Behavioural differences betweenmale and female
R E S EA R C H P A P E R
Behavioural differences between male and female carpenter bees in nectar robbing and its effect on
reproductive success in Glechoma longituba (Lamiaceae)
Y.-W.Zhang 1,2,J.-M.Zhao 2,C.-F.Yang 3&W.R.Gituru 3
1Department of Biology,Eastern Liaoning University,Dandong,China
2Department of Biology,Changchun Normal University,Changchun,China 3Wuhan Botanical Garden,The Chinese Academy of Science,Wuhan,China
INTRODUCTION
In addition to attracting pollinators,plants also attract organisms that may potentially compromise reproductive ?tness,such as nectar robbers.The plants must achieve a trade off between the bene?t and cost,and establish a sys-tem that encourages the pollinators while not encouraging the antagonists (Galen &Cuba 2001;Stanton 2003).Recent evidence shows that nectar robbing could have direct and indirect effects on plant ?tness (see review in Maloof &Inouye 2000;Irwin 2006).For example,nectar robbing may decrease reproductive output by directly damaging reproductive tissues (Irwin et al.2001;Zhang et al.2007a),or indirectly by causing changes in the
behaviour of legitimate pollinators (Irwin &Brody 2000;
Gonza
′lez-Gomez &Valdivia 2005).Nectar robbers act,in most cases,as antagonists for plant reproduction (nega-tive effect),for example,in instances where pollinators can discriminate robbed ?owers,thus reducing pollen ?ow and affecting reproductive success (Irwin &Brody 1999;Lara &Ornelas 2001).However,nectar robbers can also enhance plant ?tness (positive effect)in some spe-cies,for example,by providing pollinator services to the ?owers (Waser 1979;Higashi et al.1988;Navarro 2000).In some instances,both positive and negative effects may occur simultaneously (Zhang et al.2007a).Moreover,neutral effects of nectar robbing on host ?tness have also been found in several cases (Guitian et al.1993;Stout
Keywords
Behaviour differentiation;?tness;Glechoma longituba ;nectar robbing;net energy gain;Xylocopa sinensis .
Correspondence
J.-M.Zhao,Changchun Normal University,Changchun 130032,China.E-mail:jmz@https://www.sodocs.net/doc/be17590290.html, Editor J.Arroyo
Received:3March 2009;Accepted:17September 2009
doi:10.1111/j.1438-8677.2009.00279.x
ABSTRACT
Male and female nectar robbers may show signi?cantly different behaviour on host plants and thus have different impacts on reproductive ?tness of the plants.A 4-year study in natural populations of Glechoma longituba has shown that male carpenter bees (Xylocopa sinensis)are responsible for most of the nectar robbing from these ?owers,while female bees account for little nectar robbing,demonstrating distinct behavioural differentiation between male and female bees in visiting ?owers.The smaller male bee spends less time visiting a single ?ower than the larger female bee,consequently,the male bee is capable of visiting more ?owers per unit time and has a higher foraging ef?ciency.Moreover,the robbing behaviour of female carpenter bees is more destructive and affects ?ower structures (ovules and nectaries)and ?oral life-span more than that of the male bee.According to the energy trade-off hypothesis,the net energy gain for male bees during nectar rob-bing greatly surpasses energy payout (17.72versus 2.43J),while the female bee net energy gain is barely adequate to meet energy payout per unit time (3.78versus 2.39J).The differences in net energy gain for male and female bees per unit time in nectar robbing are the likely cause of observed behavioural differences between the sexes.The differences in food resource preference between male and female bees constitute an optimal resource allocation pattern that enables the visitors to utilise ?oral resources more ef?ciently.
Plant Biology ISSN 1435-8603
Plant Biology a2009German Botanical Society and The Royal Botanical Society of the Netherlands
1
et al.2000).The effect of nectar robbing on plant repro-ductive success results from a complex and variable array of positive,neutral or negative interactions rather than a simplistic single side effect scenario as had earlier been envisaged(Maloof&Inouye2000;Irwin et al.2001;New-man&Thomson2005;Castro et al.2008,2009). Studies have shown that insects of the same species, but different sex,can display disparate foraging modes and?or behaviour.For example,the males of Apis mellif-era when foraging on Asystasia gangetica(Acanthaceae) may collect both nectar and pollen,although they tend to concentrate more on either one or the other resource, while females collect only nectar(Villalobos&Shelly 1996).In another case,40%of honeybees visiting native cotton,Gossypium thurberi(Malvaceae),collected pollen only,while60%concentrated on nectar collection but also gathered pollen passively(Buchmann&Shipman 1990).Males and females of Lasioglossum sordidum(Api-dae)feed on different rewards and show different prefer-ences for dimorphic?owers from dioecious or gynodioecious plants(Delph&Lively1992).
