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Pollen sources for Apis mellifera L (Hym, Apidae) inSurinam, based on pollen grain volume estimates

Jc Biesmeijer, B Van Marwiik, K Van Deursen, W Punt, Mj Sommeijer

To cite this version:Jc Biesmeijer, B Van Marwiik, K Van Deursen, W Punt, Mj Sommeijer. Pollen sources for Apismellifera L (Hym, Apidae) in Surinam, based on pollen grain volume estimates. Apidologie, SpringerVerlag, 1992, 23 (3), pp.245-256. <hal-00890991>

Original article

Pollen sources for Apis mellifera L (Hym, Apidae)in Surinam, based on pollen grain volume estimates

JC Biesmeijer B van Marwiik K van DeursenW Punt MJ Sommeijer

1 Utrecht University, Laboratory of Comparative Physiology, PO Box 80086, 3508 TB Utrecht;2 Utrecht University, Laboratory of Palaeobotany and Palynology,

Heidelberglaan 2, 3584 SC Utrecht, The Netherlands

(Received 4 November 1991; accepted 19 March 1992)

Summary &mdash; Every 3 or 4 days over a 1-year period, pollen samples were taken from Apis mellife-ra hives in Surinam in order to identify pollen sources, and to determine how these sources variedduring the year. The second aim of this study was to compare the results of pollen counts with rela-tive volume estimates. Each sample contained up to 15 pollen types. On the basis of relative volumeestimates in combination with frequency, we found that the most important year-round pollen sourc-es were Cecropia sp, Palmae type 1, Cocos nucifera, and Compositae type 1. Pollen types thatwere periodically important included Ceiba pentandra, Myrtaceae type 1, Abutilon type, Spondiasmombin, and Terminalia sp. Up till now the importance of pollen sources has been measured direct-ly by counting pollen grains. In this paper we show that such data do not reveal the actual impor-tance of these sources for the bees. Data from the volume estimates show a much more diverse beediet during the year as well as on a single day than that shown by the pollen counts.

pollen analysis / pollen grain volume / pollen plant / neotropics

INTRODUCTION

For honeybees pollen is the only sourceof protein and lipids (Stanley and Linsk-ens, 1974). Like other eusocial bees,honeybees are polylectic, eg they use dif-ferent plant species. Bees constantly haveto make a choice between the availablefood sources. Their choice is determined

by the abundance and the relative qualityof the source, distance of the source fromthe hive, and by the previous experience

of individual bees (Seeley, 1985; Seeleyet al, 1991).

Food sources of bees can be studied

indirectly by analysing the pollen and nec-tar collected by the bees. Information onflower-visiting by European and African

honeybees in the neotropics is available

only for São Paulo, Brazil (Cortopassi-Laurino and Ramalho, 1988; Imperatriz-Fonseca et al, 1989), Panama (Roubik etal, 1986), Trinidad (Sommeijer et al, 1983)and French Guiana (Roubik, 1979). Al-

though Engel and Dingemans-Bakels(1980) identified the sources of pollen col-lected by stingless bees in Surinam, ourstudy is the first to examine pollen collect-ing by honeybees in the Guianas.

In this paper we also investigate the im-portance of specific pollen sources. Theimportance of a source is determined bythe quality and the quantity of the pollen.Little is known about the nutritive value ofvarious tropical pollens, how bees extractthe pollen contents, or whether they canbreak down pollen grains selectively (Stan-ley and Linskens, 1974; Kroon et al, 1974;Cruz-Landim, 1985). The importance ofdifferent plant species is normally deter-mined by counting the pollen grains (seethe review on neotropical honeybees andstingless bees; Ramalho et al, 1990). Thediversity and the variation of source utiliza-tion throughout the year is normallydemonstrated by calculating pollen nichesize and evenness (Ramalho et al, 1985;Cortopassi-Laurino and Ramalho, 1988).

In determining the importance of thesource directly from pollen grain counts, itis assumed that the quality and the volumeof every single pollen grain are equal. As aresult the conclusion is reached that abun-dant pollen types are more important forthe bees than sporadically observed types.

