proc. lndian acad. sci. (plant so.), vol. 99, no. 3, june

Proc. lndian Acad. Sci. (Plant SO.), Vol. 99, No. 3, June 1989, pp. 223-239. �9 Printed in India.

Poi l ina t ion ecology of Z i z y p h u s m a u r i t i a n a ( R h a m n a c e a e )

K RAMA DEVI, J B ATLURI and C SUBBA REDDI* Department of Botany, *Department of Environmental Sciences, Andhra University, Waltair 530 003, India

MS received 26 September 1988; revised 6 April 1989

Abstraet. At Visakhapatnam (17~176 Zizyphus mauritiana Lam. blooms twice a y e a r , once during September-January (first season) and again during March-June (second season). The ftowers are compatible to geitono and xeno pollen. They are strongly protandrous and pass through distinct developmental stages. While the first 2 flowers of umbel are invariably complete, the succeeding ones either develop up to the male stage or continue through the female. The flowers in the 2 stages are more numerous in the first season than in the second. They decrease as the seasons progress. Two plant types occur. In one, the flowers anthese at 0600 h (early) and in the other at 1000 h (late). The stigrnas of the late type receive pollen in the latter half of their receptive period, first from the early and then from the both. Those of the early type receive pollen of the late type in the beginning of recepUve pefiod, and in the last quarter first from the early and then of the both. A population with only one plant type has the stigmas receiving pollen in the last quarter of their receptive period. Pollen in the male stage and nectar in the female constitute the reward to the insect visitors that included bees, wasps, flies, ants and butterflies. The former 3 groups proved to be effeeting pollination, among which Apis florea, Ceratina sp., Trioona sp, Ropalidia spatulata, Chrysomya megacephala and Sarcophaga sp. are the major pollinators.

Keywords. Zizyphu~,, pollination; pollen flow; bees; wasps; flies.

1. Introduction

Zizyphus species possess typical fly-flowers (Knuth 1906). The flowers of Z. jujube (Chinese date) are protandrous, the male and the female phase each lasting f o r a day (Thomas 1924), and are pollinated by a big clumsy wasp (Eumenes tinctor) in Timbuctu (Hagerup 1932). Ackerman (1960) recorded honey bees, house flies and lady beetles foraging at these flowers but only the former effected cross-poUination yielding viable seed. The tlowers of Z. spina-christi exhibit protandry and xenogamy and pass through 6 distinct phases (A-F), with B--C representing the male and D-E the female phase (Galil and Zeroni 1967). Further, 2 kinds of trees occur which are staggered with respect to their time of anthesis. Teaotia and Chauhan (1963a, b), Singh et al (1970), and Chundawat et al (1979) studied the floral biology of some varieties of Z. mauritiana. They found that the flowers are protandrous, xenogamous, anthese synchronously on the entire crown of a tree, the anthers dehisce after 3 h and the stigma matures after 24 h; they are visited by Apis species and Musca domestica; the latter was more responsible for more pollen transfer. The present study on Z. mauritiana assessed the pollination potential of bees, wasps, ants, flies and butterflies that were found visiting the flowers, treated the pollination system in the light of contemporary ecological considerations and brought to light more of the features of the mechanism that determines the pollen flow patterns within and between the early and late anthesing plants.

223

224 K Rama Devi, J B Atluri and C Subba Reddi

2. Materials and methods

Zizyphus mauritiana Lam., the Indian jujube or 'ber', is both cultivated and wild. The present study was carried out using 14 trees in the orchard at Isakathota, 3 on the Andhra University campus and 2 at Ramnagar--all the 3 sites are located at Visakhapatnam (17~176 The dates of first, peak and last flowering of these plants were noted through weekly observations during 1983.

Different phenological events of a flower were recorded through observing continuously the marked mature flower buds in the initial, peak and final phases of flowering. Pollen grain number per anther was determined by placing an undehisced anther on a microscope slide in a drop of lactophenol aniline-blue and squashing it with the point of a needle. The resultant pollen mass spread into a uniform narrow band was scanned for pollen. Counts were made of grains from 25 anthers collected from different trees. Pollen-ovule ratios were computed following Cruden (1977). Both in vitro and in vivo techniques were used to determine the pollen viability pe¡ (Stanley and Linskens 1974; Kirby and Stanley 1976). To find out the stigma receptivity period, batches of virgin flowers previously emasculated were pollinated with fresh pollen at predetermined intervals for 2 days. The bagged flowers were then followed for a week to observe fruit set.

