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First published online January 16, 2009
Journal of Experimental Biology 212, 429-434 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.022343
Review |
Water homeostasis in bees, with the emphasis on sociality
Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa
e-mail: swnicolson{at}zoology.up.ac.za
Accepted 14 October 2008
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Summary |
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 TOP Summary Why bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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Key words: nectar, bubbling, water collection, evaporation
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Why bees? |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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) and
is complicated by the social context. Bees show the full spectrum of
sociality: although most are solitary it is the social bumblebees and
honeybees whose physiology and behaviour are most familiar to us
(Willmer and Stone, 2004). In
addition, the sophisticated thermal physiology of bees has received much more
attention (e.g. Heinrich,
1985; Kovac et al.,
2007) than their water regulation. Here I briefly examine the
water balance physiology of bees, considering the usual avenues of water gain
and loss, at two levels of organisation: the individual and the colony,
sometimes termed a `superorganism' (Moritz
and Southwick, 1992). It is accepted that social homeostasis can
be explained by the coordinated activity of bees as individuals, responding to
their internal or external environment, without the need to invoke centralised
control (Jones and Oldroyd,
2007; Seeley,
1995).
Water fluxes of honeybees can be very high at the colony level. For
example, Seeley estimated average annual requirements of 120 kg of nectar, 20
kg of pollen and 25 litres of water for a single wild colony
(Seeley, 1995). This applies
to honeybees in cold temperate conditions, and the estimate for nectar
includes substantial energy stores required for over-wintering. The seasonal
cycles of African honeybees are limited by rainfall, not temperature, and
better foraging weather means that in comparison massive honey stores are not
needed (Hepburn and Radloff,
1998).
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Water gain in food |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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).
Where comparisons have been made, male Xylocopa capitata and
Anthophora plumipes carry much smaller crop loads than do females
(Louw and Nicolson, 1983;
Stone, 1995). The impermeable
crop expands greatly for storage and transport of nectar and protects the
haemolymph from osmotic shock. Apis mellifera workers can carry close
to their body mass in nectar, although crop loads tend to be much smaller
(Schmid-Hempel et al., 1985)
and are positively correlated with the nectar concentration
(Hunt et al., 1995). This
suggests that under natural conditions honeybees might carry less than during
experiments in which they are fed concentrated sugar syrup (e.g.
Park, 1932;
Waller, 1972). Their feeding
system is designed to retain nectar in the crop for as long as possible. Sugar
leaves the crop at a rate dependent on the metabolic rate of the individual,
but the fluid-emptying rate (and the rate of rectal filling) are inversely
proportional to nectar concentration
(Roces and Blatt, 1999).
Two factors – the body size of bees and environmental conditions
– strongly influence their need to obtain water from nectar. Large bees
require concentrated nectar at low to moderate ambient temperature
(Ta) because of their very high metabolic water production
in flight (Bertsch, 1984;
Nicolson and Louw, 1982). In
contrast, smaller desert bees in Israel (mason bees and carpenter bees) use
dilute nectar for rehydration purposes, as shown by field measurements of
decreasing haemolymph osmolality after ingestion of nectar
(Willmer, 1986;
Willmer, 1988). For even
smaller bees in less arid environments, dilute nectar imposes a high water
load. After drinking the dilute (14% w/w) nectar of Aloe arborescens,
female allodapine bees, Allodapula variegata and Braunsapis
sp., concentrate it on the tongue by repeated regurgitation, evaporation and
re-ingestion (Fig. 1) (M. B.
Ellis and S.W.N., unpublished), presumably before mixing it with pollen and
feeding it to their larvae (allodapine bees are characterised by progressive
provisioning of the brood). This is analogous to `bubbling' or oral droplet
extrusion behaviour in fruit-feeding tephritid flies
(Hendrichs et al., 1992). The
same behaviour has been seen in Hylaeus heraldicus (Colletidae) after
collecting dilute nectar of Kniphofia sp.
(Nicolson, 1998). Other
reports of nectar dehydration are in solitary and social halictine bees
(Michener, 1974). The
behaviour is not confined to females: laboratory-fed male bumblebees evaporate
nectar on their tongues when given 30% instead of 50% sucrose
(Bertsch, 1984), and male
carpenter bees Xylocopa nigrocinta are fed nectar by females, then
dehydrate it at the nest entrance, thus improving the efficiency of
territorial flight (Wittmann and Scholz,
1989). Stingless bee males form large congregations outside the
nest where they dehydrate nectar on their tongues
(Cortopassi-Laurino, 2007). In
all these examples, oral elimination of excess water compensates for less than
ideal nectar concentrations.
