roubik DW, Dollin A, Heard T, Aguilar I, Venturieri GC, Eardley C, Nogueira-Neto P (2006) Global meliponiculture: challenges and opportunities. Apidologie 37:275–292
Crittenden AN (2011) The importance of honey consumption in human evolution. Food Foodw 19:257–273
Dalsgaard B, González AMM, Olesen JM, Ollerton J, Timmermann A, Andersen LH, Tossas AG (2009) Plant-hummingbird interactions in the West Indies: floral specialization gradients associated with environment and hummingbird size. Oecologia 159:757–766
de Bruijin LLM, Sommeijer MJ (1997) Colony foraging in different species of stingless bees (Apidae, Meliponinae) and the regulation of individual nectar foraging. Insectes Soc 44:35–47
Engel MS, Rasmussen C, Ayala R, de Oliveira FF (2023) Stingless bee classification and biology (Hymenoptera, Apidae): a review, with an updated key to genera and subgenera. ZooKeys 1172:239–312
Fleites-Ayil FA, Medina-Medina LA, Quezada JJG, Stolle E, Theodorou P, Tragust S, Paxton RJ (2023) Trouble in the tropics: pathogen spillover is a threat for native stingless bees. Biol Conserv 284:110150
Giannini TC, Costa WF, Borges RC, Miranda L, Wanzeler da Costa CP, Saraiva AM, Imperatriz-Fonseca VL (2020) Climate change in the Eastern Amazon: crop-pollinator and occurrence-restricted bees are potentially more affected. Reg Environ Change 20:9. https://doi.org/10.1007/s10113-020-01611-y
Gonzalez VH, Engel MS (2004) The Tropical Andean bee fauna (Insecta: Hymenoptera: Apoidea), with examples from Colombia. Entomol Abh 62(1):65–75
Gonzalez VH, Smith-Pardo A (2003) New distribution records and taxonomic comments on Parapartamona (Hymenoptera: Apidae: Meliponini). J Kansas Entomol Soc 76(4):655–657
Gonzalez VH, Amith JD, Stein TJ (2018) Nesting ecology and the cultural importance of stingless bees to speakers of Yoloxóchitl Mixtec, an endangered language in Guerrero. Mexico Apidologie 49(5):625–636
Gonzalez VH, Hranitz JM, Percival CR, Pulley KL, Tapsak ST, Tscheulin T, Petanidou T, Barthell JF (2020) Thermal tolerance varies with dim-light foraging and elevation in large carpenter bees (Hymenoptera: Apidae: Xylocopini). Ecol Entomol 45(3):688–696
Gonzalez VH, Cobos M, Jaramillo J, Ospina R (2021) Climate change will reduce the potential distribution ranges of Colombia’s most valuable pollinators. Perspect Ecol Conserv 19(2):195–206
Gonzalez VH, Oyen K, Vitale N, Ospina R (2022) Neotropical stingless bees display a strong response in cold tolerance with changes in elevation. Conserv Physiol 10: 073
González VH, Nates-Parra G (1999) Sinopsis de Parapartamona (Hymenoptera: Apidae: Meliponini), un género estrictamente andino. Rev Acad Colomb Cienc Exactas Fís Nat 23:171–179
Greco M, Spooner-Hart R, Holford P (2005) A new technique for monitoring Trigona carbonaria nest contents, brood and activity using X-ray computerized tomography. J Apic Res 44(3):97–100
Gröemping U (2007) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17:1–27
Halley JD, Burd M, Wells P (2005) Excavation and architecture of Argentine ant nests. Insectes Soc 52:350–356
Hilário SD, Gimenes M, Imperatriz-Fonseca VL (2003) The influence of colony size in diel rhythms of flight activity of Melipona bicolor Lepeletier Hymenoptera, Apidae, Meliponini. In: Apoidea Neotropica Mello GAR and Alves dos-Santos I, eds. Editora UNESC, Criciúma: 191–197
Jones JC, Oldroyd BP (2006) Nest thermoregulation in social insects. Adv Insect Physiol 33:153–191
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. P Roy Soc B-Biol Sci 274:303–313
Maia-Silva C, JdaS P, Freitas BM, Hrncir M (2021) Don’t stay out too long! Thermal tolerance of the stingless bees Melipona subnitida decreases with increasing exposure time to elevated temperatures. Apidologie 52:218–229
Marchioro CA, Lima VP, Sales CR (2020) Climate change can affect the spatial association between stingless bees and Mimosa scabrella in the Brazilian Atlantic Forest. Apidologie 51:689–700. https://doi.org/10.1007/s13592-020-00753-6
Michener CD (2007) The bees of the world, 2nd edn. Johns Hopkins University Press, Baltimore
Nates-Parra G, Rodríguez Á (2011) Forrajeo en colonias de Melipona eburnea (Hymenoptera: Apidae) en el piedemonte llanero (Meta, Colombia). Rev Colomb Entomol 37(1):121–127
Naumchik M, Youngsteadt E (2023) Larger pollen loads increase risk of heat stress in foraging bumblebees. Biol Lett 19:20220581. https://doi.org/10.1098/rsbl.2022.0581
Ornelas JF, Ordano M, De-Nova AJ, Quintero ME, Garland T (2007) Phylogenetic analysis of interspecific variation in nectar of hummingbird-visited plants. J Evol Biol 20:1904–1917
Perna A, Jost C, Couturier E, Valverde S, Douady S, Theraulaz G (2008) The structure of gallery networks in the nests of termite Cubitermes spp. revealed by X-ray tomography. Naturwissenschaften 95:877–884
Polatto LP, Chaud-Netto J, Dutra JCS, Alves Junior VV (2012) Exploitation of floral resources on Sparattosperma leucanthum (Bignoniaceae): foraging activity of the pollinators and the nectar and pollen thieves. Acta Ethol 15(1):119–126