Certain branches of the trees in peak bloom were enclosed with insect proof covers, then nectar volumes were measured with a calibrated micropipette at regular intervals. Nectar sugar concentrations in per cent were read on a refractometer. Paper chromatography, with butanol-acetone-water (4: 5 : 1) solvent system, was used to analyse nectar for sugar composition (Harborne 1973). Amino acid content was estimated using Baker and Baker's (1973) method. The development of greenish blue colour on applying bromo-phenol-blue to the dried nectar spots on a filter paper indicated protein presence. To ascertain the prevalent mode(s) of reproduction, hand-pollinations were made, besides testing for apomixis.

An examination of the specimens of anthophilous insects whose identity was confirmed by the Commonwealth !nstitute of Entomology, London, UK, enabled the naming of flower foragers. Censuses of visitors were made thrice, one each for the 3 phases of flowe¡ Attention was focussed on certain flowers, their visitors were counted for 30 min in every hour from dawn to dusk. The number of flowers visited in unit time (min) and the length of time (s) spent at a flower were assessed for those species that were frequent. To ascertain insects potential to pick-up pollen, they were caught at the flowers and their body washings in alcohol were observed for pollen. Further, intrafloral behaviour including mode of approach, type of forage collected and contact of essential organs was noted.

3. Results

3.1 Floral dynamics

3.1a Blooming phenology: The plants bloom twice a y e a r , once during mid September-January [95-130 ( i= 115) days, with a peak pe¡ of 30-45 (~=38) days], and again during mid March-June [66-98 (~ = 83) days, with a peak period of 10-29 (~= 18) days]. The former, being the longer period, might be regarded physiologically the first flowering season and the latter the second (Ewusie 1980).

Pollination ecology of Z. mauritiana 225

Although the 19 individual trees under study differed slightly in the duration of their flowering, the first season at the population level started at about the 3rd week of September, reached its peak between the 3rd week of October and the 1st week of December and ceased virtually by the end of June. Seven out of the 19 plants observed did not have the second flowering. The others initiated the second flowering at about the middle of March, progressed to a peak between April 2nd week and May 1st week and ceased to flower by the end of June.

3.1b Inflorescence phenolo9y: Each leaf axil of the newly formed branches bears an umbel, whose flowers open centripetally. In the first season, all flower buds opened fully while in the second nearly 50% aborted. Both seasons' inflorescences were in flower for 8-11 days. The time course and intensity of flower production in an umbel suggested that the seasons were identical in the pattern of daily flower production, but the first season produeed a larger flower crop. The number of flowers produeed on the first day was high, low on the seeond, increased to a peak between the 4th and 7th day and then declined gradually.

Du¡ the first season, umbel number increased as the blooming progressed from the initial to peak, but flower number per umbel deereased; both numbers decreased in the final phase. The number of flowers produeed per umbel in the initial, peak and final phases were respectively 14-20 (~=18), 11-20 (~=16) and 9-16 (~=12). During the second season, flower n¨ did not vary much with the flowering phase and it ranged from 6--15 (~=9).

3.1c Anthesis: In 10 of the 19 plants observed, anthesis occurred at 0600 h and in the rest at 1000 h. Those having early anthesis are named the 'early type' and the late anthesing ones the 'late type' (Galil and Zeroni 1967). Very distinct stages of development occurred in the tlower life of the 2 plant types (figure 1). The chronology of their occurrence observed on fine weather days in the first season is given in table 1. In the second season the onset of each stage was 30 min ahead of

(A) (B) (C) (D)

( [ ) (F) (G) (H)

Figure 1. F!ower showing different anthr phasr in Z. mauritiana.


Table 1. The chronology of different stages of flower devetopment in Z. mauritiana.

Time (h)

Early type Late type Stage of flower development

0600 1000 0730 11~

0730--0800 1130-1200 0900-1000 1300-1400 1030-1040 1430-1440 1130-1200 1530

1300 1700 1400 1730

1430 1800 1500 2000

Sepals begin to unfold (figure lA) Stamens convergent, enclosed by the petals; anther dehiscence occurs (figure 1B) Petals start unfolding (figure IC) Anthesis is complete, petals move away from the centre (figure ID) Stamens in erect position (figure lE) Gynoecium projects out a little with the stigma slightly bifid (figure 1F) Stamens start diverging towards periphery Stamens fully diverged, resting on petals; gynoecium still growing (figure IF) Gynoecium fully developed with the stigma receptive (figure 1G) Petals completely reflexed along with the stamens (figure 1H)

these times. At the individual tree and population level, all the flowers that opened on a particular day were almost in the same stage of development.

