Entomological Review, 1980. 59 (4): 58-73

ECOLOGY OF POLLINATION IN STRIGOSELLA

GRANDIFLORA AND ERYSIMUM BADGHYSI

(BRASSICACEAE) BY BEES (HYMENOPTERA,

APOIDEA) IN BADKHYZ: ESTIMATION OF THE

PRESSURE OF COMPETITIVE RELATIONSHIPS

YU.A. PESENKO, V.G. RADCHENKO, AND M.S. KAYGOROOOVA (KAIGOROOOVA)

Although the associated evolution of zoophilous plants and thetr pollinators is beyond doubt, the mechanisms of such evolution remain unexplained in many ways. Possibility of participation of the pollinators themselves in the formation of plant species (and the role of plants in the species fonnation of insects and other pollinators) remains a subject of dis­cussion. An opinion exists, according to which separation on the basis of places of existence and seasonal isolation have a much greater significance in the plant kingdcm for preventing interspecific hybridization than do the pollinators. The pollinators do not playas much a creative role as that of a diSintegrating agent by effecting hybridization among the plants, where it is much more Widely spread than in the animal world, and even beneficial for in­creasing genetic variability and plasticity (Baker, 1951; Anderson, 1953; Stebbins, 1959, 1970).

For successful functioning of the pollinators as an effective factor for disruptive as well as directed selection in species fonnation of the zoophilous plants, besides a whole series of properties which the pollinators must possess (a discussion on these properties has been provided by Pesenko, 1974a, 1974b), an absolutely essential condition is the presence of competition between the plants for pollinators, which is associated with a deficit of the latter. The existence of competition and its pressure in different plants for the pollinators under natural conditions are the main problems which have been poorly studied and form the subject of the present discussion (Levin and Anderson, 1970; Mosquin, 1971; Bobisud and Neuhaus, 1975; Levin, 1972; Straw, 1972; Lack, 1976; Rust and Clement, 1977, Rust, 1977; Stiles, 1977; Parrish and Bazzaz, 1978; Waser, 1978).

The present study is essentially the first attempt to direct estimation of the degree of competition relationships in the system "flowering plants-pollinators . " The main objecti ves of this study is, first, to compare the number of pollinators essential for a high quality of pollination of the supposedly competing plants with their actual population strength, in order to estimate the degree of competition between the plants for the pollinators; and second, to compare the quantity of pollen and nectar with the actual number of plants producing them in order to estimate the load of competition relationships between the pollinators for food sources required ~or the normal maintenance of pollinator populations.

Success in the work is possible by observing the following requirements in relation to the object of study. The plants selected for the study should be: 1) closely related, flowering simultaneously, and growing together; 2) they should have similar composition of pollinators, 3) they should be pollinated not by random visitors, but by specific pollinators, such as bees (superfam ily Apoidea), and 4) they should be predominantly pollinated by the pollinators that are adapted to them (oligot.rophs) or their pollinators should be attracted by other plants in the territory under study only to a small degree.

58 ISSN0013-8738/80/0004-0058$7. 50/ 0 © 1982 Scripta Publishing Co .

SITE, OBJECTS, AND METHODS OF SnJDY

Site. The study of pollination ecology of strigosella grandiflora (Bunge) Botsch. and Erysimum badgbysi (Korsh.) Lipeky ex N. Busch by solitary bees was carried out during the period of blooming of the plants from April 16 to 30, 1978 on the territory of Badkhyz Reserve forests (Southeutern Turkmenia). The area under observation was located 3 km southeast of Kepely cordon lnthe hillocky sem18aV&DD& (with pistachio) part of the forest, in the valley in an area of about 400 x 300 m between small hUls. This 18 a flat and fairly uniform valley in ita soU-pobotanical characteristics, and in the second haU of April it is completely vi~let due to mass flowering of strlgoeella. The vegetation of the valley is ephemeral sedge (Carex pacbystUls, COPl) -meado~ss (Po. bulbosa, COP2) community

with 85% minimum plant coverage. Be.ides strigoaella (CoPl' gr.) and Erysimum (Sp.­

Cop. ), less numerous .pecle. Roemeria refracta and Papaver pavoninum, as well as iso­lated Arnebia decumbena, Eremostachys labioea, Astragalus barrowianua, A. rytUobus and Ixiolirion tataricum bloomed in the valley during the period of observations.

Objects of stu~. The moderately branched shrub S. grandlflora and the herbaceous biennial species E. dgbysi are widely distributed in the foothUls and lower hill regions of T,!rianenla. They are late-spring ephemeroid. and bloom in Badkbyz in the second half of April. str1goeella starts and complete. mus fiowering 3-4 days earlier than Erysimum, and its flowering continues for about 10 day.. The flowen of strlgoaella and Erysimum have typical cruclferous structure. The flowers of strigosella, which are almost half the size of the Erysimum fiowen, are characterized by lilac color of petals, wblch are strongly elongated (4-5 times) over the 3-4 days ~ life of the flower, and turn pale in this process. Th(. flowen are arranged in racemes (in strlgoaella inOorescences are very long, up to 20 cm and more, and they are short in Erysimum), opening of fiowers is from lower side to the upper side. Pr~ causes partial isolation. Like many other typical entomophilous cruciferoua plants (Nieuwhof, 1963; Uoyd, 1965; Free and Nuttal, 1968; Hurka et al., 1976; Belyayeva et al., 1977; Solberlg and Rollins, 1977; Shivanna et al., 1978), Strigosella and Erysimum do not have genetic or embryological seU-incompatlbility, and in the absence of cross pollination they may be self-pollinated after maturation of their own pollen in the flower.

