Osmoregulation in a nectar-feeding insect, the carpenter bee ...

Physiological Entomology (1990) 15,433-440 

Osmoregulation in a nectar-feeding insect, the carpenter bee 

Xylocopa capitata: water excess and ion conservation 

SUSAN W . N I C 0 LS ON 

South Africa 

Introduction 

Department of Zoology, University of Cape Town, 

Abstract. The liquid diet and high metabolic water production during 

flight in the carpenter bee Xylocopa capitata Smith 1854 (Hymenoptera, 

Anthophoridae) causes a water excess, and this is exacerbated by a low 

dietary intake of ions. The nectar and pollen of the preferred food- 

plants, Virgilia divaricata Adamson and Podalyria cafyptrata Willd., 

and other Fabaceae had low levels of sodium. Analyses of the bees and 

their body fluids showed that the bees have an exceptionally low Na 

content, and Na homeostasis seems to depend on recycling almost all 

Na which enters the rectum. The copious dilute urine (137 mOsm) had 

Na and K concentrations of only 3.4 and 7.0 mM, respectively. Isolated 

preparations of Xylocopa Malpighian tubules secreted a fluid with a K 

concentration 10 times that of the haemolymph. This means that 

recycling of K is as important as that of Na, and the bulk of K resorption 

probably occurs passively in the ileum. This study is the first to examine 

hymenopteran Malpighian tubules. Their stimulation by CAMP is in- 

dicative of the presence of a diuretic hormone in Xylocopa. 

Key words. Water and ionic balance, sodium, potassium, nectar, 

pollen, Malpighian tubules, hindgut, Xylocopa. 

Because nectar is primarily a sugar solution and 

most pollinators have high energy demands, 

much emphasis has been placed on the energ- 

etics of the relationship between plants and 

their pollinators. Only very recently has any 

attention been paid to the water component of 

nectar and the water balance of pollinators. 

Where insects are concerned, this work has 

been confined to various species of bee. In the 

large carpenter bee Xylocopa capitata Smith 

1854 (Hymenoptera, Anthophoridae), Nicolson 

& Louw (1982) found that metabolic water 

production during flight was so high that the 

bees might acquire excess water from their 

Correspondence: Dr Susan W. Nicolson, Department 

of Zoology, University of Cape TOWR, Rondcbosch 

7700. South Africa. 

flowers. This was confirmed for male bumble- 

bees, Bornbus lucorurn, by Bertsch (1984). 

The smaller honeybee produces less metabolic 

water, and incurs a water deficit in a dry climate. 

It is then obliged to collect free water (Louw & 

Hadley, 1985). Both honeybees and the solitary 

mason bee Chalicodorna sicula have been shown 

to compromise between two conflicting needs, 

for sugar and for water (Ohguchi & Aoki, 1983; 

Willmer, 1986). Further work on Xylocopa has 

demonstrated that two species foraging at the 

same plant in southern Israel have different 

water requirements, the smaller bee being more 

dependent on the water component of the nectar 

(Willmer, 1988). 

The osmoregulatory problems of animals 

involve salts as well as water. Among nectar- 

ivores, hummingbirds have received some at- 

tention in this respect (Calder & Hiebert, 1983). 

However, there has to date been no investigation 

433

434 Susan W. Nicolson 

of the ionic balance of a nectar-feeding insect, 

other than the work of Pivnick & McNeil(l987) 

on the skipper butterfly Thymelicus, in which 

sodium ions play an unusual role in reproduction. 

That Xylocopa capitata does not experience a 

water shortage was confirmed by analyses of 

nectar and body fluids, which showed that the 

bees produce a very dilute urine and in fact may 

have problems of ion conservation (Nicolson & 

Louw, 1982). The present study examines ion 

balance in X.capitata in more detail, by looking 

at dietary intake, ion levels in the bees and their 

body fluids, and the role of the Malpighian 

tubules. 

Materials and Methods 

Bees and flowers. In the Cape Town area the 

foraging of X.capitata is largely confined to two 

genera of the Fabaceae. The food plant in early 

spring, and an important site for territorial 

males, is Podalyria calyptrata Willd., which is 

replaced by Virgilia divaricata Adamson during 

the main breeding season of X.capitata. Later 

in the summer the old females, and a few newly 

emerged bees, are found on the flowers of 

another species of Virgilia, V.oroboides (Berg.) 