The size of pollen grains, however, var-ies widely. The diameter of European pol-lens, for example, ranges approximatelyfrom 5 to 200 &mu;m (Stanley and Linskens,1974). In a study of the relations betweenstingless bees and palms in Panama, Rou-bik and Moreno (1990) found that in 9 spe-cies of palms the length of the palm pollengrains ranged from 38 to 142 &mu;m. Theystated that as the palm pollen grains wererelatively large in size, simple counts of

grains did not reflect the relative represen-tation in bee diets.

The present study was designed to: i)identify the important pollen sources used

by African honeybees in Surinam; ii), in-

vestigate the diversity and the variation ofpollen sources during the year; iii) com-pare the results of pollen counts with rela-tive volume estimates.

MATERIAL AND METHODS

Pollen samples were taken from 2 Apis melliferaL hives. One hive was sampled from 31 May1986 to 8 January 1987, the other from 9 Janu-ary to 31 May 1987. Sampling was performedusing a pollen collecting trap. From 31 May to20 August 1986 a 24-h pollen harvest was col-lected every 3 or 4 days. From 20 August 1986to 31 May 1987 the trap remained in place andpollen was collected twice a week.

Both colonies were located on the farm of Kvan Deursen in the Bomapolder, SSE of Para-maribo, 55° 5’N 5° 45’W (Surinam, South Ameri-ca). The area around the farm consists of culti-vated land (planted with Cocos nucifera,Psidium guajava, Carica papaya, Citrus spp)and on which is also found swamp and stretch-es of forest (containing Pterocarpus sp, Ceibapentandra and Triplaris guianensis).

Samples were processed by a standard ace-tolysis method (Reitsma, 1969) and analysed atthe Laboratory of Palaeobotany and Palynologyof Utrecht University.

Pollen types were identified using the refer-ence slide collection of the palynological insti-tute. This collection was built up from earlierstudies (Engel and Dingemans, 1980; Sommeij-er et al, 1983; Bootsma et al, 1988). The relativerepresentation of pollen types in each samplewas estimated by random counting of 200 pollengrains (on 2 slides).

The volume of each pollen type was estimat-ed by measuring dimensions, and calculatedvolume by mathematical formulae.

For some pollen grains which did not matchgeometric figures, volume was estimated as wellas possible. Obtained volume was divided bythat of pollen grains of Cecropia sp (the smallestpollen type found) which gives the relative vol-ume used in this paper. The absolute volumecannot be given, because this approach canlead to size modifications (Reitsma, 1969). Therelative volume, however, can be estimated ade-quately.

To investigate the impact of the methodologi-cal differences on parameters derived from

pollen counts and volume estimates, the pollenniche size and the evenness of source use werecalculated. These parameters are regularly usedto indicate the diversity of pollen sources andthe utilization of these sources during the year.

The pollen niche size, H’, is expressed by theShannon-Weaver diversity index (1949):

where ph = proportion of pollen from plant spe-cies h visited in the month in question.

The evenness index J’ was calculated ac-

cording to Pielou (1977) :

where H’max = natural logarithm of the total num-ber of pollen types present in the samples. J’therefore varies from 0 (heterogeneous utiliza-tion of sources) to 1 (homogeneous utilization ofsources).

To compare the results of grain counts withthe results of volume estimates, H’ and J’ werecalculated using the results of both methods.

RESULTS

Spectrum of pollen sources

Ninety-two pollen samples were analysed;these were found to contain 52 different

pollen types, 21 of which occurred in over10% of the samples (table I). Six typescould be identified at species level, 17 atgenus level, and 21 at family level. Eighttypes remained unidentified. Twenty-ninefamilies were represented in the samples.The number of pollen types per sampleranged from 1 to 15, the average being8.1. The pollen sources can be divided into4 groups as shown below.

Very important year-roundpollen sources

Cecropia sp, Palmae type 1, Cocos nucife-ra and Compositae type 1 were present inmore than 75% of the samples, and madeup the bulk of the volume and grains dur-ing the sampling period. On average, 62%of the volume and 84% of the total numberof grains consisted of 2 species only: Ce-cropia sp (average volume per sample36%; 68% of the grains counted) and Pal-mae (26%; 16%).

Important year-round pollen sources

Myrtaceae type 1, Spondias mombin,Graminae type 1 were present in approxi-mately half the samples spread more orless equally over the year.