Disparate behaviour patterns and modes during?ower visits by insects of the same species,but different sex,have been observed not only among legitimate pollinators but also among nectar robbers.The female Bombus occidental-is(queen)is strictly a nectar robber in many species, while the male bee both robs nectar and collects pollen (Ranta1983).Research on Fouquieria splendens(Fouqui-eriaceae)indicated that males and females of Xylocopa cal-ifornica might have different food preferences,with males feeding almost entirely on nectar while the females collect pollen(Waser1979).The different food preferences of males and females of the same species of insect may be attributed to their different roles in nest provisioning. However,hardly any studies have been conducted on the effect of behaviour differences of nectar robbers on the reproductive?tness of the host,and there are no reports exploring reasons for the behaviour differences and advantages this might confer to the nectar robbers.
Our4-year study on the pollination ecology of Glecho-ma longituba revealed that this plant has a high nectar robbing frequency by Xylocopa sinensis in many popula-tions in central China(Zhang2007),but preliminary observations indicated that male and female individuals display distinct behavioural differences during?ower visi-tation.The frequency of nectar robbing by male bees was more than four times that of female bees,and a visit by a female bee resulted not only in higher destruction of tis-sues of?ower structures,including corolla,ovules and nectaries,but also a reduction in?ower longevity in com-parison to a visit by a male bee(Zhang&Guo2006; Zhang et al.2007a).We hypothesised that the behavioural differences between male and female carpenter bees in nectar robbing of G.longituba?owers are aimed at enhancing ef?ciency in obtaining?oral resources and that these behavioural differences effect the reproductive?t-ness of the plant.On the basis of our hypothesis,our present study speci?cally addressed the following ques-tions.(i)What are the behavioural differences in nectar robbing between male and female bees?(ii)What is the effect of nectar robbing by male or female bees on repro-ductive?tness of G.longituba?(iii)What are the differ-ences in net energy gain per unit time in nectar robbing for male and female bees?We also discuss the possible ecological signi?cance of behavioural differences between nectar robbers in terms of more ef?cient utilisation of ?oral resources in the population.
MATERIALS AND METHODS
Study system
Glechoma longituba(Nakai)Kuprian(Lamiaceae),a com-monly used Chinese medicinal plant,is a clonal,perennial gynodioecious herb.In general,it begins?owering in early March in central China and?owers for5–6weeks. The?owers are clustered at stem nodes and?ower open-ing occurs sequentially from bottom to top.Despite the species being described as having two to six?owers at each node(Li1977),the plants in our study site had only two?owers at each node.The corolla of the bisexual ?ower is lavender,with a length of about22–26mm.A dark purple spot(nectar guide)is found in the lower lip. The four anthers are located at approximately the same level as the stigma.Male-sterile(female)?owers are smal-ler(10–15mm)and their anthers are degenerate.The mature stigma is bifurcated into two lobes.Most?owers open in the morning and remain in good condition for 2days before they begin to wilt.Breeding studies have shown that the bisexual?ower is self-compatible,but insects are necessary for successful pollination and fruit-ing under natural condition owing to herkogamy(Zhang 2007).Two weeks after fertilisation,the nutlets ripen in the calyx tube,with a maximum of four nutlets(i.e. seeds)developing from a single?ower.
