AMER. ZOOL., 38:418-425 (1998)
The Importance of Osmosis in Nectar Secretion and its Consumption by
Insects1
SUSAN W. NICOLSON
2
Department of Zoology, University of Cape Town, Rondebosch 7701, South Africa
Nectar is a simple food consisting of varying proportions of sucrose,
glucose and fructose dissolved in water. The mechanisms of its secretion are poorly
understood. Osmosis may explain why hexose-rich nectars are produced in larger
volumes and are more dilute than sucrose-rich nectars. Unless protected, nectar
tends to equilibrate with ambient humidity, and the concentrations available to
flower visitors can vary from 7-70% w/w. Most nectars are osmotically concentrated, especially when rich in hexose sugars. The only digestion needed is sucrose
hydrolysis, and monosaccharides and water are rapidly absorbed across the midgut of insects. Large flying insects feeding on nectar produce an excess of water
which must be eliminated by evaporation and excretion. Animals which utilise this
attractively packaged and easily digested food source may have osmoregulatory
problems when nectar concentrations do not match their water requirements.
SYNOPSIS.
to the physiology of nectar-feeding insects.
The insects which feed on nectar are pre- Paradoxically, although nectar is osmoticaldominantly adult Diptera, Lepidoptera, Hy- ly concentrated its consumption leads to a
menoptera, and some Coleoptera. Many are water excess in large active insects.
good fliers and good pollinators. Many supSUGAR/WATER RELATIONSHIPS IN NECTAR
plement their energy-rich diet with protein
from pollen or blood. Ecological aspects of Nectar composition and concentration
nectar-feeding have been reviewed by
The main sugars in nectar are sucrose
Boggs (1987) and Koptur (1992). Its con- and its component monosaccharides, glusumers benefit from the fact that nectar is a cose and fructose (Baker and Baker, 1982;
very pure food, its nutrients being small but see van Wyk and Nicolson, 1995). In
molecules which are assimilated directly, HPLC analyses of nectar sugars from sevleaving only water. Nectar feeding is thus a eral plant families (e.g., van Wyk et ah,
simple system in terms of physiology as 1993; Barnes et al., 1995), a marked diwell as ecology.
chotomy is evident between sucrose-domiWith some exceptions (Bertsch, 1984; nant nectars (sucrose >95% of total sugar)
Willmer, 1986, 1988; Nicolson, 1990), in- and hexose-dominant nectars. The patterns
sect-flower relationships have seldom been of nectar sugar composition are related to
examined from the point of view of osmo- the phylogeny of the plant families, the
regulation. Physiological studies of polli- quantities of nectar produced, and the prefnation biology have been more concerned erences of the pollinators.
with energetics and thermoregulation. In
Nectar concentrations vary widely, from
this review, I will look first at osmotic reabout
7—70% (w/w). Figure 1 illustrates the
lationships in nectar secretion, then the osdramatic
differences in water content of
motic challenges presented by a nectar diet
sugar solutions in this range of concentration: from 9 mg down to 0.4 mg water per
1
From the Symposium Responses of Terrestrial Ar- mg of sugar. Bee-pollinated flowers tend to
thropods to Variation in the Thermal and Hydric En- produce nectars with sugar concentrations
vironment: Molecular, Organismal, and Evolutionary exceeding 35%, while those visited by butApproaches presented at the Annual Meeting of the terflies, moths and birds secrete more dilute
Society for Integrative and Comparative Biology, 26nectars (Pyke and Waser, 1981; Baker and
30 December 1996, at Albuquerque, New Mexico.
2
Baker, 1982). Field observations on nectar
E-mail [email protected]
INTRODUCTION
418
OSMOTIC IMPLICATIONS OF NECTAR FEEDING IN INSECTS
10
o
8
.-
4
10 20 30 40 50 60 70
Sucrose concentration, % (w/w)
FIG. 1. Weight of water (mg) accompanying each mg
of sucrose in nectars of different concentrations. Redrawn from Bertsch (1984).
sources are not always in agreement with
laboratory studies using artificial feeders.
Even if their preferred concentrations are
high, butterflies and bees may take more
dilute nectar to meet their water needs (Watt
et al, 1974; Ohguchi and Aoki, 1983; Willmer, 1986, 1988). Sucrose often predominates in insect-pollinated flowers, especially
those visited by insects with high energy
requirements, such as bees and moths (Percival, 1961; Watt et al, 1974); this may be
because sucrose-dominant nectars tend to
be produced in smaller volumes and to be
more concentrated, while hexose nectars are
copious and dilute.
