Behavioural and developmental responses of a stingless

bee (Scaptotrigona depilis) to nest overheating

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

To cite this version:

Ayrton Vollet-Neto, Cristiano Menezes, Vera Lucia Imperatriz-Fonseca. Behavioural and develop-
mental responses of a stingless bee (Scaptotrigona depilis) to nest overheating. Apidologie, Springer
Verlag, 2015, 46 (4), pp.455-464. �10.1007/s13592-014-0338-6�. �hal-01284459�

HAL Id: hal-01284459

https://hal.archives-ouvertes.fr/hal-01284459
Submitted on 7 Mar 2016

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est

archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents
entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non,
lished or not. The documents may come from émanant des établissements d’enseignement et de
teaching and research institutions in France or recherche français ou étrangers, des laboratoires
abroad, or from public or private research centers. publics ou privés.
Apidologie (2015) 46:455–464 Original article
* INRA, DIB and Springer-Verlag France, 2014
DOI: 10.1007/s13592-014-0338-6

Behavioural and developmental responses of a stingless bee

(Scaptotrigona depilis ) to nest overheating

Ayrton VOLLET-NETO1 , Cristiano MENEZES2 , Vera Lucia IMPERATRIZ-FONSECA3

1
Departamento 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
2
Embrapa Amazônia Oriental, Tv. Dr. Enéas Pinheiro, s/n., Belém, Pará, Brazil
3
Universidade 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 adult bees especially to foraging activities are af-

fected even by 2 °C of difference between temper-
Social bees are able to control the nest environ- atures they were raised (Tautz et al. 2003). More-
ment to allow optimal performance of the adults as over, mortality and malformation increase when
well as optimal development of the brood (Wilson brood is reared outside of a very narrow range of
1971; Jones and Oldroyd 2007). In particular, so- optimal temperatures (Himmer 1927; Heinrich
cial bees are sensitive to, and invest considerable 1993; Mardan and Kevan 2002)
effort in controlling, the temperature within the Nest temperature can be increased through
nest. Honeybees (Apis mellifera ) are very effective metabolic heating generated by the shivering of
at controlling their internal nest temperature. The flight muscles in bumblebees (Hymenoptera,
workers can perform quite well over a wide range Apidae, Bombini) and honeybees (Hymenoptera,
of temperatures, but the brood is very sensitive to Apidae, Apini) (Jones and Oldroyd 2007). These
temperature fluctuations. The cognition ability of 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
Electronic supplementary material The online version of
this article (doi:10.1007/s13592-014-0338-6) contains 36 °C, even when the external temperatures are
supplementary material, which is available to authorized higher than 40 °C (Heinrich 1993). To accomplish
users. this, workers fan their wings to create an air flow
Corresponding author: A. Vollet-Neto, between the inside and the outside of the nest.
[email protected] This behaviour is combined with water collection,
Manuscript editor: Peter Rosenkranz where small droplets of water are deposited on
456 A. Vollet-Neto et al.