About10insect species were observed visiting?owers of G.longituba in the study population(Zhang et al. 2007a).The main legitimate pollinators,who provide ef?-cient pollinating service while foraging for nectar by entering?owers through the corolla opening,are Antho-phora plumipes and Apis cerana.Their visiting frequency accounts for nearly70%of total visits.The only nectar robber is the carpenter bee X.sinensis Smith,whose visit-ing frequency accounts for about20%of total visiting fre-quency in the study population.Other?oral visitors account for<10%of visits(Zhang et al.2007a). Xylocopa sinensis is a large,solitary bee that is common in central China and nests in dry or fresh wood.The whole body is hairy and there is a marked difference in body size between male and female individuals.In the study population,the male bee is yellow and smaller than the female,with a length of21–23mm,and weighs0.49–0.52g(n=10).The female bee is dark in colour,with a length of25–26mm and weighs0.62–0.65g(n=10). X.sinensis mostly obtains nectar by robbing the tubular ?owers but can also forage for nectar in plants devoid of
Robber bees and Glechoma longituba reproductive success Zhang,Zhao,Yang&Gituru 2Plant Biologya2009German Botanical Society and The Royal Botanical Society of the Netherlands
tubular corollas without robbing them(Wu2000).Previ-ous observations indicated that the?owering season of G.longituba coincides with the period of activity of X.sinensis(Zhang et al.2007a).Although the visiting fre-quency of male and female carpenter bees to?owers of G.longituba were clearly different,there was no obvious difference in the number of male and female bees at the study site according to our observations on different dates in the4study years(Zhang2007).
Study site and population
The study was conducted in spring2003–2006during the ?owering period of G.longituba in central China.The study population(Luojia population)is located at 114o21￠–460￠￠E,30o32￠–327￠￠N,at an altitude of150m. The population covers about200–300m2and is patchy, spreading from roadsides to a forested area.The density of ramets in the population was about250–350m)2and about500–700?owers bloom at the same time.Bisexual ?owers accounted for about93%of the?owers in the populations,and90%of these?owers were robbed once or twice during anthesis(Zhang et al.2007a).Other plants growing within the study population and?owering at same time as G.longituba included Prunus persica (Rosaceae)and Brassica campestris(Brassicaceae). Foraging behaviour of the carpenter bee
To investigate nectar robbing by X.sinensis on G.longi-tuba,experiments were conducted from the beginning of March to late April in each study year.We carefully observed the foraging behaviour of bees of different sexes. We especially selected?ve sunny days during the period of most intense nectar robbing(full bloom)in each year for intensive study of foraging behaviour.Four observa-tion periods of20min each were established on each study day(at09:00,11:00,13:00and15:00),during which we recorded the frequency of nectar robbing on G.longi-tuba(number of robbing visits per20min in1m·1m plots)by male and female bees.In addition,we followed 30male and30female bees and recorded the number of ?owers visited per foraging bout(a single series of repeated visits to the?owers,once per individual bee) and foraging duration on individual?owers.From this we calculated the number of?owers visited by30male and30female bees in1min.In order to prevent pseu-doreplication in data analysis caused by the random?ight of bees,we labelled individual bees by carefully sticking a small piece of feather on to the back of a bee during its visit.Because the handling time of nectar robbers on a single?ower was very short,we used a video camera attached to a laptop computer to improve accuracy. Damage to?oral structures
We observed the damage caused to corollas and other ?oral structures by nectar robbing bees in the four consecutive study years.We collected60–80?owers robbed by female bees and100–150?owers robbed by male bees in each study year,took the?owers to the lab-oratory and counted the number of damaged ovules and nectaries.The?owers were covered2days before the experiment to ensure that they were all virgin?owers and ?rst-time robbed(as fewer?owers robbed by female bees the sample collected was smaller).We also examined ovules and nectaries from100un-robbed?owers visited by legitimate pollinators.
Effect of nectar robbing on?ower life span
In order to explore the effects of nectar robbing by male and female bees on?oral life span,about300?owering ramets were covered with a tent(made of mosquito net and covering an area of2m2)1day before the onset of the experiment.The opened?owers on these ramets were removed.Between09:00to12:00on sunny days,the tent ?y was opened to allow virgin?owers to be subjected to nectar robbing by male and female X.sinensis,but arti?-cially exclude other?oral visitors using an insect net. During the experiment we tagged,by marking the right side of the?owering node,30?owers robbed by female bees and30?owers robbed by male bees.An equal num-ber of un-robbed?owers were selected as a control,and both groups of?owers were excluded arti?cially from fur-ther visitation.We recorded the state of these?owers every2h,except during the night.The end of anthesis was taken to be the time when the corolla began to wilt. This was recorded to assess the impact of nectar robbing on?oral life span.