The average number of fiowers on individual plants of Strigosella and Erysimum and the weight of pollen obtained from one flower presented in Table 1 include all the values of 60 random plants of each species on April 20-21, besides the number of flowers given in parentheses, which was obtained during the observations on dynamics during the period Aprll 17-19 on 100 inflorescence of each species. The cruclferous plants investigated differ Significantly in the dally rythm of flower opening and the period of its beginning as well as its termination, and also on the basis of peak flowering: the peak blooming in Strigosella is at 10-l2 hours and in Erysimum at 8-10 hours (Fig. 3). I

Method. The participation of the coauthors in the study was as follows: Yu. A. Pesenko studied the species composition of pollinators, ratio of their abundance and daily dynamics of their flight activity, and compilation of the distribution and population strength of the plants and bees. V. G. Radchenko investigated the bees-the major pollinators-and their nesting behavior. M. S. Kaygorodova carried out the whole complex of studies on the biology of flowering in Strigosella and Erysimum (structure and development of the flower. rhythm of flowering, dynamics of nectar and pollen release, seed setting under isolation bags and without them, and so on), a small part of the results of wbich is included in the present article. All the coauthors participated il) the observations on the behavior of polli­nators on the flows and in chronometeric recording of the speed of their working.

The study of spatial distribution and density of strigosella and Erysimum am their pollinators was carried out within the limits of the experimental area of 80 x 72 m in the northwestern part of the above mentioned valley. Square areas with their sides measuring 0.5, 1 and 2 m and a common northern corner, i. e •• included one in another, were used for sampling. Selection of the area (more precisely. the position of their northern corner) was determined randomly by placing a 1.5 xI. 5 m net with numbered horizontal and vertical lines in the layout plan of the experimental area with the help of the random number table. The number of Erysimum plants and Strigosella stems was counted in 51 x 3 area of the

59

Table 1

Average number of buds and flowers per plant

Esdmation of die number of ... '0 .. Nt-mber of buds Dowen 011 1-o ..

...I. a. Weilbt of polle D .. a. ltd daY' of releued by • Plant specie. J ... J5:" in 100 per OoweriDI per liDlie flower, ml 9 E II Ec: H :; laBONte . plant plant at a zIt i.sta itven moment

SI ri ~osel18 gran- 2.5 2 .6 3287 85.5 11.7 (15.6) 1.0 diflora

55.7 t 3.8 (5.8) 2.5 Erysimum bad- 1.4 2 .1 2652 g hysi

I

three dimensions. Individual plants of Strtgosella forming a bushy growth are difficult to identify and vary greatly in their size and the number of stems, which are characterized by a more constant number of flowers, and are convenient for estimations. The count of polli­nators in each set of three observation areas with a common corner was carried out by counting them on the flowers of Strigosella and Erysimum within a period of 3 min.

"Flower dust" from the alveoli of the bees and pollen breeches of females were weighed on a chemical balance having a precision of * O. 5 mg. It was found impossible to ob­tain the whole quantity of moist pollen collected by the female for the purpose of weighing under field conditions. Therefore, the weight of breech for each bee species was determined on the basis of the difference between the average weight of ''empty'' (without pollen) fresh starved females (the weight of which was surprisingly constant within the limits of error of measurements) and the weight of the heaviest females loaded with pollen (those which have already completed pollen collection). Further in the text, the values are presented pri­marily on the basis of the plant population, number of flowers, number of pollinators, and weight of breeches and "pollen dust"; that is sufficient for a direct and rough comparison. Calculation of the confidence intervals of the desired parameters is difficult because of the difference in the nature of variation of certain variables (for example, plant density) from the normal trend, and in some cases calculation of a fairly narrow (having a rational mean­ing) confidence zone is impossible because of insufficient material (for example, the weight of "pollen dust").

The authors express deep gratitude for cooperation in this work to tbe former Director of the Badhkyz Reserve Forests V. I. Kuznetsov and Deputy Director Kh. Atamuradov; for cons.ultations of botanical nature to the scientist at the forest T. G. Gorelova; to the scien­tists of the Botanical Institute of the USSR Academy of Sciences 1.. E. Rodin, G. S. Malysheva, and B. G. Gannibal; and to A. Z. Osychnyuk, scientist at the lnlltitute of Zoology UDder the Academy of Sciences of the Ukrainian SSR for identification of seven bee species from the genus A ndrena F.

SPECIES COMPOSITION OF THE POLIJNATORS

Lists of pollinators of cruclferous plants are given in ma~ publications and ecologi­cal-faunistic papers on bees. Several investigations were done specially on the study of polUnator fauna of individual cruciferous species, primarily those in cultivation: the culti ­vated mustard (for example, Mukbin, 1977), rapeseed (Lehmann, 1961; Galuszkowa, 1965; Benedek et al., 1972; Wengris, 1973; Pawlikowski, 1978), and other species (Latif et al., 1965; Forster et al., 1973; Mesquida, 1978). At present, information is available on the pollinator composition of at least 50 cruciferous species, on the Dowers of which about 300 species of bees have been recorded, including those adapted for pollination of crucifers. Most of the oUgotropba on crucifers in the Palearctic belong to the genus Andrena F. On the basis of the number of pollinator species adapted, the cruciferOU8 plams, In spite of the simplicity of structure and "openness" of their flower, are inferior to the plants of CompoSitae and Leguminosae.