Salter. Bees and flowers were collected between 

September 1988 and January 1989, in Newlands 

Forest and at Kirstenbosch Botanic Gardens, 

both study sites being within a few minutes by 

car from the University of Cape Town. 

As far as possible, this study was confined to 

males of X.capitata, in order to conserve the 

breeding population, and because pollen is a 

minor component of the diet of the males. 

However, males become active earlier in the 

spring and apparently have a shorter life-span 

than females. It was necessary therefore to use 

older females for some analyses in late summer. 

Although females were previously found to be 

about 25% heavier than males (Nicolson & 

Louw, 1982), no difference in body mass be- 

tween the sexes was found in the bees sampled 

in the present study. 

Diet. The nectar and pollen of V.divaricata 

have previously been analysed in some detail 

(Nicolson & Louw, 1982; Louw & Nicolson, 

1983). For Podalyria I examined the following 

attributes of the nectar and pollen, using the 

methods already described for Virgilia: nectar 

volume, sugar concentration, and sodium and 

potassium concentrations, as well as pollen 

weight, water content and Na and K concen- 

trations. Nectar of two other plants was also 

analysed: Wisteria sinensis and Robinia pseudo- 

acacia, both introduced members of the 

Fabaceae which are attractive to carpenter bees 

during their brief flowering periods. All nectar 

samples were collected between 10.00 and 11.00 

hours, on days when X.capitata was active. 

Analyses of body fluids and bees. Freshly 

collected bees frequently produced urine when 

disturbed. Other body fluids (haemolymph, 

crop contents, midgut fluid and rectal fluid) 

were collected by dissecting cold-anaesthetized 

bees and sampling with calibrated micropipettes 

(Drummond Scientific Co.). Osmotic con- 

centrations were measured using a Wescor 

(Model 5 100B) vapour pressure osmometer, 

and Na and K concentrations by means of 

standard flame photometric techniques (Instru- 

mentation Laboratory, Model IL 243). 

Water contents of the bees were obtained by 

drying at 60°C for 48 h. If unusually large 

volumes of fluid were present in crop or rectum, 

these were first removed. Cation concentrations 

were then determined on the dried samples by 

ashing at 500°C for 4 h, digesting in concentrated 

nitric acid and diluting for ion estimations by 

flame photometry. 

Determination of haemolyrnph volume. 

Cold-anaesthetized carpenter bees were 

weighed and injected with 5 p1 of a solution 

of 'H-inulin (0.78 pCi per bee). Bees were 

injected laterally between the fourth and fifth 

abdominal sclerites to minimize the risk of punc- 

turing the crop. No bleeding occurred. 

The diluted 'H-inulin was sampled 5 min 

after injection. An incision was made in the 

second abdominal segment and 5 pl of haemo- 

lymph drawn into a calibrated micropipette. 

This was transferred to 1 ml of distilled water 

in a scintillation vial before mixing with 10 ml 

Insta-gel (Packard Instrument Co.) and 

counting in a Packard Tri-Carb 460C liquid 

scintillation counter. 

Malpighian tubules. The Malpighian tubules 

of X.capitata were studied as isolated prep- 

arations under liquid paraffin, with each tubule 

placed in a drop of bathing medium and its 

open proximal end wrapped around a fine pin. 

The bathing medium surrounding the isolated 

tubules contained (in mM): NaCl 42, KCI 17, 

MgC12 5, CaC12 2, NaHC03 6, NaH2P04 4,

glycine 10, proline 10, serine 10, histidine 10, 

glutamine 10 and glucose 285. Very little is 

known about the composition of bee haemo- 

lymph. The Na and K concentrations, and total 

osmolarity , were based on earlier measurements 

on the haemolymph of X.capitata (Nicolson & 

Louw, 1982). Apparently inorganic ions con- 

tribute little to the total osmolarity, hence the 

high concentration of glucose included in the 

bathing medium. Its measured osmolarity was 

475 mOsm, less than the mean of 544 mOsm 

reported by Nicolson & Louw (1982) but well 

within the normal range of haemolymph osmo- 

lari ty of X. capitata. 