3.1d Flower sex: The flowers are bisexual, the sexes being separated in time. The first 8"5 h of the flower life is devoted to the male stage and the remaining to the female in both flower types. All the flowers do not exhibit the 2 sexual stages. The first 2 flowers of umbel invariably end in the female stage, those produced then onwards may either halt with the male or continue to the female stage, the former event being more common. The number of flowers that pass through the female stage varied with the time of flowering in each season (figure 2). In both early and late types, the ratio of male to female gradually increased as the flowering progressed. Thus in the first season, the P/O ratios were 7248:1 (early), 9046:1 (late) in the initial, 13569:1 (early), 20354:1 (late) peak and 37577:1 (early and late) final phase. A similar trend occurred in the second season also, but the respective ratios were always larger.

3.le Pollen characters: Pollen grains are small (29/zm), sticky, with a faintly reticulate exine. Their number per anther varied between 950 and 1050 (~=980). About 10% of them are ste¡ On gentle tapping of the flower, the dispersal units contained each 150-200 grains. Both in vivo and in vitro tests demonstrated that the grains remain viable for 48 h after anther dehiscence.

3.1f Stigma receptivity: The stigrna appeared turgid, viscid and shiny at the time the male stage ceased. In the early type, the male stage terminated by 1400 h, in the late type by 1730 h on the day of flower opening. The stigma matured and remained receptive for another 24 h in both flower types in the first season; after that they turned black. In the second season also the'early type stigma behaved in the same way, but the late type was receptive for only 18 h. Based on the results of hand- pollinations, these observations were confirmed. Of course, the rate of fruit set decreased with the progress of the receptive pe¡

3.1g Nectar characters: Nectar is secreted only in the female stage. Each flower secreted on average 2.5 q The dominant sugar is glucose, with sucrose and fructose


60

50

�91

30

20

10

F I r s t season 70X

I I I

I I J I I J l l J I I J I I I

, / 1 50 F f s 1 1 1 I I I I I I

F i l / J I r ~ J

f J I

/ / J ~ f i J

1 i / f / J f f /

. . o f f J f i l f / J sll oo, I 1 1 30

[ / I . . . l i / ~ 1 1 . . , /fj r11.., fjj r r . . . . . . i!! f l s r J ~ 20 fil f/~

r ~ ~ x z / / 10 1 / / XXX f / 1 r / 1 1 I I I f i l i i / lJJ XXX f i l f f t ~ / / ~ p . . . . .

A B

Second season

p ~ ~ I N I T I A L PHASE

~r PHAS~

I ~ ~ F I N A L PHASe

A !i

Figure 2. Per cent flowers ending in female stage in Z. mauritiana at different phases of flowering in the two seasons. (A) Early type; (B) late type.

in traces. Sugar concentration is 30%. The histidine score is zero which is equivalent to 7-58 #g/mi of amino acid content. Proteins are present.

3.1h Breeding behaviour. The results of hand-pollinations (table 2) show that both geitonogamous and xenogamous pollinations produce seeds and fruits in this taxon. However, both flower types are not equally successful, the early type produced more fruit through geitonogamy than the late type. The crosses between the early and late types yielded more fruit than the intratype ones. Apomixis and autogamy are absent.

3.1i Natural fruit set: Fruit set varied with the season, it being larger in the first season than in the second. Overall fruit set was smaller in the late type flowers than in the early type. Fruit set also varied with the flowering phase, it being more in the initial phase and decreasing through the season. This trend occurred in the 2 seasons (tables 3, 4).

3.2 Flower visitor activity dynamics

3.2a Composition offlower visitors: During the study period, a total of 20 insect species (Hymenoptera 12; Diptera 4; Lepidoptera 4) was caught without bias to the flower type (table 5). Five of these foraged on nectar and pollen, the others on nectar only. The 20 species were not common to the 2 seasons, 3 study sites and 2 flower types (tables 6--9).

3.2b Relative abundance of visitors: The variety of insects encountered and the visits they made were more numerous in the first season than in the second. Of the


Table 2. Results of breeding experiments pefformed in the first season.

