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bee (Scaptotrigona depilis) to nest overheating

Ayrton Vollet-Neto, Cristiano Menezes, Vera Lucia Imperatriz-Fonseca

To cite this version:

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Behavioural and developmental responses of a stingless bee

(Scaptotrigona depilis ) to nest overheating

Ayrton VOLLET-NETO1,Cristiano MENEZES2,Vera Lucia IMPERATRIZ-FONSECA3 1Departamento de Biologia da Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Universidade de São Paulo,

Av. Bandeirantes, 3900, Ribeirão Preto, São Paulo 14040-900, Brazil 2Embrapa Amazônia Oriental, Tv. Dr. Enéas Pinheiro, s/n., Belém, Pará, Brazil 3Universidade Federal Rural do Semi-Árido, km 470-BR110, Mossoró, Rio Grande do Norte, Brazil

Received 15 April 2014– Revised 16 November 2014 – Accepted 21 November 2014

Abstract– In this study, we investigate the behavioural response of the highly eusocial stingless bee Scaptotrigona depilis to high temperatures. We found that nest temperature in the brood area can be up to 2.5 °C lower relative to a control empty box during hot periods. We showed that high temperatures increase both water collection and wing fanning behaviour at the colony level, suggesting that these behaviours are adaptations to cooling the nest in this species. Additionally, we measured survival and development time of pupae incubated at five different constant temperatures (22, 26, 30, 34 and 38 °C). We found that the development time of S. depilis brood significantly varied between treatments and had a strong negative correlation with temperature. Brood survived over a large range of incubation temperatures; however, extreme temperatures (22 and 38 °C) were almost 100 % lethal, highlighting the importance of thermoregulation, at least in extreme conditions.

social thermoregulation / nest cooling / water foraging / Scaptotrigona depilis

1. INTRODUCTION

Social bees are able to control the nest environ-ment to allow optimal performance of the adults as well as optimal development of the brood (Wilson

1971; Jones and Oldroyd2007). In particular, so-cial bees are sensitive to, and invest considerable effort in controlling, the temperature within the nest. Honeybees (Apis mellifera ) are very effective at controlling their internal nest temperature. The workers can perform quite well over a wide range of temperatures, but the brood is very sensitive to temperature fluctuations. The cognition ability of

adult bees especially to foraging activities are af-fected even by 2 °C of difference between temper-atures they were raised (Tautz et al.2003). More-over, mortality and malformation increase when brood is reared outside of a very narrow range of optimal temperatures (Himmer 1927; Heinrich

1993; Mardan and Kevan2002)

Nest temperature can be increased through metabolic heating generated by the shivering of flight muscles in bumblebees (Hymenoptera, Apidae, Bombini) and honeybees (Hymenoptera, Apidae, Apini) (Jones and Oldroyd2007). These groups also have the ability to cool their nests. The honeybee is able to maintain the internal nest temperature within a narrow range of 33 to 36 °C, even when the external temperatures are higher than 40 °C (Heinrich1993). To accomplish this, workers fan their wings to create an air flow between the inside and the outside of the nest. This behaviour is combined with water collection, where small droplets of water are deposited on

Electronic supplementary material The online version of this article (doi:10.1007/s13592-014-0338-6) contains supplementary material, which is available to authorized users.

Corresponding author: A. Vollet-Neto, ayrtonvollet@gmail.com

Manuscript editor: Peter Rosenkranz

Apidologie (2015) 46:455–464

Original article

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surfaces on the inside of the nest. This reduces the temperature of the nest through evaporative cooling (Lindauer 1954). In Bombus , only fan-ning behaviour has been reported and is correlated with an increase in nest temperature (Jones and Oldroyd2007).