Nectar secretion
Nectar is derived from sucrose-rich phloem sap, but the mechanisms of secretion are
not well understood (Durkee, 1983; Fahn,
1988; Nichol and Hall, 1988). It is assumed
that the usually equal amounts of glucose
and fructose in floral nectars are a result of
enzymatic breakdown of sucrose by invertase (sucrase) in the nectary tissue. Pate et
al. (1985) found cowpea nectary invertase
to be activated only when the nectar was
diluted. With phloem sap sucrose as substrate, the enzyme functioned optimally at
a starting concentration of 14% (w/w). Nectar sugar composition then depends on the
presence and properties of nectary inver-
419
tases and the secretion concentration of the
nectar (not easily measured because of
equilibration with ambient humidity; Corbet et al, 1979).
Sucrose-H+ symporters in higher plants
are located in phloem and monosaccharideH+ symporters mainly in sink tissues (Sauer
et al, 1994). Invertase is presumed to be
associated with the cell walls of nectaries.
Sucrose hydrolysis will increase the osmotic concentration and draw water into the
nectar, leading to the secretion of a copious
dilute hexose nectar, instead of a more concentrated sucrose nectar. Invertase activity
will also maintain a favourable concentration gradient for the diffusion of sucrose
through the nectary tissue. In balanced nectars, product inhibition could limit the conversion to monosaccharides. Reabsorption
of sugar lowers nectar concentration (Nicolson, 1995) and will also alter its composition if certain sugars are reabsorbed preferentially.
Osmotic concentrations of nectar
Figure 2 illustrates the osmotic difference
between hexose and sucrose nectars: hexose
nectars are osmotically much more concentrated than sucrose nectars of the same refractometer concentrations (see also Corbet
et al, 1979). All nectars, unless very dilute,
have much higher osmolalities than insect
haemolymph. Beuchat et al. (1990) suggested that one advantage of sucrose nectars is that they contain more energy per
unit of osmotic concentration than do energetically equivalent hexose nectars, so
there will be a smaller osmotic gradient
across the anterior portion of the pollinator's gut. However, hydrolysis of sucrose
nectars in the insect gut immediately increases the osmolality, e.g., from 2,990 to
5,380 mOsm kg"1 in the crop of the carpenter bee Xylocopa capitata (Nicolson and
Louw, 1982).
At a given relative humidity, sucrose
nectars have higher concentrations than
hexose nectars when in equilibrium with
air: hexose solutions evaporate less readily
than sucrose solutions (Corbet et al, 1979).
Differences in viscosity between the two
nectar types are minor compared to changes
420
SUSAN W. NICOLSON
'kg)
3,000
(A
2,500
2,000
Osmolal ity(m(
/•"»
1,500
1,000
500
5
10
15
20
25
30
Sucrose equivalents (% w/w)
35
FIG. 2. Nectar osmolality as a function of sugar concentration in nectar samples from Eucalyptus ficifolia.
Expected osmolalities are shown for sucrose solutions (
) and a hexose mixture (
). Redrawn from
Nicolson (1994a).
in viscosity with concentration and temperature.
Even if hexose nectars are initially dilute,
equilibration with a low ambient humidity,
more rapid at high ambient temperatures,
soon results in a concentrated hexose nectar, as in the samples in Figure 2 which
were collected from the exposed flower
cups of Eucalyptus ficifolia (Nicolson,
1994a). Some insects not only feed on nectar but also live in it. Drosophila flavohirta
larvae inhabiting Eucalyptus flower cups
may be exposed to osmolalities increasing
from 500 to 3,000 mOsm k g 1 during a
warm day (Nicolson, 1994a). This suggests
impressive osmoregulatory capacities, as in
other larval Diptera which inhabit saline environments. When osmolalities are high
enough, nothing can survive—hence the
antibiotic properties of honey, an 82% solution of glucose and fructose.
SUGAR DIGESTION
Osmotic effects on crop-emptying
The evolution of an expandable crop, either a diverticulum (adult Diptera and Lepidoptera) or linearly arranged with the rest
of the gut, allowed carbohydrate feeders to
consume as much as possible of an unpredictable fuel supply for sustained flight ac-
tivity (Stoffolano, 1995). In addition to its
storage function, the crop is impermeable
to water and thus protects the haemolymph
from osmotic shock. This is particularly important when sucrose hydrolysis (the only
digestion needed in nectar feeders) begins
in the foregut, as in bees. The osmotic gradient between crop contents and haemolymph can then be very steep: e.g., a tenfold difference in Xylocopa capitata (Nicolson and Louw 1982). The a-glucosidases
which hydrolyse sucrose are produced in
hypopharyngeal glands of bees, but in midguts of other nectar feeders (Terra and Ferreira, 1994). Bees are a special case because
the processing of honey or provisioning of
brood cells requires sucrose hydrolysis to
achieve high osmolalities.