Periodically important pollen sources

Piperaceae type 1, Ceiba pentandra,Abutilon type, Onagraceae type 1, Termi-nalia sp, Tapirira guianensis, Malpighia-ceae type were present in less than 30%of the samples, but were important pollensources during short periods. A striking ex-ample in this group is Ceiba pentandra,which was found in 13% of the samplesonly from 2 March to 15 May during whichtime it made up more than 40% of the pol-len volume.

Minor pollen sources

This group includes all other speciespresent in less than 30% of the samples,many occurring only occasionally. Most ofthese species normally did not exceed the5% level per sample.

Comparison of methods

The results of the 2 methods show consid-erable differences (figs 1 and 2). Small-sized pollen grains (Cecropia sp, Pipera-ceae type 1, Myrtaceae type 1, Terminaliasp) dominate the pollen counts (fig 1).Here Cecropia sp is by far the most impor-tant pollen source and is fairly constantthroughout the year (except for April andMarch). According to the pollen counts (fig1), only a few plant species are importantpollen sources and the variation in the pol-len spectrum is very low.

Data for the volume estimates (fig 2),however, reveal a different pattern in theuse of pollen sources by the honeybees.Cecropia sp and Palmae type 1 are equal-ly important pollen sources. Cecropia sp isnot a constantly dominating source as itwas in the pollen counts, but has 2 periodsof importance (July-October; December-February) and is almost completely absentduring the rest of the year.

Many other species that have relativelylarge pollen grains (eg Ceiba pentandra,Abutilon type, Cocos nucifera, Palmae sp)have much higher values in the volume es-

timates (fig 2), and should therefore beconsidered to be more important pollensources than is suggested by the pollengrain counts (fig 1). In general, the varia-tion in important pollen sources during acertain period is higher in the volume cal-culation method than with the pollen graincount method.

Monthly pollen niche size and evennessare given in figures 3 and 4 for bothmethods. Pollen counts for both niche sizeand evenness are highest in April and low-est in August, September and January.Pollen volume measurements, however,show a more regular pattern. Noteworthyis the fact that overall values for niche sizeas well as for evenness are somewhat

higher with pollen volume measurementsthan with pollen counts.

DISCUSSION

Spectrum of pollen sources

Although the pollen spectrum of Apis mel-lifera observed in this study is the onlyrecord for Surinam, these data can be

compared with other studies carried out intropical America (table I). A considerablepart of the flora of Surinam also occurs inthe other Guianas (Guyana and FrenchGuiana) and on Trinidad. Therefore the re-sults obtained by Roubik (1979) (FrenchGuiana), Sommeijer et al (1983) (Trinidad)seem to be the most suitable ones for

comparison. Plant communities in other

parts of tropical and subtropical Americaare very different, so studies from Panama(Roubik et al, 1986) and São Paulo, Brazil(Cortopassi-Laurino and Ramalho, 1988;Imperatriz-Fonseca et al, 1989) only showoverlap at the genus and family level.

In this study Cecropia sp Palmae type 1and Cocos nucifera were found to be themost important pollen sources for honey-bees throughout the year in Surinam.These types are also major pollen sourcesin other countries (table I). Momordica cha-rantia has been previously reported as afood source for honeybees in Trinidad aswell as for stingless bees in Surinam. Thehogplum, Spondias mombin, a major pol-len source in Surinam, was also found tobe important for honeybees (and other

bees) in Trinidad. Ceiba pentandra, whichwas found to be of major importance in Su-rinam from March to mid-May, was not re-ported to be a pollen source of honeybeesin the above-mentioned studies.

There is a considerable overlap (3 spe-cies, 5 genera, 23 families) in the pollenspectrum of stingless bees (Melipona andTrigona; Engel and Dingemans-Bakels,1980) and honeybees in Surinam, butnone of the plant taxa constitutes a major

pollen source for both groups. Overlap atfamily-level does not imply that the 2 beegroups use the same species. However,because of the different methods utilized

and the lack of information on plant spe-cies occurring at the localities involved, wecannot conclude that these bees do notshare major pollen sources.

Comparison of methods

The present study

The differences in the results yielded bythe 2 methods require careful study.

Up till now all studies on food sources ofhoneybees and stingless bees in the neo-

tropics have used pollen grain counts to de-termine the importance of the sources. It isclear that for bees, the pollen volume is farmore important than the number of grains.As mentioned above, this creates a problemfor the investigator because the grains ofthe various types of pollen collected by thebees differ considerably in diameter, result-ing in even larger variations in volume.