surfaces on the inside of the nest. This reduces the that it plays a role in the cooling of the nest
temperature of the nest through evaporative because the deposition of water droplets was nev-
cooling (Lindauer 1954). In Bombus , only fan- er observed inside colonies and because cavity
ning behaviour has been reported and is correlated nesting is considered to provide a thermally stable
with an increase in nest temperature (Jones and environment (Engels et al. 1995). On the other
Oldroyd 2007). hand, Macías-Macías et al. (2011), working with
Stingless bees (Hymenoptera, Apidae, individual workers of Melipona colimana , found
Meliponini) are the largest and most diverse group that high temperatures led to an increase in water
of highly eusocial bees (Michener 2000). They are consumption, and that workers regurgitated the
restricted to tropical and subtropical habitats and water on the bottom of the boxes. The authors
are, therefore, often exposed to high temperatures. suggested that this individual behaviour could be
However, there is no evidence that they perform used at the colony level to decrease the tempera-
behaviours to actively cool the nest (Jones and ture of the nest.
Oldroyd 2007). Research shows that the internal In preliminary observations, we noted that
nest temperature differs from ambient tempera- Scaptotrigona depilis can maintain relatively sta-
ture, but most authors attribute this to the behav- ble temperature inside the nest during periods of
iour of nesting in insulated cavities and assume extreme heat. This is in line with the observations
that this is the main way by which stingless bees of Engels et al. (1995), showing that colonies of
avoid nest temperature rising to damaging levels Scaptotrigona postica , a closely-related species,
during hot periods (Engels et al. 1995; Nogueira- are able to maintain the temperature of the brood
Neto 1997; Jones and Oldroyd 2007). On the area around 40 °C when exposed to high temper-
other hand, wing fanning has been described in atures (close to 44 °C). Given the scattered, but
several species in this group, leading some re- suggestive, evidence for active cooling of the nest
searchers to suggest that this might be a cooling environment in stingless bees, we performed an
behaviour (Nogueira-Neto 1948; Macías-Macías experimental study to test the hypothesis that
et al. 2011). However, this hypothesis has yet to S. depilis has the ability to actively cool the nest
be tested. Engels et al. (1995), working with environment. We addressed two main questions:
Scaptotrigona postica , observed that colonies First, to what extent is S. depilis able to cool the
experiencing high temperatures had elevated nest when exposed to high temperatures? Second,
numbers of bees performing wing fanning. are there behavioural mechanisms for nest
Macías-Macías et al. (2011) demonstrated that cooling? To answer the second question, we
workers of Melipona colimana kept individually analysed two candidate behaviours, wing fanning
in boxes inside incubators perform wing fanning and water collection. We also investigated the
behaviour when exposed to temperatures of effects of temperature on the pupae survival and
40 °C. However, Moritz and Crewe (1988) point- development time.
ed out that wing fanning plays a role in air circu-
lation inside the nest, regulating the CO2 and O2 2. MATERIAL AND METHODS
levels inside the nest cavities of the ground
nesting species Trigona denotii . Nogueira-Neto 2.1. Study species and study site
(1948) also reports the occurrence of fanning be-
haviour in stingless bee colonies during cold win- The study was performed on the Ribeirão Preto
ter days, suggesting that this behaviour is related campus of São Paulo University, SP, Brazil, during
to gas exchange, rather than temperature summer time (from December 2011 to March
regulation. 2012—maximum temperature of 40 °C), where
There are a few reports of water collection in Scaptotrigona depilis is a common stingless bee spe-
stingless bee species (Nogueira-Neto 1997; cies. This species was chosen because many aspects of
Macías-Macías et al. 2011). However, the authors its biology have been described in the literature, includ-
associate this behaviour with individual ingestion ing some responses to high temperature, such as wing
of water and minerals and reject the hypothesis fanning behaviour (Engels et al. 1995). Colonies were
 Response of a stingless bee to nest overheating 457