Effect of nectar robbing on reproductive?tness of G.longi-tuba
In order to explore whether nectar robbing has an effect on reproductive?tness of G.longituba,and differences between nectar robbing by male and female bees,virgin ?owers(bagged2days before the experiment)were exposed to visits by X.sinensis.Only the nectar robber X.sinensis were allowed to visit the?owers,while bees that are legitimate pollinators were arti?cially excluded using an insect net.Immediately after a?ower was robbed,the?ower was picked,put in a bottle with?xa-tive(alcohol:ice-cold acetic acid=3:1)and taken to the laboratory.In each experiment,40–60?owers robbed by female bees and70–80?owers robbed by male bees were collected.We also collected50–60?owers that had been covered by a tent that only allowed visits by legitimate pollinators but excluded the larger-bodied carpenter bees. Since the legitimate pollinators are smaller than the car-penter bees,a tent with a mesh size of14mm was used to exclude carpenter bees.We removed the stigmas from these?owers and observed pollen deposition under a microscope following the methods of Kearns&Inouye (1993),and calculated pollination rate(i.e.percentage of pollinated stigmas)of the?owers.In addition,we marked
Zhang,Zhao,Yang&Gituru Robber bees and Glechoma longituba reproductive success Plant Biologya2009German Botanical Society and The Royal Botanical Society of the Netherlands3
50–60?owers that had been nectar-robbed once by female bees and80–100?owers that had been nectar-robbed once by male bees,as well as80–100un-robbed ?owers.We covered these?owers with a tent(mesh size 14mm)that excluded nectar robbers but allowed legiti-mate pollinators to visit(pilot experiments had shown that the nylon netting had no noticeable effect on visiting behaviour of legitimate pollinators).Fruit set and num-bers of seeds per fruit on these plants were counted after 2weeks.These experiments were repeated three times in 2004,2005and2006.
Foraging ef?ciency and net energy gain
To examine foraging ef?ciency and net energetic gain from male and female bees during nectar robbing,we measured average nectar standing crop(V S)per?ower and nectar concentration in the population of newly opened and un-robbed?owers that had been visited by legitimate pollinators in the morning period on16March 2006.We randomly selected30?owers to measure nectar standing crop before visits by nectar robbers commenced. Nectar was extracted from isolated?owers with calibrated microcapillaries,and put5l l into small vials stored in a box.Nectar production was measured with capillary mic-ropipettes and sugar concentration was determined(in w?w%)using a portable refractometer.Sugar per?ower was calculated using the volume,concentration and a cor-rection factor following the methods of Cruden et al. (1983).
In order to determine nectar availability or net gain nectar quantity(V O)in a?ower after nectar robbing by male and female bees,we measured residual nectar vol-ume(V R)in30?owers immediately after nectar robbing by a male or female bee as
V O?V SàV R
The net energy gain for the nectar robber was calcu-lated using the equation modi?ed from Harder&Cruzan (1990)and Dedej&Delaplane(2004):
N E?I EàO E
where N E is net energy gain,I E is intake energy,and O E is output energy(i.e.the energy spent for?ight activity during discrimination and handling).Then
I E?nSe
where n is mean number of?owers visited during obser-vation time,S is average quantity of sugar ingested from one?ower visited(mg),and e is energy content(J)of 1mg sugar(1mg sugar is equivalent to4.2calories or 17.6J;Schmidt-Nielsen1997).
O E?D EtH E
where D E is energy spent by the bee during discrimina-tion time and H E is energy spent during handling time.
D E?wt d k d
where w is bee mass,t d is discrimination time(total time spent during intermittent?ights to in?orescences(in s), k d is carpenter bee’s mass-speci?c rate of energy expendi-ture during inter-?oral?ight(J?g?s).
H E?wt h k h
where t h is total time(s)spent handling?owers during observations,k h is carpenter bee’s mass-speci?c rate of energy expenditure during handling(J?g)1?s)1).
We determined the rate of energy expenditure per car-penter bee as0.056J?s)1for discrimination(k d),and 0.044J?s)1for handling(k h),based on Dedej&Delaplane (2005).