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Fresh pollen is relatively dehydrated after exposure at anthesis, but its
water content increases after collection by bees due to the addition of nectar
and glandular secretions (Human and
Nicolson, 2006). The larval diets of bees vary greatly in water
content (Roubik, 1989). The
water content of royal jelly is around 67%
(Wongchai and Ratanavalachai,
2002), but the larval food of stingless bees contains less water,
a thicker consistency being necessary for larvae floating on top of mass
provisions (Hartfelder and Engels,
1989). Large carpenter bees provision their nests with semi-solid
masses of pollen combined with nectar, giving a final water content of only
20% in the provisions of X. capitata
(Louw and Nicolson, 1983). In
Xylocopa mordax, nectar is pre-concentrated on the tongue for this
purpose (Corbet and Willmer,
1980).
Colony
Honeybees prefer sugar concentrations of 30–50% (sugar concentrations
here are given as % w/w as in refractometer measurements) under experimental
conditions (Waller, 1972), but
in practice they collect from a much wider range of nectars. Seeley measured
15–65% in nectar loads being brought into a single colony
(Seeley, 1986), and Hunt and
colleagues recorded a similar range of concentrations in incoming loads
(Hunt et al., 1995). The
choice of nectar concentration depends on the ecological context, i.e. on the
other food sources available at the time. This has long been a complicating
factor in experimental studies of honeybee foraging behaviour. For example,
Lindauer found that the threshold sucrose concentration for eliciting
recruitment behaviour declined from 55% to 4% as the German summer progressed
(Lindauer, 1948). Empirical
measurements of energy intake rate in bees show peak values at sucrose
concentrations around 60% in bumblebees, stingless bees and honeybees
(Harder, 1986;
Roubik and Buchmann, 1984).
Note that for orchid bees (Euglossini), which use suction feeding rather than
a lapping mechanism, optimal concentrations are lower and more dilute nectars
are collected (Borrell,
2004).
Communal food storage requires that the osmolality of honey is high enough
to inhibit microbial growth (Pusey,
1999). In honeybees this is achieved first by hydrolysis of nectar
sucrose to glucose and fructose, through the addition of hypopharyngeal gland
enzymes, and then through evaporative processing by food-handling bees to
reach a concentration of about 82%. These bees evaporate nectar on their
tongues before placing droplets in open cells for further evaporation,
accelerated by fanning (Park,
1925). Among stingless bees, workers drink water condensed in the
nest during honey ripening and regurgitate it outside the entrance
(Roubik, 2006). Their ripened
honey is around 70% in concentration and tends to ferment
(Cortopassi-Laurino et al.,
2006; Roubik,
2006). Note that uncapped honey is hygroscopic and absorbs water,
so can be both a sink and source of water in the nest.
Trophallaxis is the regurgitation of the crop contents of a donor bee for
ingestion by receiver bees. Extremely rapid distribution of incoming nectar
was demonstrated by Nixon and Ribbands, who fed radiolabelled food to six
foragers and were able to detect the label in 62% of all foragers after only 4
h and in all large larvae in unsealed cells after 48 h
(Nixon and Ribbands, 1952).
Trophallactic interactions ensure that homeostasis is achieved in the
`collective stomach' of all workers, which is a nectar reserve for the colony
(Schmickl and Crailsheim,
2004). Similarly, colonies preparing to swarm store concentrated
food in their crops, comprising 20–30% of the mass of individuals and of
the swarm (Combs, 1972). In
addition to its nutritional significance, liquid transfer between adults is a
means of exchange of information about the quality and quantity of food
reserves in the colony (Crailsheim,
1998).
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Drinking/water collecting |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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). Although
bumblebees are not expected to drink, marked Bombus terrestris were
observed drinking repeatedly from a water trough during warm conditions
(Ferry and Corbet, 1996): it
is unlikely that individual bumblebees would have a water deficit so this was
probably for the benefit of the colony. When groups of 100 honeybees are
confined in cages and provided with 67% sugar, they drink about 10 µl of
water daily at Ta of 35°C and 40°C
(Free and Spencer-Booth,
1958).
Colony
Honeybee colonies collect water for two reasons, related to different types
of weather: for cooling of the brood area by evaporation on hot days, and for
feeding the larval brood when foraging is limited on cool days
(Lindauer, 1955;
Seeley, 1995). The classic
studies of Lindauer showed how bees regulate the hive temperature in hot
conditions (Lindauer, 1955).
Water is collected by water foragers, then distributed around the hive and in
cells containing eggs and larvae; fanning accelerates its evaporation, as does
regurgitation and evaporation on the tongue
(Lindauer, 1955). Visscher and
colleagues measured mean water loads of 44 mg in honeybees collecting water
under desert conditions (Visscher et al.,
1996). Paper wasps and hornets also use water for cooling their
nests, but the highly social stingless bees do not
(Jones and Oldroyd, 2007;
Roubik, 2006).