60

Table 2

Species composition of pollinators of strtgosella (S) and Erysimum (E)

Hum.r of ipect __ collected

Name of the bee tpeclel 8 II: total

t . A "eire". oculHobrl. Mor. « ~. ~ ~ i~' I< .h • 4 ~ 2. A. olbopu"ct.,. Rossi · 4 ~. A. o".'oUco AUk. -4 . A . corbo"orlo L . t6~ . to 3 t9 · to 5. A . cller.o". Warncke - t t Ii. A. aU. lormo.o Mor. iI' 31 d

t 2 7 . A. lu.co.. Erichs. 4.20 34 .330 8. A. I "WoU. Mor. - 4 9. A. mor_U,/ell. Vier. - 2

lu. A. mucoreo Mor. 9 . t20 - 9 · t20 t I . A. or"l/. Mor. t t3 ~ t4 t 2 . A. tro"IItorl. Mor.

If" - 40 t 3. A . lubrrcullue"trl. Mor. 2~

H t4. A. ulr/lfO Mor. -t 5. A "eire". Ip. 2~ 16 . H.lIctu. ,.114% Mor. -17. H. IIIucor.u. Ev. - ~g t8 . H. 9uodrlclllClu. F. - t ~ 19. H . • e"m. Ev . t6 ~ :g t9 g 20. ~"'codet !!po - L'I 21 . Nomodo pectoroll. Mor. 1 g. 6 ~ 22. Nomad. lip. 1 • 1 - 1 ~. 1 23. T.tr.lo,,'a d/.tI/I6u.nd. Mor. -

2 ~ ~~ 5

24 . T. rul/colU. Mor. - 3 25. T .• peetabll/. Mor. - 2 ~ 9 0 26 . rerr.lo,,/o lit 10

1 ~ 8 0 27. Eucer. mela eue. Mor. - 1 ~ 28. E. meto"olloma Mor. - ~~ ~~ 29 . E. n/,r/lacie. Lep. -30 . E . pu.llla Mor. 2~ ~ g. 1 ~ ~ g. 1 ~ 31 . Euctra !p. -.32 . A,,'ltopltoro ra/loulcovtl'/I Fecit. 3~. 10 4 • 2 7 • 3

Total 139~. 64 0 68~. 3S 0 207~. 90 0

Type of tIophlc Ie

ladOlllbi

08 P

08 P

08 ? P ? P

? OB 08 P ? ? ? P P P P P P P P P P P P P P P P P

"'OB-female. of the .peele. collect pollen only from the flowen of crucifelOUl plantl (olilotrophl on Brauicaceae); P-female. of the apeele. collect pollen from the flowen of many plant apeele. (polytrophl).

The 32 bee species observed by us on the fiowers of Strigosella and Erysimum are given in Table 2 together with the number of males and females taken by mass cullections on April 17, 19, and 21, in the areas adjacent to the observation plots. All the observed bees were caught, except Andrena acutilabris Mor., which was predominant in numbers over other species. A total of 297 insects were collected. More massive collections of pollinators were not made, since that would reduce their density and distort the assessment of natural competition load in the "plant-polltnator" system.

All the bee species visiting the flowers of Strigosella and Erysimum are widely distri­buted in Central Asia or in the Ancient Mediterranean. Some of these have still wider a reas of distribution. For example, Andrena carbonaria L. and Halicatus quadricinctus F. a re distributed over almost the whole of the Palearctic. Most of the species are known for the ir trophic relationships with plants. FivEl species of Andrena F. are adapted to cruci­fers, while other bees are polytrophs (Table 2). But on the basis of the number of insects visiting Strtgosella and Erysimum more than half goes to the share of ollgotropbs. Most of the total 32 species are represented by isolated insects or by males (Table 2). and they do not ha ve any great significance in pollination of Strigosella and Erysimum. Among the ommon visiting species may be included Andrena carbonaria L., A. mucorea Mor., A.

oralis Mor., and Helictus senilis Ev.; Andrena acutilabris Mor. and A. tuscoN Erichs. are found in mass. Females of A. acutilabris account for 70.5% of all female bees on the cruci ­fe rous flowers in the estimates recorded on April 20, and 53.7% in the estimates of April 22.