Stingless bees (Hymenoptera, Apidae, Meliponini) are the largest and most diverse group of highly eusocial bees (Michener2000). They are restricted to tropical and subtropical habitats and are, therefore, often exposed to high temperatures. However, there is no evidence that they perform behaviours to actively cool the nest (Jones and Oldroyd2007). Research shows that the internal nest temperature differs from ambient tempera-ture, but most authors attribute this to the behav-iour of nesting in insulated cavities and assume that this is the main way by which stingless bees avoid nest temperature rising to damaging levels during hot periods (Engels et al.1995; Nogueira-Neto 1997; Jones and Oldroyd 2007). On the other hand, wing fanning has been described in several species in this group, leading some re-searchers to suggest that this might be a cooling behaviour (Nogueira-Neto1948; Macías-Macías et al.2011). However, this hypothesis has yet to be tested. Engels et al. (1995), working with Scaptotrigona postica , observed that colonies experiencing high temperatures had elevated numbers of bees performing wing fanning. Macías-Macías et al. (2011) demonstrated that workers of Melipona colimana kept individually in boxes inside incubators perform wing fanning behaviour when exposed to temperatures of 40 °C. However, Moritz and Crewe (1988) point-ed out that wing fanning plays a role in air circu-lation inside the nest, regulating the CO2and O2 levels inside the nest cavities of the ground nesting species Trigona denotii . Nogueira-Neto (1948) also reports the occurrence of fanning be-haviour in stingless bee colonies during cold win-ter days, suggesting that this behaviour is related to gas exchange, rather than temperature regulation.

There are a few reports of water collection in stingless bee species (Nogueira-Neto 1997; Macías-Macías et al.2011). However, the authors associate this behaviour with individual ingestion of water and minerals and reject the hypothesis

that it plays a role in the cooling of the nest because the deposition of water droplets was nev-er obsnev-erved inside colonies and because cavity nesting is considered to provide a thermally stable environment (Engels et al. 1995). On the other hand, Macías-Macías et al. (2011), working with individual workers of Melipona colimana , found that high temperatures led to an increase in water consumption, and that workers regurgitated the water on the bottom of the boxes. The authors suggested that this individual behaviour could be used at the colony level to decrease the tempera-ture of the nest.

In preliminary observations, we noted that Scaptotrigona depilis can maintain relatively sta-ble temperature inside the nest during periods of extreme heat. This is in line with the observations of Engels et al. (1995), showing that colonies of Scaptotrigona postica , a closely-related species, are able to maintain the temperature of the brood area around 40 °C when exposed to high temper-atures (close to 44 °C). Given the scattered, but suggestive, evidence for active cooling of the nest environment in stingless bees, we performed an experimental study to test the hypothesis that S. depilis has the ability to actively cool the nest environment. We addressed two main questions: First, to what extent is S. depilis able to cool the nest when exposed to high temperatures? Second, are there behavioural mechanisms for nest cooling? To answer the second question, we analysed two candidate behaviours, wing fanning and water collection. We also investigated the effects of temperature on the pupae survival and development time.

2. MATERIAL AND METHODS

2.1. Study species and study site

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kept outdoors, unshaded, in white wooden boxes cov-ered by tiles under ambient conditions of light and temperature (Fig.S1A). Colonies usually contain sev-eral thousand workers and one, singly mated queen (Paxton et al.2003).

2.2. Experimental setup

a) Ability to cool the nest

To investigate the bees’ ability to cool the nest during high temperature conditions, temperature probes (15 length×5 diameter mm; SENSIRION, model SHT75; precision: 0.3 °C) were introduced into the hives through lateral holes (15-mm diam-eter). In each colony, the temperature of the brood area (TBROOD) was monitored (Fig.S1A). The data

were collected and stored at intervals of 5 min and 24 h a day. Five colonies were monitored. Another empty wooden box with the same characteristics as the one used for keeping the colonies was moni-tored by a temperature probe (held by a piece of wood that prevented contact with the floor of the box) and placed in the same conditions as the experimental hives. This box, lacking bees but under the same environmental conditions, served as a control for the conditions the bee colonies were submitted to (TCONTROL). The ambient

tem-perature was also recorded using a sensor placed in the shade, close to the hives (TAMB). All boxes

were exposed to the sunlight, which produced high temperature conditions (>40 °C in the TCONTROL

during the hottest time of the day), and conditions were similar in all hives. The data used in the analysis comprised 3 days in which the tempera-ture conditions were hot enough.