kept outdoors, unshaded, in white wooden boxes cov- abdomens, their crop content was collected with
ered by tiles under ambient conditions of light and a graduated capillary tube (Fig. S1D). The sugar
temperature (Fig. S1A). Colonies usually contain sev- content of their crop content was then
eral thousand workers and one, singly mated queen analysed using a digital refractometer (Krüss
(Paxton et al. 2003). Optronic—Alemanha—DR201-95). Only the bees
that contained at least 7 μL of liquid were
analysed. This is the minimum sample volume
2.2. Experimental setup required by our refractometer for accurate mea-
surement of the solution’s concentration. Concen-
a) Ability to cool the nest trations with less than 2 % of sugar were consid-
To investigate the bees’ ability to cool the nest ered to be “water” (Leonhardt et al. 2007).
during high temperature conditions, temperature c) Fanning behaviour
probes (15 length×5 diameter mm; SENSIRION, To determine whether wing fanning behaviour oc-
model SHT75; precision: 0.3 °C) were introduced curs as temperature increases, we monitored three
into the hives through lateral holes (15-mm diam- colonies as described above. A transparent plastic
eter). In each colony, the temperature of the brood tube was attached to the entrance (12 cm
area (T BROOD) was monitored (Fig. S1A). The data length×2.5 cm diameter) to extend the entrance
were collected and stored at intervals of 5 min and tube (where the workers position themselves to
24 h a day. Five colonies were monitored. Another perform fanning behaviours) and to allow counting
empty wooden box with the same characteristics as of individual workers fanning their wings. This
the one used for keeping the colonies was moni- behaviour is very characteristic, with the workers
tored by a temperature probe (held by a piece of standing on the substrate (in this case, the plastic
wood that prevented contact with the floor of the tube), forming a queue, with the posterior legs
box) and placed in the same conditions as the stretched, and fanning their wings (Fig. S1B and
experimental hives. This box, lacking bees but S1E).
under the same environmental conditions, served Six bioassays were conducted in which the tem-
as a control for the conditions the bee colonies perature of the boxes was gradually increased,
were submitted to (T CONTROL). The ambient tem- using one 15 Watts incandescent lamp positioned
perature was also recorded using a sensor placed in under the hives (2 cm below the box). After
the shade, close to the hives (T AMB). All boxes 45 min, the lamps were turned off. After that, the
were exposed to the sunlight, which produced high number of workers fanning in the plastic tube was
temperature conditions (>40 °C in the T CONTROL recorded every 5 min, until there were no more
during the hottest time of the day), and conditions bees fanning. The bioassays were performed from
were similar in all hives. The data used in the 11:00 to 15:00 hours. Temperature data were sam-
analysis comprised 3 days in which the tempera- pled as described earlier.
ture conditions were hot enough. d) Effect of temperature on pupae mortality and de-
b) Water collection behaviour velopment time
To test whether water collection behaviour is per- The bioassay consisted of incubating brood
formed when the temperature increases, we per- combs containing pupae at five different tem-
formed further observations on two of the colonies peratures: 22, 26, 30, 34 and 38 °C (BOD
mentioned above. The colonies had a transparent incubator). Towards the end of normal pupal
plastic tube attached to the entrance (15-cm developmental time, we observed the brood
length×2.5-cm diameter), which had a small win- combs daily to check for emergence of
dow (3×2 cm) that allowed the capture of foragers adults. We noted individual mortality (pupae
as they returned to the nest (Fig. S1C). Every hour, were considered dead if they failed to emerge
(from 08:00 to 17:00 hours) three foragers with or other characteristics of death, such as fun-
neither pollen nor resin in their corbiculae were gal growth, were observed) and, for the sur-
collected from each colony. These foragers were viving pupae, the time until spontaneous
anaesthetized with CO2, and by pressing their emergence of the bees. We used 50 pupae
458 A. Vollet-Neto et al.