Polatto LP, Chaud-Netto J, Alves-Junior VV (2014) Influence of abiotic factors and floral resource availability on daily foraging activity of bees. Influence of abiotic and biotic factors on bees. J Insect Beh 27(5):593–612
Prieto-Torres DA, Lira-Noriega A, Navarro-Sigüenza AG (2020) Climate change promotes species loss and uneven modification of richness patterns in the avifauna associated to Neotropical seasonally dry forests. Perspect Ecol Conser 18(1):19–30. https://doi.org/10.1016/j.pecon.2020.01.002
Quezada-Euán JJ, May-Itzá WJ, de la Rúa P, Roubik DW (2022) From neglected to stardom: how the rising popularity of stingless bees threatens diversity and meliponiculture in Mexico. Apidologie 53:70. https://doi.org/10.1007/s13592-022-00975-w
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.r-project.org/
Rasmussen C, Camargo JMF (2008) A molecular phylogeny and the evolution of nest architecture and behavior in Trigona s.s. Hymenoptera Apidae Meliponini. Apidologie 39(1):102–118
Roubik DW (1989) Ecology and natural history of tropical bees. Cambridge University Press, New York
Roubik DW (2006) Stingless bee nesting biology. Apidologie 37:124–143
Roubik DW, Lobo Segura JA, Camargo JMF (1997) New stingless bee genus endemic to Central American cloud forests: phylogenetic and biogeographic implications (Hymenoptera: Apidae: Meliponini). Syst Entomol 22:67–80
Slaa EJ, Sánchez LA, Malagodi-Braga KS, Hofstede FE (2006) Stingless bees in applied pollination: practice and perspectives. Apidologie 37(2):293–315
Souza BA, Carvalho CAL, Alves RMO (2006) Flight activity of Melipona asilvai Moure (Hymenoptera: Apidae). Braz J Biol 66(2b):731–737
Souza F, Pinto CE, Melo de Brito R, Imperatriz-Fonseca VL, Giannini TC (2021) Edible fruit plant species in the Amazon forest rely mostly on bees and beetles as pollinators. J Econ Entomol 114(2):710–722
Souza-Junior JBF, Teixeira-Souza VHdaS, Oliveira-Souza A, de Oliveira PF, de Queiroz JPAF, Hrncir M (2020) Increasing thermal stress with flight distance in stingless bees (Melipona subnitida) in the Brazilian tropical dry forest: implications for constraint on foraging range. J Insect Physiol 123:104056. https://doi.org/10.1016/j.jinsphys.2020.104056
Speights CJ, Harmon JP, Barton BT (2017) Contrasting the potential effects of daytime versus nighttime warming on insects. Curr Opin Insect Sci 23:1–6
Stoks R, Verheyen J, Van Dievel M, Tüzün N (2017) Daily temperature variation and extreme high temperatures drive performance and biotic interactions in a warming world. Curr Opin Insect Sci 23:35–42
Stone GN (1994) Activity patterns of females of the solitary bee Anthophora plumipes in relation to temperature, nectar supplies and body size. Ecol Entomol 19(2):177–189
Thomson BR, Hagenbucher S, Zboray R, Oesch MA, Aellen R, Richter H (2022) Automated computed tomography based parasitoid detection in mason bee rearings. PLoS ONE 17(10):e0275891
Tschanz P, Koestel J, Volpe V, Albrecht M, Keller T (2023) Morphology and temporal evolution of ground-nesting bee burrows created by solitary and social species quantified through X-ray imaging. Geoderma 438:116655
Venables WN, Ripley BD (2002) MASS: Modern applied statistics with S, 4th edn. Springer, New York, NY
Wille A, Michener CD (1973) The nest architecture of stingless bees with special reference to those of Costa Rica (Hymenoptera, Apidae). Rev Biol Trop 21(1):1–278
Willmer PG, Stone GN (2004) Behavioral, ecological, and physiological determinants of the activity patterns of bees. Adv Stud Behav 34(34):347–466
Acknowledgements
We thank Vera Lucia Imperatriz Fonseca, Guiomar Nates Parra, and anonymous reviewers for comments and suggestions that improved this manuscript. Mr. Julián Lozano, owner of El Paraíso farm in Pacho, Cundinamarca, for allowing us to conduct our study in his property and Rubén Darío Martin and Andrés Felipe Velasco for their help with field work.
Funding
Open Access funding provided by Colombia Consortium JCJ, DAR-J, and JRC were supported by the general research funds of the Universidad Militar Nueva Granada. X-ray computerized tomography was funded by the Fundación Clínica Shaio (DIB-23–07). VHG was partially supported by the University of Kansas’ Center for Latin American and the Caribbean Studies and National Science Foundation (EAR 1950805).
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JCJ and AH-M conducted field work; JCJ and DAR-J studied the nest using X-ray tomography; JCJ and VHG analyzed data and wrote manuscript. All authors reviewed, edited, and approved the manuscript.
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Jacome-García, J.C., Gonzalez, V.H., Riaño-Jimenez, D.A. et al. Foraging behavior and the nest architecture of a high-Andean stingless bee (Hymenoptera: Apidae: Meliponini) revealed by X-ray computerized tomography. Apidologie 55, 33 (2024). https://doi.org/10.1007/s13592-024-01074-8
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DOI: https://doi.org/10.1007/s13592-024-01074-8