Treatment

No. of No. of Fruit Seed flowers flowers set set

pollinated set fruit (%) (%)

Apomixis Early I00 0 0 0 Late 75 0 0 0

Autogamy Early 100 0 0 0 Late I00 0 0 0

Geitonogamy Early 250 116 46 100 Late 120 20 17 100

Xenogamy c~ Q

Early x Early 150 54 36 100 Early x Late 200 135 68 100 Late x Early 200 173 87 100 Late x Late 180 60 33 100

Table 3. Natural fruit set rates in both flower type in different flowering phases in the first season.

Flower type

No. of Average Total flowers Fruit set in Fruit set in No. of No. of developed No. of relation to relation to the

Flowering flowers/ flowers to female flowers total flowers with phase umbel sampled stage set fruit flowers % female stage %

Eady

Late

Initial 18 500 328 208 42 63 Peak 16 500 179 101 20 56 Final 14 500 60 24 5 40


Table 4. Natural fruit set rates in both flower type in different flowering phases in the second season.

Flower type

No. oŸ Average Total flowers Fruit set in Fruit set in No. of No. of developed No. of relation to relation to the

Flowering flowers/ flowers to female flowers total flowers with phase umbel sampled stage set fruit flowers % female stage %

Early

Late



Poll inat ion ecology o f Z . mauri t iana

Table 5. Floral visitors of Z. mauritiana and their forage type.

Visitor type Forage type

Diptera

Sareophagidae Sarcophaqa sp. Nectar

Calliphoridae Chrysomya megacephala Neetar and pollen

Muscidae Musca domestica Nectar

Bombyliidae Ligyra sphinx Nectar

Hyrnenoptera Apidae

Apis florea Potlen and nectar Apis cerana indica "" Tri#ona sp. "

Anthophoridae Ceratina sp. "'

Sphecidae Chalybion sp. Nectar Bembix sp. " Sphex sp. "

Vespidae Ropalidia spatulata "

Eumenidae Delta pyriformis '"

Scolidae Campsomeris sp. "

Formieidae Oecophylla samara#dina " Camponotus sp. ' '

Lepidoptera Papilionidae

Papilio polytes romulus " Phalantha phalantha "

Danaidae Euploea core ""

Lycaenidae Castalius rosimon "

229

different insect groups recognised, the bees preponderated on the 2 flower types, at the 3 study sites and in the 2 seasons (tables 6--9). The percentage of their visits varied between 52 and 95 of the total visits. The second dominant group was the flies which shared 7-34%, followr by the wasps which cont¡ 4-29*/0 of the total visits. The ant and butterfly visits were insignificant. Within each season, the visits of different insect groups varied with the flowering phase, the peak phase receiving the larger number of visits. Between the initial and t'mal phases, visits of some insects were more in the former and of some in the latter. The dominant forager was not one and the same on all the 19 plants observed. I t was either of the 6 species which included Apis f lorea, Cerat ina sp., Trigona sp. among the bees,

bo

Tab

le 6

. In

sect

vis

itor

s ce

nsus

on

earl

y ty

pe f

low

ers

in d

iffe

rent

flo

wer

ing

phas

es i

n th

e fi

rst

seas

on.

o Is

akat

hota

U

nive

rsit

y ca

mp

us

Ram

nag

ar

lnse

ct

Init

ial

Pea

k F

inal

In

itia

l P

eak

Fin

al

Init

ial

Pea

k F

inal

Ant

s Cam

pono

tus

sp.

5 11

9

9 16

8

7 14

9

Oec

ophy

lla

sam

arag

dina

4

6 3

2 5

6 0

5 2

Was

ps

Cha

lybi

on s

p.

! 9

57

6 17

16

6

18

51

1 I

Rop

alid

ia s

patu

lata

32

90

5

11

16

1 20

33

12

B

embi

x sp

. 15

24

0

0 4

0 0

20

0 Sp

hex

sp,

0 3

0 0

0 0

0 10

0

Bee

s Api

sflo

rea

288

515

221

50

96

24

110

256

92

Api

s ce

rana

ind

ica

81

94

31

3 I 1

2

24

54

17

Cer

atin

a sp

. 83

10

8 46

19

27

8

98

138

85

Trig

ona

sp.

99

196

59

28

31

I 1

74

96

69

Fli

es

Sarc

opha

ga s

p.