b) Water collection behaviour

To test whether water collection behaviour is formed when the temperature increases, we per-formed further observations on two of the colonies mentioned above. The colonies had a transparent plastic tube attached to the entrance (15-cm length×2.5-cm diameter), which had a small win-dow (3×2 cm) that allowed the capture of foragers as they returned to the nest (Fig.S1C). Every hour, (from 08:00 to 17:00 hours) three foragers with neither pollen nor resin in their corbiculae were collected from each colony. These foragers were anaesthetized with CO2, and by pressing their

abdomens, their crop content was collected with a graduated capillary tube (Fig.S1D). The sugar c o n t e nt o f t h e i r c r o p c o n t e n t w a s t h e n analysed using a digital refractometer (Krüss Optronic—Alemanha—DR201-95). Only the bees that contained at least 7 μL of liquid were analysed. This is the minimum sample volume required by our refractometer for accurate mea-surement of the solution’s concentration. Concen-trations with less than 2 % of sugar were consid-ered to be“water” (Leonhardt et al.2007).

c) Fanning behaviour

To determine whether wing fanning behaviour oc-curs as temperature increases, we monitored three colonies as described above. A transparent plastic tube was attached to the entrance (12 cm length×2.5 cm diameter) to extend the entrance tube (where the workers position themselves to perform fanning behaviours) and to allow counting of individual workers fanning their wings. This behaviour is very characteristic, with the workers standing on the substrate (in this case, the plastic tube), forming a queue, with the posterior legs stretched, and fanning their wings (Fig.S1Band

S1E).

Six bioassays were conducted in which the tem-perature of the boxes was gradually increased, using one 15 Watts incandescent lamp positioned under the hives (2 cm below the box). After 45 min, the lamps were turned off. After that, the number of workers fanning in the plastic tube was recorded every 5 min, until there were no more bees fanning. The bioassays were performed from 11:00 to 15:00 hours. Temperature data were sam-pled as described earlier.

d) Effect of temperature on pupae mortality and de-velopment time

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from five different colonies in each treatment. To ascertain the age of the pupae, we uncapped 60 brood cells that contained larvae in pre-pupae stages, which were adjacent to the pupae. As in this species, the brood comb is built as a disc, with new cells being added from the centre to the margins, and the colo-nies produce more than 200 cells per day, almost all the pre-pupae which neighbour pu-pae pupated the next day. This day was con-sidered day zero (Fig. S2). As we opened 60 cells, we removed the necessary amount of individuals to reach 50 female pupae in each comb. The removal was performed when the pupae reached the stage of black eyes, which allowed us to remove male pupae. The brood combs were placed inside a petri dish con-taining saturated solution of water and salt (NaCl) to maintain the humidity close to 75 %, which has previously been showed to be the ideal condition for in vitro queen rearing on this species (Menezes et al. 2013).

2.3. Data analysis

All analyses were performed in R 2.15.0 (R Devel-opment Core Team 2011). Cooling of the nest was considered to occur if the brood temperature (TBROOD) was lower than the control temperature

(TCONTROL). The temperatures in this category

(TBROOD<TCONTROL) were grouped into periods

(cooling periods ), during which the cooling happened. We described the temperature differences during this period and measured the duration of the cooling period. The probability that a forager bee was loaded with nectar and water (0 and 1, respectively) was modelled as a function of the nest temperature using a GLM with a binomial distribution, since the response variable followed a binomial distribution. We performed diag-nostic analyses of the model, and found that the residual deviance did not indicate overdispersion. To test wheth-er wing fanning was triggwheth-ered and increased as the temperature inside the nest increased, we performed a linear regression with the number of fanning bees as a function of brood temperature and colony (Zuur2009). All tests were two-tailed tests with a significance level set toα=0.05. We used an ANOVA to test for differ-ences in mortality of pupae reared at different

temperatures.. The relationship between temperature and development time was analysed using a Kruskal-Wallis one-way ANOVA on Ranks test (Zuur2009).