from five different colonies in each treatment. temperatures.. The relationship between temperature
To ascertain the age of the pupae, we and development time was analysed using a Kruskal-
uncapped 60 brood cells that contained larvae Wallis one-way ANOVA on Ranks test (Zuur 2009).
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 3. RESULTS
from the centre to the margins, and the colo-
nies produce more than 200 cells per day, a) Nest cooling
almost all the pre-pupae which neighbour pu- “Cooling periods” (when T BROOD was
pae pupated the next day. This day was con- lower than T CONTROL) lasted about 5 h
sidered day zero (Fig. S2). As we opened 60 (306.6±83.9 min), from approximately
cells, we removed the necessary amount of 10:00–14:00 hours. This was the time of
individuals to reach 50 female pupae in each highest environmental temperature
comb. The removal was performed when the (Figure 1).
pupae reached the stage of black eyes, which These results suggest that there is a mech-
allowed us to remove male pupae. The brood anism for cooling the nest during warm
combs were placed inside a petri dish con- periods, while during the rest of the day,
taining saturated solution of water and salt the brood was maintained at a higher tem-
(NaCl) to maintain the humidity close to perature than the control (Figure 1;
75 %, which has previously been showed to Table S1). The peaks of maximum differ-
be the ideal condition for in vitro queen ences between T CONTROL and T BROOD
rearing on this species (Menezes et al. 2013). reached 1.6(±0.2)°C (averaged over all
the colonies studied and all sampling
days). The average maximum cooling
2.3. Data analysis achieved by the colonies was 2.5
(±0.28)°C for only one of the days sam-
All analyses were performed in R 2.15.0 (R Devel- pled. The T AMB was considerably lower
opment Core Team 2011). Cooling of the nest was than the T CONTROL during the cooling pe-
considered to occur if the brood temperature riods (Figure 1).
(T BROOD) was lower than the control temperature b) Water collection
(T CONTROL ). The temperatures in this category About 20 % of the foragers (47 of 231) in
(T BROOD<T CONTROL ) were grouped into periods both colonies collected water (Table S2). Wa-
(cooling periods ), during which the cooling happened. ter collection started when the T BROOD was
We described the temperature differences during this about 29 °C. The binomial GLM analyses
period and measured the duration of the cooling period. were significant and showed that the proba-
The probability that a forager bee was loaded with bility of a forager collecting water increased
nectar and water (0 and 1, respectively) was modelled significantly with the T BROOD (slope=0.55
as a function of the nest temperature using a GLM with ±0.09, P <0.001, Figure 2).
a binomial distribution, since the response variable c) Fanning behaviour
followed a binomial distribution. We performed diag- The number of fanning bees was positively
nostic analyses of the model, and found that the residual correlated with the brood temperature (adjust-
deviance did not indicate overdispersion. To test wheth- ed R 2=0.48, F =158.8, P <0.001): the higher
er wing fanning was triggered and increased as the the temperature, the more bees were observed
temperature inside the nest increased, we performed a fanning (Figure 3).
linear regression with the number of fanning bees as a d) Effect of temperature on pupae mortality and
function of brood temperature and colony (Zuur 2009). development time
All tests were two-tailed tests with a significance level Mortality rates were lowest at 34 °C (1.2 %);
set to α=0.05. We used an ANOVA to test for differ- however, there was no significant difference
ences in mortality of pupae reared at different in mortality between 26, 30 and 34 °C. Both
 Response of a stingless bee to nest overheating 459

35

30

25

T. ambient
T. control
20 T. brood

0 12 0 12 0 12 0
Time (hours)

Figure 1. Temperature of the brood area (T BROOD—open dots showing mean and bars showing standard
deviation) from the five colonies monitored, the control box (T CONTROL thick line ), and ambient (TAMB thin line )
during three non-consecutive days. The cooling periods (when T CONTROL is higher than average T BROOD) are
highlighted (grey areas ).

extreme temperatures, 22 and 38 °C, showed Development time showed significant varia-
high levels of mortality, 100 % and 96.6 %, tion among treatments (H =675.1; P <0.001).
respectively (Figure 4; Table S4) (one-way Non-significantly different values of devel-
ANOVA: F =519.43; P <0.001–Holm-Sidak: opment time were found only between 34
P <0.05). and 38 °C (Figure 4; Table S4). There was a
1.0
0.8
Water collection probability
0.6
0.4
0.2
0.0

25 30 35 40
Brood temperature (°C)

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 (T BROOD) obtained by the binomial
GLM analysis (slope=0.55±0.09, P <0.001). The dots are the observed values (1 represent water collection).
460 A. Vollet-Neto et al.

35
Slope = 3.9739
Adj R² = 0.48, p < 0.001

30
Number of fanning bees
25
20
15
10
5
0

30 32 34 36

Brood temperature (°C)

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 R 2=0.48,
F =158.8, P <0.001).
Time (days)

40 a
35
30
25 b
20 c c
15

a b b b a
100
Survival (%)

75

50

25

0
22 26 30 34 38

Figure 4. Survival rate (bars ) and development time (boxplots ) of S. depilis pupae incubated at five different
temperature. Bars , grey sections represent the percentage of survival, while the black sections represent percentage
mortality. Boxplots , median (thick line ), upper and lower quartiles (upper and lower limits of the boxes), 95 % of data
distribution (stems ) and the values out of the 95 % data distribution (ouliers ) are represented. Different superscribed
letters indicate groups statistically different (ANOVA and Kruskal-Wallis associate with Dunn’s test, P <0.001).
 Response of a stingless bee to nest overheating 461