The pollen diet of honeybees in Suri-nam on a single day and during the year ismore diverse according to volume esti-mates than it is according to pollen counts.Several plant species are important pollensources in volume estimates, but are notrevealed as such by pollen counts.

Calculations based solely on pollencounts are also misleading. As can be con-cluded from our results (figs 3, 4), there isconsiderable difference in the monthlyniche size and evenness, as revealed bythe 2 methods. On average the graphsrepresenting the relative volume data showhigher values, indicating a higher diversityof plant species used as pollen sources

and a more homogeneous use of pollensources than one would conclude from pol-len counts. The analysis, based on the rel-ative volume data, does not give pro-nounced peaks for diversity and evennessduring specific periods of the year. Analy-sis based exclusively on the pollen counts,however, indicates that such peaks do ex-ist.

Other studies

It is clear that the shortcomings of the pol-len count method have an impact on theevaluation of the results of other studies.

The actual effect depends on the size

ranges of the recorded pollen types. Forhoneybee foragers, Cortopassi-Laurinoand Ramalho (1988) found pollen grainsranging in length from approximately 10-71 &mu;m. They considered Eucalyptus spp,Cecropia sp and Mimosa veloziana to beamong the most frequently-visited plantspecies. However, the published photo-graphs indicate that the pollen grains of all3 species are relatively small. Other stud-ies also record important sources of pollenwith small grains, for example: Cecropia sp(Sommeijer et al, 1983).

CONCLUSION

It is concluded that results of pollen graincounts alone cannot be presented and in-terpreted directly as patterns of pollensource utilization. Volume is a better meas-

ure, although a precise estimate can

sometimes constitute a problem. It is also

preferable to use relative volume datarather than pollen counts for calculatingniche size, evenness, niche overlap andother parameters.

NOTE

During the processing of this manuscript, an ar-ticle on the influence of pollen grain volume waspublished by FA da Silveira (1991). Cecropia spalso happened to be the smallest grain found inthe latter study. The present authors support themain conclusions reached in that article.

ACKNOWLEDGMENTS

We thank H Velthuis and 2 anonymous review-ers for making useful suggestions concerningthe manuscript and S McNab for linguistic im-provements.

Résumé &mdash; Les sources de pollen pourApis mellifera L au Surinam, estiméesd’après le volume des grains de pollen.Les informations sur les sources de nourri-ture des abeilles dans les régions néotro-picales sont très éparses (revue récentepar Ramalho et al, 1990) et cette étude estla première sur ce sujet concernant le Sur-inam. Notre premier objectif était d’identi-fier les sources de pollen d’Apis melliferaet d’étudier leur variation au cours de

l’année. Le second but était l’étude de l’im-

portance relative des sources spécifiquesde pollen. Jusqu’à présent, l’importancedes sources de pollen était mesurée direc-tement en comptant les grains de pollen*.Il est clair, néanmoins, que pour les

abeilles le volume des grains de pollen estbeaucoup plus important que leur nombre.C’est pourquoi les comptages ne rendentpas compte de l’importance réelle de cessources pour les abeilles. Nous avons misau point une méthode d’estimation du vo-lume relatif des grains de pollen afin dedéterminer leur importance relative. Les

résultats des 2 méthodes (comptage desgrains et estimation du volume) ont étécomparés.

Tous les 3 ou 4 j pendant toute uneannée (mai 1986-mai 1987) des échan-tillons de pollen ont été prelevés dans 92ruches d’A mellifera au Surinam et traités

par une méthode standard d’acétolyse(Reitsma, 1969). Le volume a été estiméet le volume relatif calculé par rapport àcelui des grains de pollen de Cecropia sp(le plus petit type de pollen trouvé). Cha-que échantillon comprenait jusqu’à 15

types de pollen. Au total 52 types ont ététrouvés, dont 21 étaient présents dansplus de 10% des échantillons (tableau I).D’après les estimations de volume relatifcombinées à la fréquence, les sources depollen les plus importantes tout au long del’année sont: Cecropia sp, les Palmae type1, Cocos nucifera et les Compositae type1. Les types de pollen très épisodiquescomprennent : Ceiba pentandra, les Myrta-ceae type 1, le type Abutilon, Spondiasmombin, Terminalia sp.