118

192

49

23

22

4 81

12

2 44

C

hrys

omya

meg

acep

hala

30

7 29

9 ! I

0 44

45

13

58

93

14

M

usca

dom

esti

ca

16

28

2 1

3 0

54

106

28

But

terf

lies

P

apil

io p

olyt

es r

omul

us

4 9

6 0

8 0

0 5

0 P

hala

ntha

pha

lant

ha

0 4

0 0

0 0

0 3

0 E

uplo

ea c

ore

3 5

0 0

0 0

0 0

0 C

asta

lius

ros

imon

5

5 3

0 4

0 0

3 0

o~

2.

r,,q

q~

Tot

al v

isit

s 10

79

1646

55

0 20

7 30

4 83

54

4 19

09

383

3275

59

4 28

36

lsak

atho

ta

: ln

itia

l 17

.10.

1983

P

r 20

.11.

1983

F

inal

18

.12.

1983

U

nive

rsit

y ea

mp

us

: In

itia

l 15

.10.

1983

P

eak

14.1

1.19

83

Fin

al

13.1

2.19

83

Ram

nag

ar

�9

lnit

ial

20.1

0.19

83

Pea

k 24

.11.

1983

F

inal

31

.12.

1983


Talfle 7. Insect visitors census on early type flowers in different flowering phases in the second season.

lsakathota Ramnagar

Insect Initial Peak Final Initial Peak Final

Ants Camponotus sp. 1 0 0 0 Oecophylla samaragdina 0 0 0 0

Wasps Ropalidia spatilata 82 212 28 67 Chalybion sp. 0 26 0 67

Bees Apisflorea 87 175 27 19 Apis cerana indica 0 126 0 33 C~atina sp. 93 144 16 27 Trigona sp. 0 60 23 30

Flies Sarcophaga sp. 0 40 17 0 Chrysomya megacephala 14 0 0 24 Musca domestica 18 0 0 0

Butterflies

Euploea core 0 5 0 0

Total visits 295 788 111 267 1194

8 0 3 0

57 22 24 0

182 34 99 0

134 28 156 26

15 13 0 0

24 0

0 0

702 123 1092

Isakathota : Initial 3.4.1983 Peak 2.5.1983 Final 7.6.1983 Ramnagar : Initial 5.4.1983 Peak 28.4.1983 Final 30.5.1983

Chrysomya megacephala and Sarcophaqa sp. among the flies, and Ropalidia spatulata among the wasps.

3.2c Diurnal actioity ofinsectforagers at theflowers: On the early type flowers, the activity of flies began at 0600 h, increased rather suddenly to a peak at 0900 h, then declined rather suddenly up to 1200 h, and then stayr at a low ebb till 1800 h when it ceased. Bees also made their appearance from 0600, their visits gradually increased and stayed at the high level between 0900-1100 h, then decreased rather suddenly the next hour, and gradually up to 1800 h. The wasp activity was evident from 0700, abruptly rose from 0800 h to a peak at 1000, then declined suddenly up to 1200, and stayed at a low level till 1800 h.

On the late type also, the flies became active at 0600 h. Their frequency increased gradually to a peak at 1100 h and fell suddr the next hour. The activity resurged slightly at 1400 and then decreased gradually up to 1800 h. Bee activity commenced at 0600 h, kept on increasing graduaUy to a maximum at 1300 h, then decreased rather suddenly and ceased at 1800 h. Wasps, though, commenced their activity by 0600, their visits were very few up to 1000 h, then increased gradually to a peak at 1300 h, from then on the activity fell suddenly and ceased at 1700 h.

3.2d Relative mobility of insect visitors: Based on the number of flowers visited in unit time (min) and the length of time (s) the visitors spent at the flowers (table 10),

Tab

le 8

. ln

sect

vis

itor

s ce

nsus

on

late

typ

e fl

ower

s in

dil

lcre

at f

low

erin

g ph

ases

in

the

firs

t se

ason

.

L,O

I-

O

Isak

atho

ta

Uni

vers

ity

cam

pu

s R

amn

agar

Inse

ct

Init

ial

Pea

k F

inal

In

itia

l P

eak

Fin

al

[nid

al

Pea

k F

inal

g~

Ant

s Cam

pono

tus

sp.

8 11

5

9 16

13

6

18

10

Oec

ophy

lla s

amar

agdi

na

0 1

0 0

2 I

0 3

1

Was

ps

Cha

lybi

on s

p.