3. RESULTS

a) Nest cooling

“Cooling periods” (when TBROOD was lower than TCONTROL) lasted about 5 h (306.6±83.9 min), from approximately 10:00–14:00 hours. This was the time of highest environmental temperature (Figure1).

These results suggest that there is a mech-anism for cooling the nest during warm periods, while during the rest of the day, the brood was maintained at a higher tem-perature than the control (Figure 1; TableS1). The peaks of maximum differ-ences between TCONTROL and TBROOD reached 1.6(±0.2)°C (averaged over all the colonies studied and all sampling days). The average maximum cooling achieved by the colonies was 2.5 (±0.28)°C for only one of the days sam-pled. The TAMB was considerably lower than the TCONTROLduring the cooling pe-riods (Figure1).

b) Water collection

About 20 % of the foragers (47 of 231) in both colonies collected water (TableS2). Wa-ter collection started when the TBROODwas about 29 °C. The binomial GLM analyses were significant and showed that the proba-bility of a forager collecting water increased significantly with the TBROOD (slope=0.55 ±0.09, P <0.001, Figure2).

c) Fanning behaviour

The number of fanning bees was positively correlated with the brood temperature (adjust-ed R2=0.48, F =158.8, P <0.001): the higher the temperature, the more bees were observed fanning (Figure3).

d) Effect of temperature on pupae mortality and development time

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extreme temperatures, 22 and 38 °C, showed high levels of mortality, 100 % and 96.6 %, respectively (Figure 4; Table S4) (one-way ANOVA: F =519.43; P <0.001–Holm-Sidak: P <0.05).

Development time showed significant varia-tion among treatments (H =675.1; P <0.001). Non-significantly different values of devel-opment time were found only between 34 and 38 °C (Figure4; TableS4). There was a

T. control T. ambient T. brood 20 25 30 35 0 12 0 12 0 12 0 Time (hours)

Figure 1. Temperature of the brood area (TBROOD—open dots showing mean and bars showing standard

deviation) from the five colonies monitored, the control box (TCONTROLthick line ), and ambient (TAMB thin line )

during three non-consecutive days. The cooling periods (when TCONTROLis higher than average TBROOD)are

highlighted (grey areas ).

25 30 35 40 0.0 0.2 0.4 0.6 0 .8 1.0 Brood temperature (°C) W

ater collection probability

Figure 2. The relationship between water collection and brood temperature. The fitted values (solid line ) represent the probability of a forager collecting water relative to the brood temperature (TBROOD) obtained by the binomial

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30 32 34 36 0 5 10 15 20 25 30 35 Brood temperature (°C) Number of f anning bees Slope = 3.9739 Adj R² = 0.48, p < 0.001

Figure 3. Scatterplot showing the effect of brood temperature on the number of fanning bees. The line represents the best-fit line and was drawn based on the parameter estimates obtained from the linear regressions (adjusted R2=0.48, F =158.8, P <0.001). a b c c 15 20 25 30 35 40 Time (da ys) a b b b a 0 25 50 75 100 22 26 30 34 38 Sur viv al (%)

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strong negative correlation between incuba-tion temperature and development time (spearman rank correlation=−0.95). The mean time of development halved from 26 to 34 °C.

4. DISCUSSION

Our results show that S. depilis brood nest temperature is colder than the empty control box during the hottest part of the day. Although the difference between TBROODand TCONTROLmight seem to show only moderate cooling, it has been suggested that even small increases in temperature during very hot periods can be highly damaging to brood (Undurraga and Stephen1980; Mardan and Kevan2002; Tautz et al.2003), as our data also showed for extreme temperatures (“Results” (d)).