strong negative correlation between incuba- Our results suggest that S. depilis exhibit at
tion temperature and development time least two active mechanisms which may play a
(spearman rank correlation=−0.95). The role in the cooling of the nest: (i) fanning behav-
mean time of development halved from 26 iour and (ii) water collection. Both behaviours are
to 34 °C. present in the behavioural repertoire of the re-
sponse of honey bees to high temperatures de-
scribed by Lindauer (1954).
4. DISCUSSION Water collection for cooling purposes has up
until now only been described in the Apini tribe
Our results show that S. depilis brood nest and in several species of social wasps (Jones and
temperature is colder than the empty control box Oldroyd 2007). Here, we provide the first evi-
during the hottest part of the day. Although the dence of water collection for the purpose of nest
difference between T BROOD and T CONTROL might cooling in stingless bees. In Apini and wasps, the
seem to show only moderate cooling, it has been mechanism of cooling seems to be similar: the
suggested that even small increases in temperature water is deposited in small droplets on the sur-
during very hot periods can be highly damaging to faces of the nest, or the surface is licked, and as the
brood (Undurraga and Stephen 1980; Mardan and water evaporates, it lowers the temperature of the
Kevan 2002; Tautz et al. 2003), as our data also nest (Lindauer 1954; Simpson 1961; Nicolson
showed for extreme temperatures (“Results” (d)). 2009). Despite previous observations of water
This damage is thought to mostly occur due to collection in Meliponini, this has not been linked
disruption of cellular physiological processes. Bees to the cooling of the nest, but to nutritional needs
and most other animals seem to be much more (hydration and minerals). Such a link was proba-
robust to cold temperatures (Angilletta 2009). bly not previously made because the deposition of
Although the data we collected indicate that water droplets or licking behaviour has not been
active mechanisms of fanning and water collec- observed before (Jones and Oldroyd 2007). As in
tion could be related to nest temperature decrease, honeybees, our results show that high ambient
we cannot rule out the possibility that nest struc- temperatures are linked to water collection
tures and simple presence of the bees are not (Lindauer 1954), but the mechanism underlying
influencing the nest temperature oscillations, the process of cooling in stingless bees is still
since they were not present in the empty control unknown. It is likely that the water is deposited
box. The brood, adult bees, wax structures, honey on internal nest surfaces or evaporated through
and pollen pots could result in thermal inertia, licking by the workers, but this awaits investiga-
decreasing the rate of temperature rise in nests. tion. There is the possibility of the adults using
However, both the adult workers and the brood this water to decrease their own body temperature,
produce metabolic heat (Roubik and Peralta 1983; as has been described in honeybees (Heinrich
Jones and Oldroyd 2007), which could have the 1979; Cooper et al. 1985). This would nonetheless
opposite effect, increasing the nest temperature be a way of decreasing the nest temperature. Our
and make active cooling more difficult. Therefore, results suggest a causal link between nest temper-
while further investigations are necessary to fully ature and water collection behaviour, rather than a
understand the mechanisms that decrease nest coincidental occurrence of water collection at the
temperature in stingless bees, our data strongly time of highest ambient temperature, because
suggest that active behavioural efforts play a role stingless bee foraging activity for other resources
in nest thermoregulation. It is noteworthy that (nectar, pollen or resin) normally decreases during
T AMB is lower than T CONTROL during the hottest extremely high temperatures (Silva et al. 2011;
period of the day, highlighting the necessity of a Hilário et al. 2012; Figueiredo-Mecca et al.
control box when studying the thermoregulation 2013). The same phenomenon was observed in
of social insects that nest in cavities. Such a con- large bees, such as Bombus terrestris (Kwon and
trol is absent in all other studies on nest cooling by Saeed 2003). Water foragers may be able to toler-
social insects. ate foraging at higher temperatures by using
462 A. Vollet-Neto et al.