4 5

11

0 0

0 4

6 2

Rop

alid

ia s

patu

lata

5

13

8 0

0 0

6 2

5 B

embi

x sp

. 5

44

23

0 0

0 15

31

0

Sphe

x sp

. 0

1 0

0 0

0 0

1 0

Bee

s Api

sflo

rea

273

483

135

20

42

2 18

8 28

3 98

A

pis

cera

na i

ndic

a 31

14

2 5

0 0

0 56

89

11

C

erat

ina

sp.

210

212

161

26

41

8 10

2 23

1 59

Tr

ioon

a sp

. 26

3 28

4 15

2 40

53

13

83

19

8 43

Fli

es

Sarc

opha

•a

sp.

39

176

23

1 1

0 22

36

17

C

hrys

omya

meo

acep

hala

65

26

7 35

9

9 5

38

45

28

Mus

ca d

omes

tica

1 31

5

0 2

0 14

22

I I

Tot

al v

isit

s 90

4 16

70

563

104

156

42

534

965

285

3137

30

2 17

84

t...

e-v

g~

q3"

g~

lsak

atho

ta

Uni

vers

ity

cam

pu

s R

amn

agar

: In

itia

l 17

.10.

1983

P

eak

20.1

1.19

83

Fin

al

18.1

2.19

83

: ln

itia

l 15

.10.

1983

P

eak

14.1

1.19

83

Fin

al

28.1

2.19

83

: In

itia

l 20

.10.

1983

P

eak

24.1

1.19

83

Fin

al

31.1

2.19

83

Tab

le 9

. ln

sect

vis

itor

s ce

nsus

on

late

typ

e fl

ower

s in

dif

fere

nt f

low

erin

g ph

ases

in

the

seco

nd s

easo

n.

, ,

~,

,,

lsak

atho

ta

Uni

vers

ity

cam

pus

Ram

naga

r

�9 In

sect

ln

itia

l P

eak

Fin

al

Init

ial

Pea

k F

inal

ln

itia

l P

eak

Fin

al

g~

Ant

s

Cam

pono

tus

sp.

Was

ps

Rop

alid

ia s

patu

tata

C

haly

bion

sp.

Bee

s Api

s flo

rea

Api

s ce

rana

indi

ca

Cer

alin

a sp

. Tr

iqon

a sp

.

Fij

es

Chr

ysom

ya m

eoac

epha

la

Mus

ca d

omes

tica

Sarc

opha

ga s

p.

Tot

al v

isits

0 7

0 5

0 0

0 3

0

84

82

18

0 0

0 68

79

31

0

0 0

0 0

0 0

0 17

77

112

30

0 0

O

63

94

27

0 95

0

0 0

0 61

75

29

31

74

0

31

144

19

0 82

26

38

12

4 27

11

8 19

5 16

94

97

38

18

0 0

0 0

0 0

33

0 0

0 0

0 0

0 28

23

0

0 0

0 0

29

0 18

25

0

248

494

75

149

368

35

332

511

168

817

552

10~1

f% N

e,,

lsak

atho

ta

Uni

vers

ity

cam

pus

Ram

naga

r

: ln

itia

i 3.

4.19

83

Pea

k 2.

5.19

83

Fin

al 7

.6.1

983

: ln

itia

l 15

.4.1

983

Pea

k 4.

5.19

83

Fin

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11.6

.198

3 :

Init

ial

5.4.

1983

P

eak

28.4

.198

3 F

inal

30.

5.19

83


Table 10. Number of flowers visited per unit time and the length of time spent at flowers in male and female stages of Z. mauritiana by va¡ floral visitors.

Length of time spent Length of time spent at No. of flowers at flowers in male stage flowers in female stage visited/minute (s) (s)

lnsect name n R ~ SD n R ~ SD n R ~ SD

Apisflorea 10 6--7 15 3.479 5 3-5 3"5 0"866 5 2-5 3 1'225 Apis cerana indica 10 6-12 10 1:969 5 3-5 5.0 0-894 5 3-5 5 0.894 Ceratina sp. 10 15-18 17 0"994 5 3-5 4.0 1.000 5 3-5 4 1.000 Trigona sp. 10 9-15 11 2-066 5 3-5 4-0 1.000 5 1-4 4 0-447 Bembix sp. 10 25-33 30 2.644 5 1-2 1-0 0.447 5 1-2 1 0-447 Sarcophaga sp. 10 10-24 21 4-243 5 2-4 3.4 0-894 5 2-4 3 0"866 Chrysomya megace- lO 10-19 17 2.404 5 2-3 2-0 0"447 5 2-3 2 0-447