Les résultats des comptages et des esti-mations de volume présentent des diffé-rences considérables. Les données prove-nant des estimations de volume indiquentpour les abeilles un régime beaucoup plusdiversifié que les comptages, aussi biendurant l’année qu’au cours d’une journée.Nous en concluons que les comptages depollen ne peuvent pas être considéréscomme reflet direct de l’utilisation dessources de pollen. Le volume est une me-sure meilleure, bien que son estimation

précise puisse poser des problèmes.

* Pendant la publication du présent article,un autre travail de FA de Silveira sur l’in-

fluence du volume des grains de pollen adonné lieu à une publication (1991). Lesplus petits grains de pollen de cette étudefurent aussi ceux d’une espèce de Cecro-pia. Les auteurs du présent article souscri-vent aux principales conclusions de FA deSilveira.

analyse pollinique / volume du grain depollen / plante pollinifère / région néo-tropicale

Zusammenfassung &mdash; Die Pollenquellenfür Apis mellifera L (Hym, Apidae) in

Surinam, bestimmt durch Schätzungdes Volumens der Pollenkörner. Infor-

mationen über die Nahrungsquellen der

Bienen in den Neotropen sind sehr unvoll-ständig (zum letzten Mal zusammengefa&szlig;tdurch Ramalho, 1990) und dies ist dieerste Untersuchung über Nahrungsquellenfür Bienen in Surinam. Unser erstes Zielwar die Bestimmung der Pollenquellen vonApis mellifera und die Untersuchung derVariation dieser Quellen das Jahr über.

Unser zweites Ziel bestand darin, die rela-tive Bedeutung von bestimmten Pollen-

quellen zu untersuchen. Bisher wurde dieBedeutung der Pollenquellen direkt durchZählung der Pollenquellen gemessen*. Esist jedoch klar, da&szlig; für die Bienen das Vo-lumen der Pollenkörner weit wichtiger ist

als ihre Zahl. Deshalb geben diese Zahlennicht die wirkliche Bedeutung dieser Quel-len für die Bienen wieder. Wir entwickelten

eine Methode zur Schätzung des relativenVolumens von Pollenkörnern, um ihre rela-tive Bedeutung zu bestimmen. Die Resul-tate von den üblicherweise benutzten Pol-

lenzählungen und unserer Methode der

Schätzung des relativen Volumens wurdenverglichen.

Alle drei Tage wurden über ein vollesJahr (Mai 1986-Mai 1987) von Völkern vonApis mellifera in Surinam Pollenprobenentnommen (insgesamt 92) und nach einerStandard-Azetolysemethode behandelt

(Reitsma, 1969). Das Volumen der Körnerwurde geschätzt und das relative Volumenim Vergleich zu den Pollenkörnern von Ce-cropia sp (dem kleinsten vorhandenen Pol-lentyp) berechnet. Jede Probe enthielt biszu 15 Pollentypen. Insgesamt wurden 52

Pollentypen gefunden, von denen 21 in

mehr als 10% der Proben auftraten (Tabel-le I). Auf der Grundlage der relativen Volu-menschätzungen in Kombination mit der

Häufigkeit wurden als wichtigste Pollen-

quelle das ganze Jahr über Cecropia sp,Palmen-Typ 1, Cocos nucifera und Kom-

positen Typ 1 bestimmt. Pollenformen von

gro&szlig;er Bedeutung zu bestimmten Perio-den waren Ceiba pentandra, MyrtaceaeTyp 1, Abutilon Typ, Spondias mombin,Terminalia sp.

Die Ergebnisse der Pollenzählungenund der Volumenschätzungen zeigten be-trächtliche Unterschiede. Die Daten der

Volumenschätzungen zeigen viel grö&szlig;ereUnterschiede in der Bienennahrung überdas Jahr wie auch über einen einzelnen

Tag als die Pollenzählungen. Wir

schlie&szlig;en daraus, da&szlig; die Ergebnisse derPollenzählungen nicht unmittelbar als Mus-ter der Nutzung von Pollenquellen darges-tellt werden können. Das Volumen ist ein

besseres Ma&szlig;, obwohl seine SchätzungProbleme bieten kann.

* Inzwischen wurde ein Artikel von FA daSilveira veröffentlicht (1991). Wir bestäti-gen die wichtigsten Schluss-folgerungen.

Pollenanalyse / Pollenvolumen / Schätz-verfahren / Pollenpflanze / Neotropen

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