evaporative cooling from their bodies (Prange temperature treatments which showed the fastest
1996; Pereboom and Biesmeijer 2003). brood development and highest survival (30 and
We also confirm previous suggestions (Engels 34 °C). Extreme temperatures were found to be
et al. 1995; Nogueira-Neto 1997; Jones and very damaging to the brood, highlighting the im-
Oldroyd 2007) that the wing fanning behaviour portance of temperature control. A change of even
is indeed a colony-level response to an increase in 1 °C could make the difference between survival
nest temperature and, therefore, is likely to be or death. However, it is important to note that
performed to cool the nest. The higher the tem- these temperatures were held constant in our de-
perature inside the nest, the more bees start to fan velopment bioassay, but temperatures are not con-
their wings in the entrance tube. We also observed stant in nature. The impact of short episodes of
that this behaviour occurs inside the nest, in re- extremes temperatures on brood development
gions not connected to the entrance. It is important would benefit from investigation. Even 1 h of
to note that this behaviour is also a response to exposure to temperatures of 50 °C caused a mor-
high levels of CO2 inside the nest in other social tality of 100 % in pupae and pre-pupae of the
bees, and is used to improve gas exchange in the solitary bee Megachile rotundata (Hymenoptera,
nest (Simpson 1961; Moritz and Crewe 1988; Megachilidae), while an exposure of several hours
Weidenmuller et al. 2002). Indeed, high CO2 to 45 °C did not significantly increased mortality
levels could also be the ultimate cause of the (Undurraga and Stephen 1980). The development
ventilation, since increased metabolic rates during time of Osmia bicornis (Hymenoptera,
high temperature periods could increase CO2 Megachilidae) brood was also decreased when
levels. This variable should be included in further the temperatures fluctuated, as compared to con-
studies to conclusively determine whether fanning ditions of constant temperatures based on the av-
is a response to overheating per se, or to an in- erage of the fluctuations (Radmacher and Strohm
crease in CO 2 concentrations caused by 2011).
overheating. Lastly, another possibility is that the In honeybees, a variation of 5 to 6 °C from the
fanning behaviour could have a role of decreasing 33 °C optimal temperature for brood development
humidity inside the nest by facilitating the air greatly increases brood mortality and
exchange between the brood area and the outside. malformations (Himmer 1927; Mardan and
Such an integration between ventilation and evap- Kevan 2002), while in S. depilis , mortality does
orative cooling would be particularly important not change over a range of at least 8 °C. However,
when the ambient air temperature exceeds the the development of S. depilis is considerably
upper critical temperature. When this limit is slower than that of A. mellifera . The minimal
reached, non-evaporative heat loss is progressive- development time from pupae to emergence of
ly reduced because the air temperature is higher S. depilis is around 15.7 and 16.2 days, at 38
than the temperature inside the nest, causing sim- and 34 °C, respectively. In honey bees, the closed
ple ventilation itself to be ineffective. This hy- cell phase (prepupal and pupal) development time
pothesis also remains to be tested. is around 9.5 to 12 days (Michener 1974). We
The effects of temperature on brood develop- suggest that the precise temperature control
ment time varied greatly between intermediate achieved by honeybees when compared to
temperature treatments (26, 30 and 34 °C; Fig- S. depilis has led to adaptation to a narrow range
ure 4). However, while we found a small positive of temperatures. The stingless bees species which
correlation between an increase in temperature are poorer thermoregulators would be better
and pupae survival, this correlation was not sig- adapted to a wider range of temperatures, leading
nificant. However, the extreme temperatures (22 to slower development, but one that is more robust
and 38 °C) increased brood mortality (Figure 4). to temperature fluctuations (Angilletta 2009). This
Our data showed that the T BROOD was on average still remains to be thoroughly tested, especially
30.5±2.9 °C (mean±s.d.) over the whole day and considering the difference in individual sizes and
34±1.4 °C (mean±s.d.) during the cooling periods. weight between S. depilis and A. mellifera . Sting-
These temperatures are most similar to the two less bee species are good candidates to test this
 Response of a stingless bee to nest overheating 463