phala Musca domestica 10 7-13 10 2-751 5 3-5 4-0 1.000 5 3-5 5 0"894 Ropalidia spatulata 10 2-10 6 2.846 5 3-4 3-0 0-707 5 3-3"5 3 0-224 Chalybion sp. 10 21-26 24 1"633 5 2-4 2.0 0-894 5 2-3 2.5 0-500 Sphex sp. 10 15-20 18 1-524 5 3-5 4-0 1.000 5 2-5 4 1"224 Papilio polytes romulus 10 18-21 19 0.942 5 3-7 5.5 1.500 5 4--6 5.5 0"866 Phalantha phalantha 10 10-13 13 0.949 5 2-4 3"3 0-837 5 3-4 3 ff671

n, Number of samples; R, range; i, average.

Bembix sp. proved to be the most mobile, followed by Chalybion sp., Sarcopha#a sp., Papilio polytes romulus, Sphex sp., Ceratina sp., C. megacephala, Apis florea, Phalantha phalantha, Tri#ona sp., Apis cerana indica, Musca domestica and R. spatulata in that order. There was no appreciable difference in the length of time the visitors spent at the male and the female stages of flowers.

3.2e lntraspecific and interspecific interactions: Among the flies, C. megacephala was found to chase Sarcophaga sp., which usually flew away, but it sometimes resisted. Among the bees, there were practically no interactions. Individuals of R. spatulata pushed each other aside. The ants, particularly Oecophylla samaragdina drove away all other insects. Flies as a group drove away the bees, and the bees drove away the wasps.

3.2f Mode of approach to the flowers: A majo¡ of the flower visitors landed on the leaves and then crawled towards the umbel, after foraging they again crawled a short distance and then flew from one leaf to the next on the same branchlet or to the leaf of the next branchlet. Trigona sp. and Ceratina sp. alighted directly on the umbel and then flew to another.

3.2g Body washings offlower visitors: Of the visitors studied, Trigona sp. bore the most pollen on its body, to be followed by A. florea, A. c. indica, Ceratina sp., C. megacephala, R. spatulata, Chalybion sp., Sarcophaga sp., Bembix sp., and M. domestica (table 11). Body washings of ants did not reveal any pollen grains.

3.2h Predators of pollinators: Spiders (Peucetia viridana), lizards and preying mantids were found to be the main predators. They used a 'sit and wait' stratcgy at the inflorescences to catch the prey. Spiders captured mostly the fijes, rarely the

Pollination ecology of Z. mauritiana

Table !1. Pollen pick-up by various foragers on Z. muuritiaml assessed through body washings.

Insect name n R ~ SD

Apisflorea 5 325q522 488 121 Apis cerana indica 5 216-501 344 106 Ceratina sp. 5 52-148 95 37 Trigona sp. 5 232-998 581 299 Bembix sp. 5 4-18 8 7 Sarcophaga sp. 5 8-36 20 11 Chrysomya megacephala 5 20-52 34 13 Musca domestica 5 2-14 8 5 Chalybion sp. 5 3-58 26 25 Ropalidia spatulata 5 17~68 32 21

n, No. of samples; R, range in pollen grain numbers encountered in body washings; L average.

235

bees, while the other groups preyed on both. The wasps did not form the prey, for their movement was rapid.

4. Discussion

4.1 Breeding system

It has been known since the time of Darwin (1876) that nature favours cross- pollination. Most bisexual plants achieve this through either structural modification of flowers or differential maturation of sexual organs or self-incompatibility. Z. mauritiana is geared to achieve cross-pollination through a combination of self- incompatibility (in the sense that the flowers are not autogamous) and dichogamy with strong protandry. A similar mechanism was reported in Discaria toumatou, also of Rhamnaceae (Webb 1985). Further, the synchrony in flower development at both individual plant and population level, and the creation of 'early' and 'late' anthesing plants contribute a lot to the promotion of xenogamy and the attendant genetic variability. The extra care taken in the form of dichogamy to prevent auto pollination might be to avoid wastage of pollen and stigma sites through unwanted 'nonsense' poUination which is ineffective (Pijl 1978). As against the observation of Teaotia and Chauhan (1963b) that a solitary tree cannot set fruit, the authors observed fruit in such trees which should have resulted from geitonogamous pollinations. Because of prolonged receptivity, the stigmas receive pollen from the flowers of the same plant that bloom the next day.