Secretion rates of X. capitata tubules were 

measured under control conditions and in the 

presence of 1 mM adenosine 3’3’ cyclic mono- 

phosphoric acid (CAMP, Na salt, Sigma Chemi- 

cal Co.). CAMP mimics the action of insect 

diuretic hormones on Malpighian tubbles. The 

isolated tubules were maintained at a constant 

temperature of 25°C. Secretion rates were ob- 

tained by measuring the diameters of the se- 

creted droplets with an eyepiece graticule, 

and calculating their volumes. The same drop- 

lets were then removed with siliconed micro- 

pipettes for determinations of their Na and K 

concentrations. 

All results are presented as means +SE, with 

n in parentheses. Independent sample t-tests 

were used to assess the significance of differ- 

ences between means, with P values of


Table 2. Nectar composition of Wisteria sinensis and Robinia pseudoacacia. 

Wisteria Robinia 

Volume (pI/flower) 1.4020.14 (10) 0.5720.09 (10) 

Sugar concentration (g/100 ml) 39.7k2.3 (10) 85.6a7.2 (10) 

Total sugar (mg) 0.55a0.07 (10) 0.46k0.06 (10) 

Na (mM) 0.320.1 (7) 1.1k0.3 (4) 

K (mM) 4.120.4 (7) 6.4k1.1 (4) 

& Nicolson (1983): there were no significant 

diurnal changes in nectar volume, concentration 

or sugar content, nor was there any difference 

in these parameters in screened and unscreened 

flowers. 

Water and ion contents of bees 

These analyses were done on territorial males 

collected in early spring (October), and on 

females at the end of the breeding season (late 

January). In the latter sample, the head plus 

thorax and the abdomen were analysed separ- 

ately. The results are presented in Table 3. 

Although varying amounts of fluid remained 

in the digestive tracts, all values were very 

consistent between individuals, as shown by the 

small SEs. The lack of variability may be partly 

due to the minimal amounts of stored fat in 

X.capitata during late spring and summer (cf. 

Tucker, 1977). The water and ion contents of 

females were significantly lower than those of 

males: without further analyses it is not clear 

whether this is a difference between the sexes 

or a decline with age. Although the water con- 

tents of the abdomens were higher, there was 

Table 3. Water and ion contents of Xylocopa capitata. 

n 

no significant difference in cation content be- 

tween the different body regions in female bees. 

The values for sodium content given in Table 3 

are remarkably low. 

Analyses of body fluids 

Data on the composition of the body fluids 

are given in Table 4. In general these figures are 

in close agreement with previously published 

values (Nicolson & Louw, 1982), and data on 

V. divaricata nectar from the latter reference 

have been included in Table 4 for comparison. 

Na and K levels in the crop contents are low, 

as expected from the low dietary intake. The 

mid-gut fluid shows a dramatic reduction in 

osmolarity in comparison with the crop contents 

(data from Nicolson & Louw, 1982). Na and K 

were not measured in midgut fluid, but are 

likely to be rapidly absorbed into the haemo- 

lymph against concentration gradients for both 

ions. It is apparent from Table 4 that these 

cations (with their associated anions) account 

for only a small proportion of the total os- 

molarity of the haemolymph. This is also true 

of the rather dilute urine with extremely low 

Na K 

Water (wo4 (walk 

(70 wet mass) dry mass) dry mass) 

Males, whole body 9 64.520.5 47a3 183+3 

Females, whole body 11 63.020.3 30i3 147~5 

P*

Osmoregulation in a carpenter bee 437 

Table 4. Composition of body fluids of Xylocopa capitata and nectar of Virgilia 

divaricata. 