Crop-emptying regulates the entry of
sugar into the midgut and is the rate-limiting process in sugar absorption. The rate of
crop-emptying in the blowfly Phormia regina is inversely proportional to the osmotic concentration of the crop contents, high
sugar concentrations being released more
slowly (Gelperin, 1966). The mechanism
involves the haemolymph osmolality, because crop-emptying was slowed by injecting various sugars, NaCl or alanine (Gel-
OSMOTIC IMPLICATIONS OF NECTAR FEEDING IN INSECTS
perin, 1966). Similar results have been
found for honeybees (Crailsheim, 1988a).
The role of osmosis in pollen digestion
is not known. Pollen grains were found to
burst when transferred to lower osmolality
in vitro (Kroon et al, 1974), but this may
depend on the thickness of the pollen grain
wall (exine). Dandelion pollen grains in
honeybee midguts and Protea pollen grains
in the faeces of nectar-feeding rodents have
unbroken exines, the protoplasts shrinking
as they are digested through the germination pores (Peng et al, 1985; van Tets,
1997). The osmotic influx of water may increase the probability of opening of these
pores. In butterflies of the genus Heliconius
and in Drosophila flavohirta, hydration of
pollen held on the proboscis is thought to
cause the release of nutrients in a form of
external digestion (Gilbert, 1972; Nicolson,
19946).
Absorption of sugars
Absorption of sugars in insects has been
reviewed by Turunen (1985) and recently
by Turunen and Crailsheim (1996). In contrast to the situation in vertebrates, the evidence (mainly from studies using 14C-labelled glucose) points to passive uptake of
monosaccharides through the midgut. Nothing is known of the transporters involved.
A favourable gradient for glucose transport
is maintained by several factors: the high
concentration of sugars in the gut lumen,
removal of glucose from the haemolymph
by conversion into trehalose, and rapid absorption of solvent water (Turunen and
Crailsheim, 1996). A high osmotic permeability of the midgut is assumed. Among
nectar feeders, only honeybees have been
studied in detail (Crailsheim, 19886). Glucose transport occurs in the first two-thirds
of the midgut. Fructose and 3-O-methylglucose are absorbed at similar rates and the
latter sugar, because it is not metabolised,
reaches an equilibrium between the midgut
contents and haemolymph (Crailsheim,
19886). Sugar absorption can be extremely
rapid, labelled glucose being incorporated
into trehalose within 2 min of feeding bees
after an exhaustive flight (Gmeinbauer and
Crailsheim, 1993). Note that polymerisation
of glucose molecules to form trehalose re-
421
duces their osmotic effect. Moreover, one
molecule of water is released for each molecule of trehalose formed.
Sugars are absorbed at close to 100% efficiency in the midguts of honeybees, cockroaches, blowflies and butterflies (Hainsworth et al. [1990] and references therein).
Since nectar sugars are in relatively pure
form compared with other foods, this leaves
almost pure water to be eliminated.
WATER ELIMINATION
Evaporative losses
Water may be removed from sugary food
by evaporation. Examples are evaporation
of nectar in the hive before its storage by
honeybees; dehydration of honey crop nectar by female Xylocopa before provisioning
larval cells (Corbet and Willmer, 1980) and
by male Xylocopa before prolonged territorial flights (Wittmann and Scholz, 1989);
and regurgitation and reingestion of liquid
droplets ("bubbling behaviour") by tephritid flies and possibly other Diptera (Hendrichs et al, 1992). Small colletid bees
{Hylaeus heraldicus) collecting the nectar
of red-hot pokers {Kniphofia) show similar
behaviour (unpublished data, C. L. Griffiths), necessary because the concentration
of this hexose nectar is only 11%. The
evaporation of nectar may be for thermoregulation rather than water regulation, as
when honeybees regurgitate droplets of
crop contents to cool their heads. Body water is preserved and the behaviour also
serves to concentrate the nectar before storage (Heinrich, 1979).
Body size, flight and diuresis
The water status of an insect is influenced by its size, flight activity and the environmental conditions. Excess water is not
usually a problem for small nectar feeders.
At high ambient temperatures honeybees
collect free water, and small solitary bees
modify their foraging behaviour and seek
dilute nectars. Field measurements of haemolymph osmolality in the mason bee
Chalicodoma sicula showed rapid transfer
of nectar water into the haemolymph (Willmer, 1986).
In larger bees such as Xylocopa and
Bombus, metabolic water production ex-
422
SUSAN W. NICOLSON
ceeds evaporative water losses (Nicolson
and Louw, 1982; Bertsch 1984). In addition
to the pre-formed water in the nectar (Fig.
1), the oxidation of each mg sugar produces
0.6 mg of metabolic water. Bertsch (1984)
carried out an elegant study of the water
and energy budgets of male bumblebees
feeding on 50% w/w sucrose at 20°C and
spending 4 hr per day in flight. In 24 hr
each 220 mg male bumblebee drinks its
own weight of nectar, containing 110 mg of
water and producing an additional 66 mg of
metabolic water. With evaporative losses of
40 mg, a water load of 136 mg must be
voided daily. The concentration of the nectar ingested is thus critical for the insects'
water balance. Bertsch concluded that bumblebees feeding on more dilute nectars
would have great difficulty excreting the
excess water. Honeybees have the advantage of being able to evaporate such nectars
in the colony, but dilute nectars increase the
crop load and hence energy expenditure
during foraging.