This damage is thought to mostly occur due to disruption of cellular physiological processes. Bees and most other animals seem to be much more robust to cold temperatures (Angilletta2009).

Although the data we collected indicate that active mechanisms of fanning and water collec-tion could be related to nest temperature decrease, we cannot rule out the possibility that nest struc-tures and simple presence of the bees are not influencing the nest temperature oscillations, since they were not present in the empty control box. The brood, adult bees, wax structures, honey and pollen pots could result in thermal inertia, decreasing the rate of temperature rise in nests. However, both the adult workers and the brood produce metabolic heat (Roubik and Peralta1983; Jones and Oldroyd2007), which could have the opposite effect, increasing the nest temperature and make active cooling more difficult. Therefore, while further investigations are necessary to fully understand the mechanisms that decrease nest temperature in stingless bees, our data strongly suggest that active behavioural efforts play a role in nest thermoregulation. It is noteworthy that TAMBis lower than TCONTROLduring the hottest period of the day, highlighting the necessity of a control box when studying the thermoregulation of social insects that nest in cavities. Such a con-trol is absent in all other studies on nest cooling by social insects.

Our results suggest that S. depilis exhibit at least two active mechanisms which may play a role in the cooling of the nest: (i) fanning behav-iour and (ii) water collection. Both behavbehav-iours are present in the behavioural repertoire of the re-sponse of honey bees to high temperatures de-scribed by Lindauer (1954).

Water collection for cooling purposes has up until now only been described in the Apini tribe and in several species of social wasps (Jones and Oldroyd 2007). Here, we provide the first evi-dence of water collection for the purpose of nest cooling in stingless bees. In Apini and wasps, the mechanism of cooling seems to be similar: the water is deposited in small droplets on the sur-faces of the nest, or the surface is licked, and as the water evaporates, it lowers the temperature of the nest (Lindauer 1954; Simpson 1961; Nicolson

2009). Despite previous observations of water collection in Meliponini, this has not been linked to the cooling of the nest, but to nutritional needs (hydration and minerals). Such a link was proba-bly not previously made because the deposition of water droplets or licking behaviour has not been observed before (Jones and Oldroyd2007). As in honeybees, our results show that high ambient temperatures are linked to water collection (Lindauer 1954), but the mechanism underlying the process of cooling in stingless bees is still unknown. It is likely that the water is deposited on internal nest surfaces or evaporated through licking by the workers, but this awaits investiga-tion. There is the possibility of the adults using this water to decrease their own body temperature, as has been described in honeybees (Heinrich

1979; Cooper et al.1985). This would nonetheless be a way of decreasing the nest temperature. Our results suggest a causal link between nest temper-ature and water collection behaviour, rather than a coincidental occurrence of water collection at the time of highest ambient temperature, because stingless bee foraging activity for other resources (nectar, pollen or resin) normally decreases during extremely high temperatures (Silva et al. 2011; Hilário et al. 2012; Figueiredo-Mecca et al.

2013). The same phenomenon was observed in large bees, such as Bombus terrestris (Kwon and Saeed2003). Water foragers may be able to toler-ate foraging at higher temperatures by using

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evaporative cooling from their bodies (Prange

1996; Pereboom and Biesmeijer2003).

We also confirm previous suggestions (Engels et al. 1995; Nogueira-Neto 1997; Jones and Oldroyd 2007) that the wing fanning behaviour is indeed a colony-level response to an increase in nest temperature and, therefore, is likely to be performed to cool the nest. The higher the tem-perature inside the nest, the more bees start to fan their wings in the entrance tube. We also observed that this behaviour occurs inside the nest, in re-gions not connected to the entrance. It is important to note that this behaviour is also a response to high levels of CO2inside the nest in other social bees, and is used to improve gas exchange in the nest (Simpson 1961; Moritz and Crewe 1988; Weidenmuller et al. 2002). Indeed, high CO2 levels could also be the ultimate cause of the ventilation, since increased metabolic rates during high temperature periods could increase CO2 levels. This variable should be included in further studies to conclusively determine whether fanning is a response to overheating per se, or to an in-crease in CO2 concentrations caused by overheating. Lastly, another possibility is that the fanning behaviour could have a role of decreasing humidity inside the nest by facilitating the air exchange between the brood area and the outside. Such an integration between ventilation and evap-orative cooling would be particularly important when the ambient air temperature exceeds the upper critical temperature. When this limit is reached, non-evaporative heat loss is progressive-ly reduced because the air temperature is higher than the temperature inside the nest, causing sim-ple ventilation itself to be ineffective. This hy-pothesis also remains to be tested.