Osmolarity 

(mOsm/l) 

Nectar* 2993t11 (11) 

Crop contents* 5381 5240 (6) 

Midgut fluid 956568 (6) 

Haemolymph 536515 (11) 

Rectal fluid 228t33 (6) 

Urine 137513 (11) 

Na 

3.8k0.1 (15) 

3.920.8 (10) 

- 

48.122.1 (10) 

17.0k4.1 (6) 

3.4k0.6 (13) 

K 

1.4k0.1 (15) 

9.8k1.2 (11) 

- 

17.121.1 (10) 

14.522.6 (6) 

7.0k1.1 (11) 

* Data for Virgilia nectar, and for osmolarity of crop contents, arc from Nicolson 

& Louw (1982). 

concentrations of Na and K (with anions, 

only 15% of the total osmolarity). It would be 

interesting to see whether nitrogenous waste or 

unassimilated sugar is the main osmotically 

active constituent of the urine. Body fluids were 

sampled from bees foraging on V. divaricata; 

and there is no difference in Na concentration 

between the nectar of this flower and the urine 

of X.capitata (t-test, P>O.O5). 

The bees, especially males, frequently ejected 

large volumes of urine (c. 30 ~ 1) when handled. 

Willmer (1988) has also recorded the production 

of a copious dilute urine in X.pubescens. In a 

few freshly caught X.capitata which did not 

produce urine when handled, rectal fluid was 

sampled directly and was found to have higher 

osmotic and ionic concentrations than urine 

(Table 4). In these samples of rectal fluid the 

maximum K value was 20 mM (within the normal 

range of haemolymph K concentrations) and 

the maximum Na value was 34 mM (approximating 

the level in the fluid produced by isolated 

Malpighian tubules; see below). 

Haemolymph volume 

The 5 min allowed for equilibration of in- 

jected 3H-inulin was considered adequate be- 

cause all bees commenced vigorous ventilatory 

movements of the abdomen (associated with 

preflight thermogenesis) within 3 min of in- 

jection. This ensured rapid circulation of the 

haemolymph. The haemolymph volume of 

female Xylocopa averaged 219+.35 p1 (n=5). 

The mean mass of these bees was 1.309 g, 

giving a value of 167 ~1 of haemolymph per g 

body mass, close to the approximately 150 Fllg 

measured for Bombus terrestris by Surholt et al. 

(1988). 

Malpighian tubules 

The tubules of X.capitata were transparent or 

pale yellow, very numerous and often entangled 

with one another, and exhibited slow, rhythmic 

muscle contractions. Because of the large 

number of tubules, secretion rates of individual 

tubules were slow. Table 5 shows the effects of 

cAMP on fluid secretion rates and on the Na 

and K concentrations of the secreted fluid. 

Although secretion rates approximately trebled 

in the presence of CAMP, ion concentrations in 

the resulting fluid remained unchanged. The 

Malpighian tubules of X. capitata secrete a fluid 

Table 5. Secretion rates of Xylocopa capitata Malpighian tubules and ion concen- 

trations in secreted fluid. 

Control cAMP P 

Secretion rate (nllmin) 1.420.2 (9) 3.6k0.3 (9)


with the high K and low Na concentrations 

which are characteristic of most insect tubules. 

Discussion 

Foraging of X. capitata is largely confined to the 

flowers of Podalyria calyptrata and two closely 

related species of Virgilia, V.divaricata and 

V.oroboides. The nectar and pollen of these 

species are remarkably similar in composition 

(Table 1). The close similarity in nectar compo- 

sition extends to the flowers in inflorescences of 

W.sinensis and R.pseudoacacia, which are 

commonly utilized food sources for carpenter 

bees during shorter flowering periods. All four 

species belong to the subfamily Faboideae of 

the Fabaceae, suggesting a possible taxonomic 

correlation with nectar composition. The similar 

morphologies of these ‘pea’ flowers ensure that 

nectar is little affected by environmental 

conditions. The narrow range in values for total 

sugar content per flower (0.43-0.55 mg) is 

especially noteworthy. Very little information is 

available on the ion concentrations of flower 

nectars, but the data given by Hiebert & Calder 

(1983) also show low levels of sodium in the 

nine plant families they sampled. 

The very concentrated nectar produced by 

X. capitata’s flowers is advantageous to the bees 

in that it imposes a smaller water load than 

more dilute nectars. The elegant study of 

Bertsch (1984) demonstrated that water loading 

limits the activity of male bumblebees (Bombus 

lucorum) fed on 50% sucrose; their daily water 

turnover was found to equal the total volume of 

body water. Willmer (1986, 1988) has discussed 

further the role of water as a physiological 

constraint for foraging bees (including 

Xylocopa), and the effects of climate and body 

size. X.capitata is such an enormous bee that 

the metabolic water produced during flight far 

outweighs the water gained from nectar; the 

nectar sugar concentration is thus not particu- 

larly relevant to its water budget (Willmer, 

1988). Where the diuresis associated with flight 

is concerned, ion concentrations in the nectar 

are more important. 