The follOWing differences were noted in the composition of pollinators of Strtgosella and E rysi mum: (1) the fauna of the visitors of Eyrsimum (25 species listed) is richer tha n

61

Table 3

Relative abundance of major pollinators of Strigosella (S) and Erysimum (E)

Fraction of the ~ciea in the e.tlmatiolW , "

Pollinator specie. eatlm . on April 20 , n = 79 ertlm . on April 22, n = 274

S I E I differ. and S I E I d iffe : . and stand . error stand . error

A " dr ena aculilabr/. 51.6 66.7 15.1±10.6 20 .5 41.8 21. 3 ±5.S •

A . Iu I(o.a + A. carbonada 21.9 20.0 t.9±8.6 43 .1 8 .9 34 .2± 8.6 ~

*Differences .ignificant at p ''= O. OS. In counting the bee. In the oblervation areas , the large black A . tuscOla and A. carbonaria were counted together because of diffi ­culty in distingulihing them under field conaltlorw .

that of Strigosella (20 species), but this should be stlll greater, considering half the volume of collections from Erysimum (Table 2); (2) the larger flowers of Eyrsimum, containing more nectar, clearly attract the long-proboscis anthophorids (genera Tetralonia Spin. and Eucera Scop. of the family Anthophoridae) more strongly as compared to strigosella (Table 2); and (3) in spite of some fluctuations in relative abundance of pollinators on cruclferous plants on different days (average collections of April 17, 19, and 21 in Table 2 and estimates of population strength in the observation area on April 20 and 22 in Table 3), there is no doubt about a greater attraction of the Strlgosella flowers for A. fuscosa as compared to the flowers of Eyrsimum, as opposed to A. acutilabris, which constitutes a greater proportion among the pollinators of Erysimum.

Visual observation showed that, besides Visiting Strigosella and Erysimum, the polytroph species A. fuscosa in the area of study also visits the flowers of Roemeria refracta, Papaver pavonimum, Ferula badrakema, and Samaria bulbata. The t1.owers of S. bulbata (Brassicaceae) are also visited by A. acutllabris. The species of Anthophora Latr., Eucera Scop., and Tetralonia Spin., listed in Table 2, are found mainly on the flowers of Eremostachys regeliana and Arnebia decumbens.

BEHAVIOR OF THE MAJOR POLLINATORS ON FWWERS

The female of A. acutUabris, landing on the flowers of Strigosella, . is enclosed within the petals. The flower tUts under the weight of the bee and these two petals are lowered. Catching them by its legs the bee holds on to the lower petals, which are strongly bent to­ward the floral tube in this process. The female bends the lower petals at their baBe with the help of front legs and head, and while pushing itself ahead (upward) by the middle and hind legs, it introduces its head into the corolla tube. If the petals are long (in flowers on the 3rd day of blooming), the hind legs and the bent abdomen also rest on the lower petals; if the petals are shorter, the hind legs and the abdomen of bee rest on the upper dor ­sal part of the corolla tube . While reaching with its proboscis up to the nectaries, which are located at the base of the style and filaments, the bee touches the anthers and the stigma with its head. In this process, the moist pollen sticks to the frons, vertex, and mentum of the female. Sometimes the bee stretches one of its anterior legs (rarely both) deep into the corolla tube and moves them quickly. During the visit of one strigosella flower, it does not change its position, only pulls out its head partly while moving it in dif­ferent directions around the pistil.

The Erysimum flower, during the visitation of a female A. acutilabris, bends a little. The bee does not bend the "lower" petals completely. and bends them only slightly toward the base of the corolla tube. Therefore, it penetrates by its head into the corolla tube not from the side between the base of petals, as in the flower of Strigosella, but from the top, first from the side closer to itself and then pulls out its head completely, crawls further on the flower, and penetrates its head into the corolla tube from the side opposite to itself , or the insect itself moves to the other side of the flower. The anterior legs together with the head are located in the corolla tube, the female holds itself on the "lower " peta ls by the

62

Table 4

Rate of visitation of flowers by major polllnators

Poll! nator species

Average number of flowers viJi12d by the female. In

one min

StrllO'l"lI.' Erysimum 11'",::.'- bald,byol

Arld"",a acut/lobr" to .t 7 .0 A. /u . co.a + A . car- to .7 9.2

bOrlarlIJ

middle and hind legs, and pushes the body foward . During the visit of the Erysimum flower by A. acutilabris, pollen falls not only on the head. but also on the ventral surface of the thorax. A female A. fucosa, on the whole. behaves in the same manner on the Erysimum flower . On the flower of Strigosella this larger bee is not accommodated . and is always compelled to attach itself by the hind legs at the base of corolla tube and enter into it with the help of its bent abdomen.

Thus, the females of Andrena F. do not collect pollen speCially from the cruciferous plants. The pollen falls on the body surface on contact with the polUnator insect at the time of their feeding upon nectar. Transfer of pollen by the brushes of the anterior and middle legs from the head and thorax and accumulation of pollen load on the hind trochante rs, femora and tibia is done by the female insect during movement from one flower to another, in the course of flight and at the time of special halts during flight for feeding as well as be­fore entry into the nest. On the basis of limited observations, A. acutllabris in this pro­cess holds itself by the mandibles on the stem of the plant and works vigorously with all its legs, whlle A. fuscosa attaches itself with a single hind leg and hangs with the head down .

The females spend about 0.5-1 sec in surveying a single flower. and 5-10 sec are re ­quired for feeding on nectar and pollen collection. We wUl deal below only with such "complete" visitations. when the transfer of pollen from the body of the bee to the stigma takes place with a greater probability. Taking into account the time spent on movement from one flower to another and the flights, the pollinators visit. on an average, 8-10 flowers of cruclferous plants per min. More precise observations on the rate of visitation of Strigosellaand Erysimum flower by them, on the basis of the results of chronometrical observations on the major pollinators during 10-16 hours, are presented in Table 4. Visual observations on the major pollinators of the crucifers studied showed that they do not have a tendency for "constant" behaVior, i. e. for visitation by a female only of a single plant species during a single flight, or more so, during whole of its life (results of the analysis on pollen loads supporting these observations are not included in the present arti­c le) •

NEST FORMATION AND NESTING BEHA VIOR

All the bee species recorded on the flowers of Strig08ella and Erysimum make nests in soU. We could locate the nests during the study and describe their structure in Andrena fuscosa and A. mucorea. In these species, nest formaUon was not known previously.