The effects of temperature on brood develop-ment time varied greatly between intermediate temperature treatments (26, 30 and 34 °C; Fig-ure4). However, while we found a small positive correlation between an increase in temperature and pupae survival, this correlation was not sig-nificant. However, the extreme temperatures (22 and 38 °C) increased brood mortality (Figure4). Our data showed that the TBROODwas on average 30.5±2.9 °C (mean±s.d.) over the whole day and 34±1.4 °C (mean±s.d.) during the cooling periods. These temperatures are most similar to the two

temperature treatments which showed the fastest brood development and highest survival (30 and 34 °C). Extreme temperatures were found to be very damaging to the brood, highlighting the im-portance of temperature control. A change of even 1 °C could make the difference between survival or death. However, it is important to note that these temperatures were held constant in our de-velopment bioassay, but temperatures are not con-stant in nature. The impact of short episodes of extremes temperatures on brood development would benefit from investigation. Even 1 h of exposure to temperatures of 50 °C caused a mor-tality of 100 % in pupae and pre-pupae of the solitary bee Megachile rotundata (Hymenoptera, Megachilidae), while an exposure of several hours to 45 °C did not significantly increased mortality (Undurraga and Stephen1980). The development time of Osmia bicornis (Hymenoptera, Megachilidae) brood was also decreased when the temperatures fluctuated, as compared to con-ditions of constant temperatures based on the av-erage of the fluctuations (Radmacher and Strohm

2011).

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hypothesis, since many different thermoregulato-ry strategies are present among closely related species.

Our results suggest that S. depilis have adap-tations similar to honeybees for coping with high temperatures. This likely represents an incident of convergent evolution, since these adaptations de-pends on a social context, and the origin of euso-ciality in both groups is considered to have oc-curred independently (Michener1974). Stingless bees do not thermoregulate their nest as precisely as honeybees do. However, our results suggest that S. depilis brood is more resistant to tempera-ture variation during their development. We sug-gested that stingless bees’ strategy would be to increase the thermal resistance—coupled with proper nest site selection. In other words, increas-ing capacity to tolerate higher temperature varia-tion, expanding the range of thermal tolerance by sacrificing higher performances at optimal tem-peratures, results in longer development time (Huey and Hertz1984; Angilletta2009).

ACKNOWLEDGMENTS

We thank Rodrigo Augusto Santinelo Pereira and Christoph Grüter for their help with the statistical anal-ysis. We are especially grateful to Christoph Grüter, Francisca Segers and Tommer Czaczkes for their sug-gestions that improved the manuscript. We would also like to thank the three anonymous referees and the journal editor, who provided valuable comments that improved the manuscript. We thank Capes and Fapesp for financial support (AVN 2012/11144-0; CM 07/ 50218-1; VLIF 04/15801-0).

Réponses, sur le plan du comportement et du d é v e l o p p e m e n t , d' u n e a b e i l l e s a n s a i g u i l l o n ( Scaptotrigona depilis ) à une surchauffe du nid Thermorégulation sociale / refroidissement du nid / approvisionnement en eau / Meliponini / Apidae Verhaltens- und entwicklungsspzifische Reaktionen einer stachellosen Biene ( Scaptotrigona depilis ) auf eine Überhitzung des Nestes

soziale Thermoregulation / Kühlen / Wassersammeln / Meliponini / Apidae

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