The second need for water – for consumption by nurse bees when
feeding the brood – is an aspect of water use by honeybees that tends to
be underestimated (Johansson and
Johansson, 1978). Nurse bees feed young larvae a secretion from
their hypopharyngeal glands; for worker larvae after the third day this jelly
is supplemented with honey and pollen
(Crailsheim, 1998). As already
mentioned, the water content of royal jelly is high, so nurse bees have a
great need for water when brood rearing is intensive; this water cannot always
be obtained from nectar.
The regulation of water collection in honeybees is discussed in detail by
Seeley (Seeley, 1995). In
essence, the rate of unloading of water foragers indicates the colony demand
for water (i.e. the feedback system is similar to that for nectar). In this
way the balance between collection and consumption of water is maintained.
Importantly, water collection does not interfere with the collection of
concentrated nectar by the colony
(Kuhnholz and Seeley, 1997).
The first bees to start water collection may be stimulated by the collective
increase in crop sugar concentration of all bees in the nest, due to
trophallaxis (Lindauer, 1955;
Seeley, 1995), or possibly by
the collective increase in haemolymph osmolality. Apart from environmental
factors, the tendency of honeybee foragers to collect water, nectar or pollen
has a genetic component (Hunt et al.,
1995). Workers with the lowest sucrose response thresholds, i.e.
those able to distinguish low sucrose concentrations from water in proboscis
extension response tests, become water foragers
(Pankiw and Page, 2000).
Water foraging is regulated according to current demand and water is not
stored in combs by temperate honeybee colonies: this is because nectar
availability fluctuates widely and water sources usually do not
(Seeley, 1995). For African
honeybees, occasional water storage has been recorded in wild bee nests, as
after summer rain in the Kalahari Desert
(Eksteen and Johannsmeier,
1991). Park recorded temporary storage of water in the crops of
`reservoir bees' (Park,
1923).
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Metabolic water gains |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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;
Nicolson and Louw, 1982),
especially at low or moderate Ta. Honeybees ferrying large
water loads to the hive at high Ta produce enough
metabolic water to offset their evaporative water losses
(Louw and Hadley, 1985).
However, it cannot be assumed that metabolic gains will balance evaporative
losses in flight. Because variation in metabolic heat production is used by
bees (Apis and Centris) as a primary mechanism of
thermoregulation in flight (Roberts and
Harrison, 1999; Roberts et
al., 1998), at high Ta metabolic water
production will decrease as evaporative water loss increases. For individual
bees, the thermal environment is crucial to water balance in flight.
Colony
Bees engaged in brood warming generate metabolic heat using their flight
muscles. At low Ta, the metabolic rates of incubating
bumblebees are extremely high (Heinrich,
1974). Honeybee brood nest temperatures are maintained constant at
about 35°C by bees that `shiver' on the comb surface or inside empty cells
in the brood area (Kleinhenz et al.,
2003), and high metabolic water production can be assumed during
this energy-intensive heating activity. However, the general colony heat
production to which all workers contribute does not require much increase in
metabolism (Harrison,
1987).
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Evaporative losses |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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;
Roberts et al., 1998).
Although the cuticular permeability of both species increases with
Ta, neither cuticular nor respiratory water losses are
sufficient to explain the very high evaporative water losses at high
Ta. These probably involve cooling mechanisms such as
regurgitation of crop contents onto the proboscis
(Heinrich, 1980). This `tongue
lashing' at high Ta has been observed in a variety of bees
(Roberts and Harrison, 1998)
and in honeybees has been shown to increase evaporative losses dramatically
(Louw and Hadley, 1985). As a
result, the thoracic temperatures of nectar and water foragers are
significantly lower than those of pollen foragers
(Cooper et al., 1985;
Feuerbacher et al., 2003).
Colony
The amount of water that has to be evaporated from dilute nectar is
enormous (Fig. 2). In order to
increase the sugar concentration from 20% to 82%, bees must evaporate 0.75 g
water for every 1 g of nectar collected, and the mass of honey produced from a
given mass of nectar is correspondingly reduced. Recently we have shown that
foragers of A. mellifera scutellata collecting dilute nectar of
Aloe greatheadii var. davyana in dry winter air begin to
concentrate the nectar before returning to the hive
(Nicolson and Human, 2008).
Because the crop is impermeable to both sugar and water, we can only explain
the doubling of crop sugar concentration, from 20% to 40%, by evaporation on
the tongue. This contradicts the conventional wisdom that the concentration of
nectar is unchanged during its transport by bees between flowers and the hive
(Park, 1932). The advantage
for the bees lies in reducing the water load that has to be carried and the
amount of evaporation needed in the hive
(Fig. 2); the cooling effect is
less desirable for individual foragers but disturbances of heat or water
balance can be corrected in the hive.
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The various processes involved in cooling the honeybee nest –
collecting water, spreading it within the brood comb, and speeding its
evaporation by fanning and regurgitation – have been mentioned above.