Data analysis
We used one-way anova to compare the numbers of ?owers visited per foraging bout,foraging duration on a single?ower by male and female bees,number of pollen grains deposited and seeds per fruit.We also used one-way anova to compare residual nectar volumes,rate of damage to ovules and nectaries caused by nectar robbing, pollination rate and fruit set caused by male and female carpenter bees in a single visit,as well as effects of nectar robbing by male and female bees on?oral life span.Dif-ferences in frequency of nectar robbing between insect robbers of different sex and between years were analysed with a two-way anova,with sex of nectar robber as the ?xed factor and study year as the random factor.Percent-age data were arcsine transformed to adjust the variances before analyses.The signi?cance level was set at0.05. All statistical analyses were performed using spss(v.13.0, spss Inc.,Chicago,IL,USA)statistical packages. RESULTS
Carpenter bee foraging behaviour
Our investigation showed that nectar robbing of G.longi-tuba by carpenter bees usually begins in the second week of the?owering season(from early March to mid-April) and reaches a peak(accounting for about20%of total?o-ral visits)along with the peak in https://www.sodocs.net/doc/be17590290.html,monly, X.sinensis starts to visit G.longituba populations and begins nectar robbing at around8:30,and reaches a peak at about11:00,after which visits slow and end after15:00. We did not?nd obvious differences in the time at which the male and female bees appeared,either in a day or within the season in the study populations(Zhang2007). According to our observations,each?ower was robbed once or twice during anthesis.The male bee lands on the corolla,which it grasps with its front legs,it then punc-tures the base of the corolla with its sharp mandibles and removes nectar(Fig.1A).The whole process takes on average2.18s(±1.11,n=30,mean±SE)to complete. Although the corollas of robbed?owers sustain one to
Robber bees and Glechoma longituba reproductive success Zhang,Zhao,Yang&Gituru 4Plant Biologya2009German Botanical Society and The Royal Botanical Society of the Netherlands
two longitudinal tears at the base,damage to the corolla is not extensive and the robbed?ower can still secrete nectar.Visits to the robbed?owers by legitimate pollina-tors continue,albeit at a reduced frequency(also see Zhang et al.2007a).The female bee is considerably hea-vier,and the corolla of G.longituba?owers can hardly sustain its weight;it grasps the corolla tightly and then perforates the base of the corolla with its sharp mandibles to obtain the nectar(Fig.1B).The female bee is rather clumsy,and nectar robbing takes on average7.48s (±2.32,n=30).The handling time on a single?ower for a female bee is longer than for a male bee(F1,58= 350.321,P<0.001).While the male bee typically robs 42.48(±15.24,n=30)?owers and rarely more than120?owers in a single foraging bout,the female bee typically robs only8.81(±6.23,n=30)?owers in a foraging bout before leaving the patch or the population.The difference in number of?owers visited per bout between male and female bees is statistically signi?cant(F1,58=231.797, P<0.001).We also observed that the mean number of ?owers visited per minute by male bees(21.4±7.3, n=30)was signi?cantly higher than that for female bees in a similar period(4.3±4.1,n=30)),and the differ-ence was statistically signi?cant(F1,58=324.521, P<0.001;Table1).
During our4-year study of5days per year,the fre-quency of nectar robbing by male bees was signi?cantly higher than by females(Fig.2;F1,38=105.651,P<0.001).There was a higher frequency of nectar robbing for both male and female bees in the morning(09:00–12:00)than in the afternoon(13:00–15:00).Furthermore,there was a sig-ni?cant difference in the frequencies of nectar robbing among the four observation periods for both males and females(Fig.2A;F3,76=34.357and25.955,P<0.001) and among study years(Fig.2B;F3,16=9.283and5.174, P<0.01and0.05,respectively),but the interaction between sex and year was not signi?cant(F3,36=1.415, P=0.071).
The carpenter bees also visited other plants that were in bloom(including Prunus persica and Brassica campes-tris),where the number of female carpenter bee visits was signi?cantly higher than by male bees(3.2:1,author unpublished data).This phenomenon calls for further investigation.
Damage to?oral structures caused by nectar robbing Nectar robbing whether by male or female bees clearly caused damage to?oral structures,tissues and function. However,an episode of nectar robbing by a female bee in?icts several punctures to the base of the corolla,while that by a male bee causes only one or two such punc-tures.Our results indicated that21.86%(±4.89,n=4)of ovules and16.38%(±5.47,n=4)of nectaries in?ow-ers robbed by female bees had been punctured,compared to 6.69%(±1.81,n=4)and 5.12%(±2.25,n=4)in
A B
Fig.1.Nectar robbing by the carpenter
bee in Glechoma longituba.A:nectar robbing
by a male carpenter bee,and B:nectar
robbing by a female carpenter bee.