The scarcity of sodium in the diet of X.capitata 

foraging on V.divaricata has already been re- 

marked upon (Nicolson & Louw, 1982). 

The present study shows that foraging on 

P.calyptrata in early spring can not provide 

these insects with additional reserves of sodium; 

nor can brief but intensive periods of foraging 

on other flowers like W.sinensis and R.pseu- 

doacacia. The late summer food source for 

X.capitata is V.oroboides, which has nectar 

virtually identical in volume and concentration 

to that of V. divaricata (Louw & Nicolson, 1983), 

so that K and Na concentrations in this nectar 

are almost certainly low. 

Female carpenter bees provision their brood 

cells with a mass of pollen mixed with nectar. 

X.capitata is a very large bee (approx. 1.5 g) 

and each pollednectar ball contains, on 

average, 2064 mg of pollen and 936 mg of 

nectar (Louw & Nicolson, 1983). From this we 

can calculate the quantity of sodium available 

for the development of a single bee. The data 

for V.divaricata flowers (Table 1) are used 

because this is the main food source of pro- 

visioning females. The pollen provides 29 pmol/ 

g dry mass or 39.8 pmol of Na per pollen/nectar 

ball, and the nectar contribution is 3.8 mmol/l 

or 2.9 pmol per pollednectar ball, giving a total 

of 42.7 pmol of Na. 

Table 3 gives the Na content of male bees 

collected in early spring as 47 pmol/g dry mass, 

which represents a mean of 26.1 pmol per bee 

(mean dry mass 0.556 g; n=9). The food pro- 

visioned for larval development is thus more 

than adequate as far as Na requirements are 

concerned. Perhaps Na is more of a limiting 

factor in ionic homeostasis of the adult bees, in 

which salt losses due to diuresis are aggravated 

by a low dietary intake. 

Table 6 summarizes what little information I 

have been able to find on the Na and K contents 

of insects. Diets of these species differ: they 

include an omnivore (Periplaneta), a herbivore 

(Schistocerca), a carnivore (Dytiscus) and two 

nectarivores (Xylocopa and the hesperiid 

butterfly Thymelicus). It is generally accepted 

that Na levels are low in plant tissues (e.g. 

Seastedt & Crossley, 1981), so we might expect 

a lower Na content in Schistocerca than in 

Dytiscus. Of the insects listed in Table 6, 

however, only the two nectarivores were feeding 

on their natural diets, and their Na contents 

differ greatly. Alfalfa nectar, one of the pre- 

ferred food sources of Thymelicus, is not rich in 

Na (Pivnick & McNeil, 1987); yet male butter- 

flies have a Na content which is 10 times that of

Table 6. Na and K contents (pmol/g dry mass) of five insect species. 

Species Na K Reference 

Osrnoregulution in a carpenter bee 439 

Periplaneta americana, males 125 474 Tucker, 1977 

Schistocerca gregaria, males 80 136 Albaghdadi, 1987 

Thymelicus lineola, mated males 407 - Pivnick & McNeil, 1987 

Dytiscus verticalis 180 - Frisbie & Dunson, 1988 

Xylocopa capitata, males 47 183 Present study 

Xylocopa males. This discrepancy is only partly 

explained by the fact that Thymelicus is a special 

case as far as Na balance is concerned. 

‘Puddling’ behaviour by the males ensures that 

their Na levels remain high, and Pivnick & 

McNeil (1987) have provided clear evidence 

that males transfer considerable quantities of 

Na to females during mating. 

X.capitata adults have access only to nectar 

and pollen of very low Na concentrations. Their 

Na content is much lower than that of the other 

insects in Table 6. Their adult life is long and it 

is possible that the Na content may decline 

steadily with age (see the difference between 

males and females in Table 3). The haemolymph 

Na concentration does not vary with age or sex 

(unpublished data); its mean value of 48 mM 

represents, with a haemolymph volume of 

219 yl, about 40% of the total body Na (and 

a much higher percentage in old females; 

Table 3). It is obvious then that the haemolymph 

Na must be carefully conserved. 