hypothesis, since many different thermoregulato- REFERENCES

ry strategies are present among closely related
species. Angilletta, M.J. (2009) Thermal adaptation: a theoretical
Our results suggest that S. depilis have adap- and empirical synthesis. Oxford University Press, USA
tations similar to honeybees for coping with high Cooper, P.D., Schaffer, W.M., Buchmann, S.L. (1985)
temperatures. This likely represents an incident of Temperature regulation of honey bees (Apis mellifera )
foraging in the Sonoran desert. J. Exp. Biol. 114 (1), 1–
convergent evolution, since these adaptations de- 15
pends on a social context, and the origin of euso- Engels, W., Rosenkranz, P., Engels, E. (1995) Thermoreg-
ciality in both groups is considered to have oc- ulation in the nest of the neotropical stingless bee
curred independently (Michener 1974). Stingless Scaptotrigona postica and a hypothesis on the evolu-
tion of temperature homeostasis in highly eusocial
bees do not thermoregulate their nest as precisely bees. Stud. Neotropical Fauna Environ. 30 (4), 193–
as honeybees do. However, our results suggest 205
that S. depilis brood is more resistant to tempera- Figueiredo-Mecca, G., Bego, L.R., Nascimento, F.S.
ture variation during their development. We sug- (2013) Foraging behavior of Scaptotrigona depilis
gested that stingless bees’ strategy would be to (Hymenoptera, Apidae, Meliponini) and its relation-
ship with temporal and abiotic factors. Sociobiology
increase the thermal resistance—coupled with 60 (3), 280–285
proper nest site selection. In other words, increas- Heinrich, B. (1979) Keeping a cool head: honeybee ther-
ing capacity to tolerate higher temperature varia- moregulation. Science 205 (4412), 1269–1271
tion, expanding the range of thermal tolerance by Heinrich, B. (1993) The hot-blooded insects. Harvard Uni-
sacrificing higher performances at optimal tem- versity Press, Cambridge, Massachussets
peratures, results in longer development time Hilário, S.D., Ribeiro, M.F., Imperatriz-Fonseca, V.L.
(Huey and Hertz 1984; Angilletta 2009). (2012) Can climate shape flight activity patterns of
Plebeia remota Hymenoptera, Apidae)? Iheringia
Série Zoologia 102 (3), 269–276
Himmer, A. (1927) Ein Beitrag zur Kenntnis des
ACKNOWLEDGMENTS Wärmehaushalts im Nestbau sozialer Hautflügler. J.
Comp. Physiol. A: Neuroethol. Sens. Neural Behav.
We thank Rodrigo Augusto Santinelo Pereira and Physiol. 5 (2), 375–389
Christoph Grüter for their help with the statistical anal- Huey, R.B., Hertz, P.E. (1984) Is a jack-of-all-temperatures
ysis. We are especially grateful to Christoph Grüter, a master of none? Evolution: 441–444
Francisca Segers and Tommer Czaczkes for their sug- Jones, J.C., Oldroyd, B.P. (2007) Nest thermoregulation in
gestions that improved the manuscript. We would also social insects. Adv. Insect Physiol. 33 , 153–191
like to thank the three anonymous referees and the Kwon, Y.J., Saeed, S. (2003) Effect of temperature on the
journal editor, who provided valuable comments that foraging activity of Bombus terrestris L. (Hymenop-
improved the manuscript. We thank Capes and Fapesp tera: Apidae) on greenhouse hot pepper (Capsicum
for financial support (AVN 2012/11144-0; CM 07/ annuum L.). Appl. Entomol. Zool. 38 (3), 275–280
50218-1; VLIF 04/15801-0). Leonhardt, S., Dworschak, K., Eltz, T., Bluthgen, N. (2007)
Foraging loads of stingless bees and utilisation of
stored nectar for pollen harvesting. Apidologie 38 (2),
125–135
Réponses, sur le plan du comportement et du Lindauer, M. (1954) Temperaturregulierung und
développement, d'une abeille sans aiguillon Wasserhaushalt im Bienenstaat. Z. vergl. Physiol.
( Scaptotrigona depilis ) à une surchauffe du nid 36 (4), 391–432
Macías-Macías, J.O., Quezada-Euán, J.J.G., Contreras-
Thermorégulation sociale / refroidissement du nid / Escareño, F., Tapia-Gonzalez, J.M., Moo-Valle, H.,
et al. (2011) Comparative temperature tolerance in
approvisionnement en eau / Meliponini / Apidae
stingless bee species from tropical highlands and
lowlands of Mexico and implications for their
Verhaltens- und entwicklungsspzifische Reaktionen conservation (Hymenoptera: Apidae: Meliponini).
einer stachellosen Biene ( Scaptotrigona depilis ) auf eine Apidologie 42 (6), 679–689
Überhitzung des Nestes Mardan, M., Kevan, P.G. (2002) Critical temperatures for
survival of brood and adult workers of the giant hon-
soziale Thermoregulation / Kühlen / Wassersammeln / eybee, Apis dorsata (Hymenoptera: Apidae).
Meliponini / Apidae Apidologie 33 (3), 295–302
464 A. Vollet-Neto et al.