https://www.sodocs.net/doc/be17590290.html,parison of parameters of nectar robbing by male and female carpenter bees on Glechoma longituba and its effects on?oral struc-tures and?oral life span(mean±1SE).
handling time in a single
?ower(s)no.of?owers
visited
in1min
no.of?owers
visited in a
foraging bout
ovule damage
rate(%)
nectary damage
rate(%)
?oral life
span(day)
male 2.18(±1.11,n=30)21.4(±7.3,n=30)42.48(±15.24,n=30) 6.69(±1.81,n=4) 5.12(±2.25,n=4) 1.7(±0.35,n=30)a female7.48(±2.32,n=30) 4.3(±4.1,n=30)8.81(±6.23,n=30)21.86(±4.89,n=4)16.38(±5.47,n=4)0.8(±0.53,n=30)b control–––0(n=4)0(n=4) 2.2(±0.36,n=30)c
comparison test F1,58=231.797,
P<0.001
(F1,58=324.521,
P<0.001)
F1,58=350.321,
P<0.001
F1,6=54.276,
P<0.001
F1,6=23.172,
P<0.01
F2,87=15.547,
P<0.01
Different letters represent signi?cant differences.
Zhang,Zhao,Yang&Gituru Robber bees and Glechoma longituba reproductive success Plant Biologya2009German Botanical Society and The Royal Botanical Society of the Netherlands5
?owers robbed by male bees.The differences were statisti-cally signi?cant (F 1,6=54.276,P <0.001and F 1,6=23.172,P <0.01,respectively,Table 1).No damaged ovules were found in the ?owers that had not been robbed.
Effect of nectar robbing on ?ower life span
Nectar robbing had a signi?cant effect on the life span of ?owers (F 2,87=15.547,P <0.01).Subsequent to nectar robbing by a male bee,?oral life span was reduced with respect to that in the control group from 2.2days (±0.36,n =30)to 1.7days (±0.35,n =30)(F 1,58=27.354,P <0.01).Nectar robbing by female bees had an even greater and signi?cant effect on life span of robbed ?owers (0.8±0.53days,n =30;F 1,58=119.033,P <0.001),and ?owers started wilting within 2h after an episode of nectar robbing by a female bee.The reduction in ?oral life span caused by nectar robbing by female carpenter bees was sig-ni?cantly greater than that caused by robbing by male car-penter bees (F 1,58=57.487,P <0.001;Table 1).
Effects of nectar robbing on reproductive ?tness of G.longituba
We found that 19.45%(±3.31,n =4)and 20.51%(±2.59,n =4)of stigmas of ?owers that had been robbed only once by either a male or female bee and not visited
by any other ?oral visitors had pollen grains deposited on them.The difference between pollination rate by male and female bees was not signi?cant (F 1,6=1.224,P >0.05);however,pollination rate by nectar robbers in a single visit were very low compare to open-pollinated ?owers (81.32%±4.87,n =4;F 2,9=46.543,P <0.001).From a sample of 234marked ?owers robbed by the female bee (Fr),389?owers robbed by the male bee (Mr)and 258un-robbed ?owers (Co)pollinated naturally by legitimate pollinators,we recorded fruit set of 34.72%(±5.45,n =4),73.59%(±6.43,n =4)and 79.77%(±6.84,n =4),respectively.The differences in fruit set between the three treatments were signi?cant (F 2,9=78.432,P <0.001;Fr versus Mr:F 1,6=31.953,P <0.001;Fr versus Co:F 1,6=100.272,P <0.001;Mr versus Co:F 1,6=4.631,P <0.05).There was,however,no signi?cant difference in number of seeds per fruit for the three treatments (2.34±1.44,n =81, 2.61±1.22,n =286,2.68±0.97,n =206,respectively;F 2,347=3.698,P >0.05;Table 2).