This enables the temperature in the brood area to be precisely regulated at
35°C, but humidity in the hive is less constant
(Human et al., 2006). Air in
the hive will generally be more humid than outside, as a result of
transpiration of the inhabitants and evaporation during nectar flows. While
high humidity is necessary for brood development, a dry atmosphere favours
nectar ripening. We have measured absolute humidity (thus excluding
temperature effects) in various regions of the hive, and found higher values
in the brood area than in nectar stores, suggesting adjustments by the bees
(Human et al., 2006). However,
trade-offs with regulation of temperature and respiratory gases will disrupt
the establishment of optimum humidity levels.
Colony level respiration is important in social homeostasis. Periodic
synchronised fanning leads to tidal ventilation in honeybees and stingless
bees when only one nest entrance is present
(Moritz and Crewe, 1988;
Southwick and Moritz, 1987).
Measurement of cyclic fluctuations in water vapour pressure and temperature at
the nest entrance would enable estimation of evaporative water losses at the
colony level.
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Excretory losses |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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;
Nicolson and Louw, 1982;
Pasedach-Poeverlein, 1940;
Roubik, 1989). Diuretic
hormones (DHs) are likely to be involved. The availability of the honeybee
genome has enabled genomic mining for neuropeptides: using a combined
bioinformatics and peptidomics approach, Hummon and colleagues have confirmed
the presence of a calcitonin-like DH in Apis mellifera and inferred a
corticotropin-releasing factor (CRF)-like DH by homology
(Hummon et al., 2006). In
Bombus and Xylocopa there is extensive hindgut reabsorption
of Na+ and K+ from the tubule fluid, and it is clear
that ion conservation is essential during diuresis
(Nichol, 2000;
Nicolson, 1990). The fine
structure of the six elongated rectal pads of adult honeybees was described by
Kummel and Zerbst-Boroffka, who also measured high osmolalities (mean 719
mosmol l–1) in the pad lumen but very low osmolalities (163
mosmol l–1) in the rectal lumen, showing that the rectal pads
are effective in reabsorbing ions (Kummel
and Zerbst-Boroffka, 1974). There are no data on the functioning
of honeybee rectal pads under more dehydrating conditions necessitating water
recovery from the excreta.
Colony
The non-random disposal of the excreta of social insects, such as ejecting
faeces late in larval development, is assumed to be for hygienic reasons
(Weiss, 2006). In honeybee
larvae, the midgut–hindgut junction is occluded until the end of the
larval stage, and defaecation coincides with cocoon formation, the excreta
being incorporated into the structure of the cocoon
(Jay, 1964). Healthy adult
Apis do not defaecate in the nest, even during overwintering in
temperate climates (but defaecation in or around the nest is a sign of
infection with the midgut parasite Nosema). Defaecation flights occur
when weather permits, and until then rectal fluid may be stored for prolonged
periods, the distended rectum occupying much of the abdominal cavity
(Fig. 3). Obviously an
individual honeybee's water content fluctuates enormously depending on the
volume of crop or rectal contents. An inverse relationship between crop and
rectal volumes has been measured in honeybees confined for varying times after
feeding (Roces and Blatt,
1999).
|
). Heat-shedding benefits have been suggested for the giant
honeybee Apis dorsata, which builds exposed combs and engages in mass
flights involving half the colony, each bee jettisoning 20% of its body mass
(Mardan and Kevan, 1989).
However, more comprehensive recordings for the same species show that mass
flight activity is highest during maximum brood production, and timed so that
brood temperature is minimally affected by the temporary absence of the
protective curtain of bees (Woyke et al.,
2004). Water shedding may be a more important function of mass
flights than heat shedding. |
Conclusion |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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Workers of Apis mellifera do not forage for themselves and in
social bees there is a blurring between the individual and colony in terms of
water balance physiology. Common to water regulation at both the individual
and colony level is the regurgitation of nectar or water on the tongue for
evaporative purposes. This is involved in water elimination from nectar both
in the hive and during foraging, and water is evaporated in the same way to
cool either the hive or the individual bee in flight. Heinrich has previously
drawn attention to the similarities in individual cooling, nest cooling and
food storage behaviours (Heinrich,
1985). Perhaps these all originate in bubbling (a term I prefer to
tongue lashing), which appears to function as a nectar-concentrating mechanism
in a variety of bees, and may have a profound influence on the water balance
physiology of solitary bees in addition to social homeostasis. The high
propensity of bees for regurgitation is important in both trophallaxis, which
is not confined to highly social species
(Kukuk and Crozier, 1990), and
bubbling to evaporate water.
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Acknowledgments |
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TOPSummaryWhy bees?Water gain in foodDrinking/water collectingMetabolic water gainsEvaporative lossesExcretory lossesConclusionReferences |
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