At this point we should consider the circu- 

lation of ions, first Na and then K, in the 

excretory system of the carpenter bee. When 

bathed in a fluid resembling the haemolymph in 

ion composition, the Malpighian tubules secrete 

fluid containing about 35 mM Na. This fluid then 

passes along the narrow ileum to the rectum. 

Analyses of rectal fluid showed that the Na 

concentration of the primary urine may remain 

unchanged during passage along the ileum, but 

micropuncture sampling of ileal fluid is necess- 

ary to confirm this. The large and distensible 

rectum possesses six circular rectal papillae and 

it is probable that these are the site of Na 

resorption, resulting in a final Na concentration 

as low as 3.4 mM (range 1-8 mM). This is 

almost as impressive as the mean of 1 mM Na in 

the rectal fluid of Schistocerca fed on tap water 

only (Phillips, 1964). 

Although K does not at first appear to be a 

limiting factor in the diet of Xylocopa, the bees 

do require efficient mechanisms of K regulation. 

Imms (1957) describes the alimentary canal of 

the Hymenoptera and states that both Bombus 

and Apis possess about a hundred Malpighian 

tubules. As a rough approximation, assuming 

that Xylocopa has the same number of tubules, 

the rate of primary urine formation in this insect 

would be 8.4 pl/h under normal conditions or 

21.6 yllh when the tubules are stimulated (data 

for control and CAMP-stimulated tubules in 

Table 5). This could complicate K homeostasis. 

The K concentration of the Malpighian tubule 

fluid is high, 160 mM, while that of the haemo- 

lymph is low at 17 mM. If the Malpighian 

tubules were secreting at maximal rates, almost 

all the K could theoretically be removed from 

the haemolymph in only an hour. Obviously 

there must be rapid resorption of this ion, 

particularly as the final urine contains only 7 

mM K. Such resorption would be especially 

important to males feeding on nectar only. The 

data for rectal fluid in Table 4 suggest that the 

bulk of this resorption takes place in the ileum 

rather than the rectum. Such K resorption would 

be a passive process, resembling that occurring 

in the ileum of the butterfly Pieris brassicae 

during post-eclosion diuresis (Nicolson, 1976). 

In P. brassicae the result of this K resorption is 

also a dilute urine. The rectal papillae of 

X.capitata are probably capable of resorbing K 

and C1 as well as Na ions, and could then lower 

the K concentration still further. 

In order to remain in salt balance, carpenter 

bees must therefore recycle almost all Na and K 

entering the hindgut in the primary urine. 

Bombus must possess an equally efficient ex- 

cretory system: bumblebees can be kept for 10 

days on a diet of pure sucrose solution, with 

several hours of intensive flight, and associated 

diuresis, each day (Bertsch, 1984; Surholt et al., 

1988).


This discussion has been somewhat speculat- 

ive, because the recent work of Irvine et al. 

(1988) is the only rigorous study of transport 

processes in the insect ileum. To the best of my 

knowledge, no work has been done on the 

excretory physiology of any of the Hymenoptera. 

The present study is the first to examine the 

Malpighian tubules of a member of this order, 

and the demonstration of a stimulatory effect of 

CAMP is good evidence for the presence of a 

diuretic hormone in X.cupituta. This is not at all 

surprising in view of the excess of metabolic 

water production during flight (Nicolson & Louw, 

1982), the frequent urination of Xylocopu and 

other bees during flight, and the habit of female 

Xylocopa of squirting faecal fluid in defence of 

the nest (Anzenberger, 1977). There remains 

a rich field for future research in the water 

economy and osmoregulation of the Hym- 

enoptera. 

Acknowledgments 

I am grateful to the Foundation for Research 

Development for generous financial assistance, 

and to Kirstenbosch Botanic Gardens and the 

Newlands Forest Station for permission to 

collect bees and flowers. Gideon Louw and 

John Hoffmann kindly commented on the 

manuscript. 

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Accepted 17 November 1989

Osmoregulation in a nectar-feeding insect, the carpenter bee ...

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