Andrena fuscosa Ericha. bas a unique type of nest formation not reported previously in the bees. All the nests found (5) had efttrance in the deserted burrows of rodents (Fig. 1) I which made them extremely dltftcult to locate. Entry into the bee nest is located above the lateral paths of rodents (which begin8 at the bottom of the burrow) on the vertical wall of the burrow at a depth 01 15-20 em. The main passage to the 70-75 cm long nest extends from the entrance of the nest for a distance of 45-50 em at a level parallel to the soU sur­face, forming an arch, after which it makes a spiral turn and moves downward to a depth of 25 cm. Diameter of the main passage as well as the entry to the nest is 9.8-10.3 mm.

63

S cm

Fig.!. Nest of Andrena fuscosa Erichs.

Its walls are smooth, but not covered with anything or plastered. From the terminal of the main passage, 7-9 lateral paths 3.5-14.5 cm in length and 8. 3-8 .8 mm in diameter originate in all directions. They are also bent accurately and have different inclinations-from almost horizontal to almost vertical.

At the end of each lateral passage, one cell is located, which is slanted downward (angle of inclination in relation to soil surface is 380 ). The cell is of ellipsoid shape, has very smoothly plastered walls, and is covered with oral secretion. Length of the cell is 17.9-19.5 mm, diameter along the horizontal line 9. 2 -10.5 mm, and along the vertical line 8.1-8.3 mm. The cells are located at a depth of 25-37 cm. The uppe r most cells are made first (when the nest was excavated young larvae were already located in them and the lowest ones were still not completed). At the bottom of the cell the spherical pollen ball is located, which is slightly flattened at the poles because of its own weight. The food ball is very derise, only slightly moistened with nectar. The food balls in the nests investigated consisted of pollen from different plants. Relatively minute food balls (size 6 .0-6. 3x 6.8-7.0 mm and weight 135-159 mg) are most probably meant for males (which are smaller than females) and were prepared from the pollen of poppy and Roemeria . The larger food balls (size 6 . 7 x 7.6 mm and weight about 250 mg) consisted of pollen from Strigosella and Erysimum.

The female does not perform the characteristic landing before entry into the nest. Usually it sits on the plants growing nearby and crawls into the nest over them. On emerging from the nest, thE: bee crawls from the rodent burrow, along the plant stems up to the top, and then flies off. It starts collecting food 2 -3 m away from the nest . The flight for food continues for 80-100 min. The female stays in the nest for 15-20 min between food col­lecting flights. After each flight, the female sits on a plant near the nest and carefully cleans the body of the pollen for 4-5 min and forms pollen loads.

The egg is laid on the top on the prepared food ball and touches it by both ends. Afte r egg lay ing, the entry of the cell is sealed with a soil plug, and the lateral passage leading to it is completely covered with soil. The female constructs only one cell at a time and then fi lls it with food. Development of the preimaginal stages most probably takes place quite slowly: in most of the cells opened at the end of the flight of this species (April 23-28) , the eggs were still presem, and only in a few cells (1-2 in each nest) larvae of age group I were found . A kleptoparasite of A. fuscosa is Nomada pectoralis Mor ., which could be found frequently near the rodent burrows.

64

;':I' ~ , . ... ... - ... . - .p.""","' ''''' ;"!r ':~-""''''

." y . .- . .

Fig. 2. Nest of Andrena mucorea Mor-:----

Andrena mucorea Mor. The largest aggregation of nests of this species (consisting of 26 nests) was found on the side of a village road 30 m toward north of the observation area in a small hillock with sparse vegetation over an area of about 1.5 m2• Six nests had entries in the vertical wall of the hillock, which was 40 cm high. Other entries were furnished with a Tumulus. Diameter of the entrance into the nest was 4.9 mm. The main passage was undulate, 70-105 cm long, 5.5 mm in diameter, and extended downward to a depth of 55-60 cm. Lateral decl1nate passages of 9-10 cm length originate from its end. It was not possible to determine the nature of arrangement of the lateral passages, since the peried of opening of the nests (April 27 and 28) was the beginning of molting of this species, and only 1 --2 cells were located in each of the nests (Fig. 2). The cells are of ellipsoidal shape with plastered walls. Length of the cell is 9.7 mm and diameter 5.7 mm. The cells are slanted downward approximately at 30° in relation to the soU surface. The spherical food ball made of Strigosella and Erysimum pollen is located at the bottom of the cell; the females laid eggs on its top and attached them by both ends to the food. The food ball is dense, practically dried, only slightly moistened with nectar.

SPATIAL DISTRIBUTION AND POPULATION STRENGTH OF CRUCIFERS AND THEIR POLUNATORS

Strigosella forms distinct beds of various shape from 1 to 4 meters across. Individual plants of Erysimum grow in isolation, but a comparison of their distribution on the basis of observation plots of all the three sizes wtth the expected (random) frequency by Poisson distribution with the help of X2 showed that the spatlal distribution of Erysimum on the observation plots differs significantly from random distribution at P = 0.01, and is also of aggregate type. Distribution of the pollinators (total of all the species) analyzed by the sarne method was not significantly different from the random distribution at P = 0.05 for the areas of all the three sizes.