AMP (Nicolson, 1990). Diuresis has not
been reported in hovering sphinx moths.
It is interesting to compare the osmotic
physiology of nectar feeders with that of
sap-sucking Homoptera. Xylem sap contains <0.1 mM sugar in a fluid of 26
mOsm kg"1, and the problem of internal
flooding is solved in cicadas by osmotic
transfer of water from anterior to posterior
midgut in the filter chamber, the excreted
fluid being extremely dilute (Cheung and
Marshall, 1973; Andersen et al, 1989).
Phloem sap has much higher and variable
sugar concentrations (6-27% w/w), and
aphids excrete excess sugar and water as
honeydew after retention of nitrogenous
components. Compared with nectarivores,
aphids have adopted an entirely different
solution to the problem of an osmotically
concentrated diet: high haemolymph sugar
levels, and polymerisation of dietary sugars to form oligosaccharides (Fisher et al,
1984; Rhodes et al, 1997). The honeydew
sugars are mostly oligosaccharides, such as
the trisaccharide melezitose, and the extent
of polymerisation is directly related to the
sucrose concentration of the diet. In Myzus
persicae fed 10-30% (w/v) sucrose (8301800 mOsm kg"1), haemolymph and honeydew osmolalities remain similar and independent of diet concentration (Fisher et
al., 1984).
Large but less active fliers may not have
serious water excess problems. The cetoniid
fruit beetle Pachnoda sinuata (approx. 1 g)
was flown on a flight mill for 15 or 30 min
periods, but showed no significant changes
in body mass, water content, haemolymph
osmolality or faecal fluid osmolality (the
latter about 350 mOsm kg"1)- There was no
sign of diuresis during flight, and no accelerated fluid secretion when Malpighian tu- Salt balance
bules were set up as in vitro preparations
Nectar feeders are obliged to eliminate
immediately after a 15 min flight (unpubwater while retaining salts, but they do oblished data, S. W. Nicolson).
+
+
The slower metabolism of beetles, flies, tain Na and K from nectar (Hiebert and
and butterflies, and more gradual digestion Calder, 1983; Nicolson and Worswick,
of nectar meals, may prevent disturbances 1990). Ions in nectar will help to keep the
of water balance. In butterflies diuresis is nectar dilute, by lowering the concentration
obvious after eclosion but not after feeding in equilibrium with a given RH (unpub(Nicolson, 1980). Diuretic hormones are lished data, S. A. Corbet). The water excess
undoubtedly involved in the elimination of experienced by Xylocopa capitata is exacthe fluid excess from a nectar diet. The erbated by a low dietary intake of ions in
voiding of dilute urine during flight is con- the preferred nectars of Fabaceae. However,
spicuous in bumblebees and carpenter bees these ions appear to be largely recovered by
(Bertsch, 1984; Nicolson, 1990; Willmer, the ileum, and the copious dilute urine con1988). Hymenopteran Malpighian tubules tains only 3.4 mM Na+ and 7.0 mM K+
have not yet been studied except for a brief (Nicolson, 1990). Dow's (1986) comment
look at those of Xylocopa, in which nu- on the lack of information concerning the
merous fine tubules are stimulated by cyclic gut physiology of nectar feeders is still true,
OSMOTIC IMPLICATIONS OF NECTAR FEEDING IN INSECTS
but in locusts the ileum is a major site of
Na+ regulation (Irvine et al., 1988).
COMPARISONS WITH BIRDS
423
sources, and collect free water if necessary.
Too much specialisation on particular flowers might cause osmoregulatory problems.
This has seldom been considered in pollination studies, except by Willmer (1986,
1988) for small solitary bees foraging in an
arid environment.
Avian nectarivores tend to consume more
dilute nectars than do insects. Sugar transport in the hummingbird intestine (in contrast to the insect midgut) is an active proACKNOWLEDGMENTS
cess, and the low passive permeability of
the intestine is considered an adaptation to
This work was supported by the South
prevent loss of blood solutes to the gut lu- African Foundation for Research Developmen during rapid fluid transit (Diamond et ment and the University of Cape Town. W.
al., 1986). However, passive sugar transport Stock commented on the manuscript. I
may be more important in other avian nec- thank Jon Harrison for inviting me to partarivores, such as lorikeets (Karasov and ticipate in the symposium, and the NSF for
Cork, 1994). Crop-emptying controls sugar a generous contribution to travel costs.
digestion in hummingbirds as well as in insects, the birds perching quietly until they
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