Foraging ef?ciency and net energy gain
The average nectar standing crop (V S )was 0.25l l (±0.16,n =30)per ?ower and the nectar concentration was 29.2%(±4.3,n =3)in our study populations.Residual nectar volume (V R )in ?owers robbed by a male bee was 0.09l l (±0.04,n =30),while that in ?owers robbed by a female bee was 0.08l l (±0.03,n =30).The net nectar quantity (V O )obtained by male and female bees upon robbing a single ?ower was 0.16l l (±0.03,n =30)and 0.17l l (±0.04,n =30),respectively (Table 3).Thus,in 1min of nectar robbing,intake energy (I E )for the male bee is 17.72J (±3.0,n =30),while that for the female bee is 3.78J (±1.1,n =30).Output energy (O E )for the male bee is 2.43J (±0.7,n =30),while that for the female bee is 2.39J (±0.6,n =30).In general,for the male bee,net energy gain (N E )is 15.29J,while for the female bee it is only 1.39J (Table 3).DISCUSSION
At the population level,nectar is a major determinant of pollinator behaviour,in?uencing the number of pollina-tor visits (Galen 1989;Mitchell 2004)and the length of time a pollinator remains at a ?ower (Klinkhamer et al.2001).Moreover,the size and structure of the ?ower also
Table 2.Reproductive success resulting from a single episode of nectar robbing by either a male or female carpenter bee on Glechoma longituba .
pollination rate (%)
pollen deposition fruit set (%)
seeds per fruit male 19.45%(±3.31,n =4)a 9.61(±3.42,n =59)a 73.59(±6.43,n =4)a 2.61(±1.22,n =286)a female 20.51%(±2.59,n =4)a 17.79(±6.25,n =37)b 34.72(±5.45,n =4)b 2.34(±1.44,n =81)a control
81.32%(±4.87,n =4)b 13.85(±5.68,n =262)c 79.77(±6.84,n =4)c
2.68(±0.97,n =206)a comparison test
F 2,9=46.543,P
<0.001
F 2,355=19.382,P <0.01
F 2,9=78.432,P <0.001
F 2,570=1.336,P
>0.05
Signi?cant difference between two variables is indicated by different superscripts letters (mean ±1SE).
807060male bee female bee
160140120100806040200
504030F r e q u e n c y o f n e c t a r r o b b i n g (t i m e s /20 m i n )
20100
09:00–09:20
11:20
11:00–13:20
13:00–15:20
20032004
20052006
Y ear
Period of day
15:00–
in?uences foraging ef?ciency of?ower visitors,including nectar robbers(Navarro2001;Castro et al.2008,2009; Zhang et al.2009).Furthermore,?oral visitation has been demonstrated to be affected by the effective quality of?o-ral reward,including ease of extracting the reward,which in turn is in?uenced by the morphological‘?t’of pollina-tor and?ower(Inouye1980,1983;Harder1986;Grant& Temeles1992;Temeles1996).This re?ects coevolution between plants and their selected pollinators(Harder1986; Nilsson1988;Morgan&Schoen1997;Zhang et al. 2007b).
Male and female behavioural differentiation:how and why? Sexual dimorphism is a common phenomenon in some insects including X.sinensis(Waser1979;Delph&Lively 1992;Wu2000).The females of X.sinensis are distinctly larger than the males and weigh about30%more. Because the corollas of G.longituba are only just sturdy enough to bear the weight of the female carpenter bee,it takes a longer time for the female bee to complete the nectar robbing process compared to the male bee.The males of X.sinensis are smaller and can easily be sup-ported by the corolla of G.longituba.Thus,male carpen-ter bees have higher foraging ef?ciency compared to females on?owers of G.longituba.
The bene?t–cost hypothesis based on energy trade-offs could explain the phenomena of behaviour differentiation between male and female carpenter bees(Adler&Irwin 2005)and net energy gain from nectar robbing differs between male and female bees.The energy gain that a female carpenter bee obtains from nectar robbing per unit time is only suf?cient to meet the energy payout expected (3.78versus2.39J).Conversely,the energy gain from nec-tar robbing for the male carpenter bee is considerably lar-ger than its payout(17.72versus2.43J)per unit time. Consequently,in terms of energy trade-off,male carpen-ter bees have greater motivation for robbing?owers of G.longituba than female bees.We also found that the vis-iting frequencies of nectar robbers are positively corre-lated with?ower density in different populations(Zhang 2007),further con?rming the energy trade-off in nectar robbing.Earlier research indicated that foraging behav-iour of?oral visitors has undergone coevolution with their target plants(Pyke1978;Alexandersson&Johnson 2002).The present study showed that a female carpenter bee visited only a few?owers of G.longituba before leav-ing a patch,which may indicate that G.longituba does not constitute the main nectar resource for female car-penter bees(see Zhang&Guo2006).