In spite of the differences in the nature of spatial distribution of cruciferous plants and their pollinators, the pollinator density depends significanUy on the density of food plants: number of bees recorded in the observation area of 2 x 2 m (on the areas of smaller size, the small volume of material makes it difficult to analyze the results statistically) had a strong linear correlation with the number of food plants, r = + 0.599 (significant at P = = 0.001).

The population strength of crucifers on the observation area was estimated from the results of counts on the areas of 1 x 1 m, since the areas of other dimenalona 18ve lower values (0. 5 x O. 5 m for Erysimum and 2 x 2 m for StrigoseUa, cf. Table 5). Estimation of

65

Table 5

Estimation of population density of Strigosella and Erysimum

Plant species

Strigosella grandiflora: stems

I I Calculation of the ob­Total number of ~Iants.on se rved results for 1 m2 51 obi . areas of dIffer . slles area

I 0.25 m21 I IpoPu. size in

t m2 , m 2 avg . over f 5760 2 1 2 area 0 m , m thouaand

909 3349 4529 65.7 373.4 Number of plants (from Table 1) 370 1340 1810 26.3 151.4 Erysimum badghysi (no. of plants) 4 71 292 1.4 iLl

Table 6

Estimation of the visits of pollinators to Strigosella (S) and Erysimum (E)

Bee spe c ies

rena acutilabris females)

And -(-

A . fuscosa I- A . carbonaria: otal

n umber of females Oth er species:

otal n

To umber of females tal pollinators: atal

n umber of ft! ma les

Number of insec ts recorde d ·)n 51 obse rva t ion are as

of 4 m2

s I E I total

J3 to 43

14 3 17 5 3 8

Ii 2 19 8 2 10

64 15 79 46 15 61

Estimate of momentary pop-I Estimate of ulation strength over an area the number

of 5760 m 2 of females

I ,I lavg. over ri~~~:~;he S E total 1 m2 5760 m2

930 280 1210 0.22 1800

390 90 480 0 .09 -140 90 2:30 0 .04 400

480 60 540 0 .10 -2:.10 60 290 0.05 400

1800 430 2230 0 .41 -IJOO 430 17JO O.JO 2600

pollinator density in the observation area (Table 6) was carried out on the basis of the re ­suits of quantitative estimations in the areas of 2 x 2 m size on April 20. The bee popUla­tion at a given moment in an area should be considered as the number of individual insects simultaneously working on the flowers during the period of the day optimum for their work ­ing (10-17 hours). Estimation of the number of females feeding on the observation plot, necessary for comparison of their requirement for pollen with the existing reserves of pollen on the area, was obtained by increasing the value of momentary pollen count by a fa ctor of 1. 5. Such increase has the following empirical basis: 1) 20% underestimation determined from extrapolation of the r esults of the special experiments conducted earlier (Pesenko, 1972 ), 2) results of observations on the nests and reports in literature showed that during the period of ac tive food collection, the fe males of the nest-forming species spend 1/:3 - 1/4 of their time in the nests.

DAILY RHYTHM OF FLOWERING AND ACTIVITY OF POLLINATORS

During the period of estimations, sunshine reached the observation area only at about 6.50 hours because of the hills surrounding the valley. Only more than an hour later, the first bees appear on the flowers of cruciferous plants-males of A. fuscosa, which mostly spend the night sticking to the Strigosella stems. With the gradual warming of air ( and the surface layer of soil), evaporation of dew and reduction in relative humidity (Fig. 3) , the number of pollinators increases. This increase until noon primarily takes place because of the appearance of the females (see the curve of~~% in Fig. 3), primarily A. acutilabris which forms half of all the pollinators at these hours. Subsequently, the fra ction of females

66

11/

t"c ;1,

22

20

18

I

JOI· ~(I

30

20

:0

c

I'I'~ 100

90

80

70

60

"0 30

20

Fig. 3. Rhythm of flowering in Strigosella and Erysimum and the flying activity of pollinators during the day.

I) Meteorological conditions on April 22: tOe (solid line) - air temperature in shade (shown by ventilated dry thermometer in the psychrometer at the height of 0.7 m above soil surface), G% (broken line) - relative humidity (estimated on the basis of dif­ference between the values of dry and wet bulb thermometers and by using psychrometric tables at the pressure of 100 mb); II) flowering rhythm: fl - average number of flowers open in an hour in 100 inflorescences of 5trigosella (5, broken and dotted line) and ErySimum (E, broken Une) (mean values of the obser­vations recorded on April 17-19), Pol (solid line) - quantity of pollen in open flowers during 1 h (g) taking into account the re­sults of Tables 1 and 5 converted over the area of 80 x 72 m; 1II) dynamics of flight of the pollinators: x - number of bees recorded during 3-min counts on six plots of 2 x 2 m during 1 h on April 22 (1, solid line-all the bees; 2, broken line-Andrena acutilabris; 3, broken and dotted line-A. fuscosa + A. carbo­naria), ~ ~ % (solid line with crosses) -proportion orthe females -- of all the bee species in the estimates, %.

among the pollinators decreases to 42-50%, and only toward the evening, when the major flight of pollinators comes to an end and only a few females of large antophorids continue food collection almost up to sunset (19 hours), their percentage again increases sharply. The most heat-loving insects are A. mucorea and members of the genus Halictus Latr., which begin food collection only at 11 hours when the air temperature attains 220 C.