Menezes, C., Vollet-Neto, A., Imperatriz Fonseca, V.L. Radmacher, S., Strohm, E. (2011) Effects of constant and
(2013) An advance in the in vitro rearing of stingless fluctuating temperatures on the development of the
bee queens. Apidologie 44 (5), 491–500 solitary bee Osmia bicornis (Hymenoptera:
Michener, C.D. (1974) The social behavior of the bees: a Megachilidae). Apidologie 42 , 1–10
comparative study. Belknap Press Roubik, D., Peralta, F. (1983) Thermodynamics in nests of
Michener, C.D. (2000) The bees of the world. JHU Press two Melipona species in Brasil. Acta amazonica,
Moritz, R.F.A., Crewe, R.M. (1988) Air ventilation in nests 13(2), 453-466
of two African stingless bees Trigona -Denoiti and Silva, M.D., Ramalho, M., Rosa, J.F. (2011) Why do the
Trigona-Gribodoi . Experientia Basel 44 (11–12), stingless bee Melipona scutellaris (Hymenoptera,
1024–1027 Apidae) forage at high relative air humidity? Iheringia
Nicolson, S.W. (2009) Water homeostasis in bees, with the Série Zoologia 101 (1–2), 131–137
emphasis on sociality. J. Exp. Biol. 212 (3), 429–434 Simpson, J. (1961) Nest climate regulation in honey bee
Nogueira-Neto, P. (1948) Notas bionomicas sobre colonie. Science 133 (3461), 1327
meliponineos. I. Sobre ventilação dos ninhos e as Tautz, J., Maier, S., Groh, C., Rossler, W., Brockmann, A.
constucões com ela relationadas. Rev. Bras. Biol. 8 ,
465–488 (2003) Behavioral performance in adult honey bees is
influenced by the temperature experienced during their
Nogueira-Neto, P. (1997) Vida e criação de abelhas pupal development. Proc. Natl. Acad. Sci. U. S. A.
indígenas sem ferrão. Editora Nogueirapis, São Paulo
100 (12), 7343–7347
Paxton, R.J., Bego, L.R., Shah, M.M., Mateus, S. (2003)
Low mating frequency of queens in the stingless bee Undurraga, J., Stephen, W. (1980) Effect of tempera-
Scaptotrigona postica and worker maternity of males. ture on development and survival in post-
Behav. Ecol. Sociobiol. 53 (3), 174–181 diapausing leafcutting bee pupae (Megachile
rotundata (F.)). II. Low temperature. J. Kansas
Pereboom, J.J.M., Biesmeijer, J.C. (2003) Thermal con- Entomol. Soc.: 677–682
straints for stingless bee foragers: the importance of
body size and coloration. Oecologia 137 (1), 42–50 Weidenmuller, A., Kleineidam, C., Tautz, J. (2002) Collec-
tive control of nest climate parameters in bumblebee
Prange, H.D. (1996) Evaporative cooling in insects. J Insect
Physiol 42 (5), 493–499 colonies. Anim. Behav. 63 , 1065–1071

R Development Core Team. (2011) R: A language and Wilson, E.O. (1971) The insect societies. Harvard Univer-
environment for statistical computing. R Foundation sity Press, Cambridge, Massachusetts
for Statistical Computing, Vienna, Austria. ISBN 3- Zuur, A.F. (2009) Mixed effects models and extensions in
900051-07-0, URL http://www.R-project.org/ ecology with R. Springer