Flowers have unique adaptations that can shed light on the dynamics underlying natural selection(Macior1971; Morgan&Schoen1997;Fenster et al.2006).The pliable corolla,deep corolla tube and low-nectar volume per ?ower of G.longituba all serve to increase the cost of for-aging for the larger female bee,thus causing it to prefer to forage on other species growing in close juxtaposition to the study plants(e.g.Prunus persica and Brassica cam-pestris)that afford the bee higher nectar rewards and have ?owers that are easier for the bee to handle.This differ-entiation in food resource preference by male and female bees is bene?cial to the large-bodied female bee,which requires more food resources(see Zhang&Guo2006). Plants,including G.longituba,that have low volumes of nectar per?ower cannot readily satisfy the energy needs of the larger female bee,which also causes it to resort to simultaneously foraging for nectar.The optimal foraging pattern of male and female bees may constitute a form of ecological niche differentiation(Zhang et al.2007b)that enables visitors to more ef?ciently utilise available?oral resources.
Effects of nectar robbing by male and female bees on plant reproductive?tness
Nectar robbing can in?uence patterns of nectar availabil-ity,and this change may affect?ower attractiveness and in?uence?oral visitor behaviour(Zimmerman&Cook 1985;Irwin&Brody1999;Irwin et al.2001;Maloof 2001;Gonza′lez-Gomez&Valdivia2005).The effects of nectar robbing by carpenter bees on reproductive?tness in G.longituba are complex.The behaviour of the carpen-ter bee leads to destruction of?oral structures,such as the corolla,ovules and nectaries,and shortens?oral lon-gevity.On the other hand,carpenter bees pollinate?ow-ers of G.longtuba while nectar robbing(Zhang et al. 2007a;Table2).The pollination function of X.sinensis is useful in increasing pollen?ow and probably improves male?tness(Zhang et al.2007a),as found in other stud-ies on nectar robbing(Zimmerman&Cook1985;Maloof 2000;Irwin2003;but see Castro et al.2008).However, nectar robbing by the carpenter bee also reduces repro-ductive?tness of the robbed?owers.The present study indicates that although fruit set in G.longituba was reduced after nectar robbing by male carpenter bees,such a reduction was minimal when compared with fruit set
Table3.Nectar and energy transfers in nectar robbing by male and female carpenter bees on Glechoma https://www.sodocs.net/doc/be17590290.html, energy gain equals intake energy minus output energy in a one-minute visitation(mean±1SE).
residual nectar per?ower after one visit(l l)nectar obtained in a visit
to one?ower(l l)
intake energy in a
1-min visitation(J)
output energy in a
1-min visitation(J)
male0.09(±0.04)0.17(±0.04)17.72(±3.0) 2.43(±0.7)
female0.08(±0.03)0.16(±0.03) 3.78(±1.1) 2.39(±0.6)
ANOVA F1,58=0.756,P>0.05F1,58=0.427,P>0.05F1,58=212.365,P<0.001F1,58=1.429,P>0.05 Zhang,Zhao,Yang&Gituru Robber bees and Glechoma longituba reproductive success Plant Biologya2009German Botanical Society and The Royal Botanical Society of the Netherlands7
obtained from open pollination.In contrast,nectar rob-bing by the female bee resulted in a signi?cant reduction in fruit set compared to open pollination.This may be attributed to the fact that?owers robbed by female bees have a shorter life span than those robbed by male bees. This leads to a loss of opportunity for pollination and less ef?cient pollen export for these?owers(see Zhang et al. 2007a).In addition,the higher rate of damage to ovules and nectaries through nectar robbing by female bees com-pared to that by male bees also affects reproductive out-put of the robbed?owers.
The differentiation in food resource preference bet-ween male and female carpenter bees constitutes an optimal resource allocation pattern that enables the visi-tors to more ef?ciently utilise?oral resources in the population.We propose that this is a case of co-adapta-tion between the nectar robber and the plant.Further investigation is required to further elucidate the possible role played by nectar robbing on the evolution of?oral design in G.longituba and in other species subject to nectar robbing.
ACKNOWLEDGEMENTS
We thank Kuo Liao,Lei Chen and Xue-Yi Wang for assistance in the?eld,Zhi-Gang Zhao and Yu Song for assisting in manuscript preparation and data analysis and the anonymous reviewers for their comments and sugges-tions on an earlier version of the manuscript.This work was supported by grants from the National Science Foun-dation of China to YanWen Zhang(30970200)and to Ji-Min Zhao(30970554).
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