67

To avoid overcrowding of the curves, the confidence intervals of the mean va lu 5 are not indicated in Fig. 3. We may indicate the confidence interval (at P = 0. 05 ) of peak flowering in Erysimum at 8-10 hours, and at 10-12 hours in Strigosella, and the time dif­ference between them, maximum flight activity of A. acutilabris at 11 - 15 hours , the max i­mum value in A. fuscosa at 13-17 hours and the time difference between them, as well as the optimum period of flight activity of all the bee pollinators recorded in cruciferous plants at 10-17 hours and its peak at 12-16 hours.

The peak flowering in Strigosella and Erysimum is approximately two hours ahead of the maximum flight of their pollinators. Therefore, the corresponding time se ries (quantity of polle .l appearing and total density of all the pollinators in one hour in the day ) were not correlated (r = +0.051). Together with this, the bee population has a direct linear r elation ­ship with air temperature (r = +0.381, significant at P = 0.01) and inverse r elationship with relative humidity (r = -0.438, significant at P = 0.01).

DISC USSION

Estimation of the Pressure of Competitive Relationships

Repeated visitations of the bees are essential for effective pollination of c rucifers. The larger the probability of a flower being visited, the smaller is the intra- and inter ­speCific competition among the plants for the pollinators. Comparisons of the number of Strigosella and Erysimum flowers in the observation area of 5760 m2 (1/3 estimations of momentary population count of the flowers on 1-3rd days of flowering were taken into account, cf. Tables 1 and 5) with the number of flowers which can be visited once during the day by the pollinators present in the area are presented in Table 7. The latter value was calculated by multiplying the momentary population count of pollinators in the area (Table 6) by the average number of flowers visited by a single bee per min (Table 4, somewhat lower values were taken for the pollinators: 10 flowers of Strigosella and 8 flowers of Erysimum ) and by the duration of the main period of daily pollinator activity (10-17 hours, cf. Fig. 3; 7 h = 420 min).

It is important to analyze the three-fold attraction by the Erysimum flowers (on an average, 38.2 visits per flower during the day) as compared to those of Strigosella (12. 8 visits, Table 7). This is related with the higher pollen (Table 1) and nectar productivity of its flowers (results not presented). However, even the probability of Strigosella flowers remaining not visited at all during the day is extremely small. On the basis of random distribution of the visits to the flowers, this probability is equal to:

i.e., on an average, only 3 flowers of Strigosella out of one million will remain unvisited by the pollinators.

Thus, the pollinators were available in more than required quantity in the estimation area of the cruciferous plants in 1978. Each of the flowers was visited, on an average, 14 times during the day (and over 3 d'lVS of the life of each flower, 42 times). Consequently, intra- and interspecific competition for the pollinators is not developed in Strigosella and Erysimum, more so because they have sUghtly different periods of blooming (Strigosella begins and terminates mass flowering 3-4 days before Erysimum) and different daily rhythms of flowering (peak flowering in Erysimum is approximately 2 h ahead of blooming in Strigosella, Fig. 3), and they are also capable of autogamous reproduction. Similar shlfts in the periods and daily rhythm of flowering reduce the possibility of interspecific competition for pollinators, but without additional data they themselves cannot be interpreted as a deVia­tion in different niches as a result of such a competition pressure, which is erroneously done by some authors (Levin and Anderson, 1970; Lack, 1976; Rust, 1977; StUes, 1977; Parrish and Bazzaz, 1978).

Now we may compare the actually existing pollen reserve in the flowers of StrigoseUa and Erysimum produced dally on the experimental area of 80 x 72 m, which was estimated to be 683 g (Table 8, where the number of flowers is given on the basis of Table 6, and quantity of

68

Table 7

Estimation of the average number of visitations by pollinators of a single flower of strlgosella (5) and Erysimum (E)

Parameten (values for the oblervation area of 5760 m2) I S Ie . Total

Momentary population count of polUnaton 1800 430 2230 Number of flo_n visited once by the pollina- 7560 1402 8962

ton durlnlh the day , thouaand . Number of owen opening during the day, 590.3 31J.7 627 .0

thowand Average number of visitations by pollinaton to 12 .8 38 .2 14 .2

a single flower dwing the day

Table 8

Estimation of pollen reserves in flowers of 5trigosella (5) and Erysimum (E)

Parameten s E Total

Number of 9o_n blooming d~y in an area 590.3 36.7 627.0 of 5760 m , thouland

Weight of pollen released by one flower, mg 1.0 2 .5 Weight o~ pollen released daJly in the area of 590.3 92 .8 68:1.1

5760 m by all flowen , g

pollen in a flower on the basis of Table 1), with the quantity of pollen required for the formation of one food ball each by all the females feeding In the observation area (Table 9, designated by M). The females of Andrena F., as a rule, do not fill more than one cell in one day and usually construct only 6-:-12 cells In a period of 15-30 days of foraging activity. Therefore, the weight of pollen 238 g (Table 9) should be considered as the minimum quantity required. It was half of the actual quantity of pollen released by crucifers ( Table 8). Consequently, at least half of the pollen in the Strlgosella and Erysimum flowers on the experimental area remained uncollected (thts is partly confirmed by visual exami­nation of the flowers). Besides, the polytrophic species partly collected pollen from the flowers of other plant species also. For example, more than half of the cells of A. fusc08a opened coptained food balls of the pollen of Roemeria and poppy.

The clearly expressed excessive number of pollinators undoubtedly points toward the absence of a clearly expressed competition between Strigosella and Erysimum for pollinators. A slightly extra volume of pollen reserves in the cruciferous flowers visited by bees over the requirements of the pollinators, taking Into account the approximate nature of assess­ment of the bee denSity, where all their breeches and food balls were used In calculating the required quantity of pollen reserve allowing at least 50% error, in itself cannot prove a weak competition load between the pollinators for food resources. The flowers of crucifers contain a relatively small quantity of pollen (Table 1) and for the formation of a single food ball, depending on the bee species, the entire pollen from dozens or even hundreds of Strigosella or Erysimum flowers is required (Table 9). But a female during a single visit to the flower i,., able to collect only a small part of the total pollen reserve in the flower, since the anthers I.n the flowers of cruciferous plants dehisce at different times and not completely. Therefore, the female should collect pollen from several hundred flowers for making a single food ball, and considering the short visits to the flowers from which the available pollen has already been collected by othnr pollinators, the number of flowers Visited by a single female during a day reaches a few thousands. This number strongly depends on the population of pollinators working Simultaneously.

Table 9

Estimation of pollen requirement of female Bees

Average weight, mg Number of females

Pollinator species breeches females I food balls visiting the M, g

of one with observation female pollen area

A "dre" •• eu,a.brll 4 42 70· 1800 126

A. IUleol. 15 140 250 } 400 84 A. e.rbo"orl. 11 100 170· Other specie. 4 •• 40" 70·· 400 28

Total - - - 2600 238

.Calculated on the basis of extrapolations of the ratlclll of weight of female bee , Its breech, and food ball fer the larva (bued on our own relUlts and reports in literature) , .·Average values .

Increase in the number of flowers visited by bees in search of pollen sharply increases their energy loss for food collection. The energy load of foraging activity is indicated by the observation that the pollinators used the most optimum strategy during the survey of the flowers and inflorescences of different plant species in the selection of the food plant and time (hour of the day) of its food collection activity, as well as the paths and distance of the flights from one plant to another, and also by direct measurement of energy losses (Heinrich and Raven, 1972; Heinrich, 1977; Pyke, 1978a, 1978b). Precise estimation of these losses should be done through special physiological experiments and estimation of nectar reserves in the flowers, the sugars of which serve as the energy "fuel" for the pollinators (the pollen is almost exclUSively used for feeding the larvae). Therefore, the possibility of some competition among the pollinators of Stri.gosella and Erysimum cannot be excluded for the food resources l..nder the Badkhyz even during the period of their maximum abundance in the season.

SUMMARY

Estimation of the load of competitive relationships in the "flowering plant-pollinator" system carried out on two cruciferous plants in one season and at one location, in itself does not permit us to draw a broad conclusion. However, there is reason to believe that the relationships observed by us are typical for the natural conditions in arid and semiarid zones. The entomophilous plants release a much greater quantity of pollen and necta r than is re­quired for attracting the pollinators for a few essential visitations, and ca n "mai ntain" a huge army of pollinators. Therefore, the population strength of entomophilous plants, a s a result of great excess of seed producivity, is usually regulated not by the pollinators, but by other factors (soil-climatic factors, competition for sources of nutrition and energy, etc. ). Competition among the plants for pollinators, and consequently also the possibility of functioning of the pollinators as a factor for selection and species formation in plants are manifested only under extreme ecological-geographic conditions for the pollinators. For example, reports are available about deficit of pollinators in tundra (Hocking, 1968), and in some periods of a season even in the forest zone (Mosquin, 1971). Unfavorable ecologi­cal conditions for pollinators can appear sporadically even in other zones.

The bees are characterized by unlimited area of nest formation, small number of eggs laid by each female and a well developed effort toward progeny care, leading to a minimal mortality at preimaginal stages. These properties ensure a relative stability of population strength of bees. The main factor in its regulation is the magnitude of polle n and nectar reserves available to meet the energy losses in their collection. The competition load for food resources has already been indicated for the pollinators of certain plants (for example, Linsley and Cazier, 1970; Morse, 1977).

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70

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71

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BOBISUD, L.E., and R.J. NEUHAUS. 1975. Pollinator constancy and survival of rare species. Oecologla, 21(3): 263-272. •

FORESTER, I. W., P. G. CLINCH, and T. PALMER-JONES. 1973. Observationa on the pollination of chou moellter (Brassies oleracea L.). New Zealand J. Exp. Agric., 1( 1): 46-48.

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HEINRICH, B., and P. H. RA YEN. 1972. Energetics and pollination ecology. Science, 176(4035): 597-602.

HOCKING, B. 1968. Insect-flower associations in the high Arctic with special reference to nectar. Oikos, 19(2): 359-387.

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72

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Zoological Institute, USSR Academy of Sciences, Leningrad; Institute of Zoology, Ukrainian Academy

of Sciences, Kiev; Natural Sciences Institute, Perm State Universit.y

73