4.2 Pollen flow directions

The data on daily anthesis, pollen presentation and stigma receptive periods, behaviour of flower visitors, enabled to depict the probable directions of pollen flow in a population consisting of the early and late type plants (figure 3). In both types pollen is presented for 6.5 h, from 0730-1400 h in the early type, from 1100-1730 h in the late type. The stigmas of both flower types remain receptive for 24 h from


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Figure 3. Pollen flow directions in Z. mauritiana. (E) Early type; (L) late type.

1400-1400 h, thus receptivity spreading partly over 2 consecutive days. Al1 the recorded flower visitors are day active, hence mediate pollen flow du¡ daylight hours. As such, though the stigmas ate receptive during light and dark hours, no pollen flows during dark hours (1830--0600).

Du¡ daylight hours, the late type stigmas receive pollen in the latter half of their receptive period, first the early type pollen for 3"5 h and then pollen of both types for 3 h. On the other hand, those of early type receive pollen in the first and last quarter of their receptive period. In the beginning pollen of the late type is available for 3 h. In the first half of last quarter the stigmas receive pollen of the early type for 3-5 h and then of the both for 3 h and finally of the late type for 30 ruin. It is thus clear that if the population consists of only one plant type, pollen reception is possible only in the last quarter of the stigma receptive period. Therefore, keeping in view the decrease of fruit set with the progress of stigma receptive pe¡ it is suggested that for an orchard to yield more fruit it should consist of both early and late anthesing plants.

4.3 Pollinators

The flowers of Z. mauritiana are promiscuous and received foraging visits from bees, flies, wasps, ants and butterflies. The reward to the visitors is linked with the sex stage of flowers, the male offering pollen and the female providing nectar. To be a successful pollinator the visitor should cover both flower stages. The bees exploited both resources by making intentional visits to both flower stages, and therefore could be the successful pollinators of this taxon.

Wasps feed on nectar but not pollen (Proctor and Yeo 1972; Faegri and Pijl 1979). Interestingly, the wasps visited both sexual stages. While discussing the


pollination zystem of Cylicomorpha, Jacaratia, Jarilla, Carica, in which only the staminate plants provide a reward while the pistillate are visited and pollinated by 'mistake', Baker (1976) suggested that such 'mistake pollination' may prove to be a widespread phenomenon where flower visitors with low powers of disc¡ are encouraged. It is likely that the wasps failed to discriminate the 2 flower stages and so visited the male stage flowers anticipating the same reward they get from the female stage. The visits of wasps may also be interpreted in the light of the 'bonanza and blank' hypothesis proposed by Feinsinger (1978). When a population of a particular plant species has some flowers with considerable amounts of nectar (bonanzas) dispersed among many flowers with little or no nectar (blanks) a bonanza-blank pollination reward schedule results. Ir the pollinator responds to this variability by visiting many flowers, then a bonanza-blank distribution may be an adaptation promoting gene flow. The wasps under consideration responded to the variability in nectar secretion between the male and the female stages and promoted cross-pollination.

Flies formed an important group of pollinators of Z. mauritiana. Of these, C. megacephala foraged for both nectar and pollen, and the others for nectar only (table 5). However, the 4 species recorded, paid visits to both flower stages. Probably, the nectar-feeding flies having little discriminatory power visited the flowers in male stage like the wasps by 'mistake'. Short tounged flies characteristically visit open flowers with well exposed nectar (Proctor and Yeo 1972). The nectar sugar concentration range preferred by these flies is generaUy considerably higher than that at which the nectar is secreted by the nectary and therefore, ideal fly flowers are expected to produce nectar in small aliquots (many small flowers), and as the nectary is freely exposed post secretory evaporation causes nectar to be concentrated (Corbet 1978). Z. mauritiana flowers exhibit these traits and may be regarded as typical fly flowers (Knuth 1906).

Ants are implicated in the pollination of certain plant species (Faegri and Pijl 1979). But those under study bore no pollen on their bodies and seldom contacted the stigmas. However, they being bellicose indirectly caused increased flow of geitono and xeno pollen through their interaction with other insects which being scared of ants moved more often from umbel to umbel, branch to branch and tree to tree. The butterflies confined to the flowers in female stage. Occasionally, they visited the male stage ones by 'mistake' but their mouthparts seldom touched the anthers. Hence, here they are visitors only.

4.4 Major and rainor pollinators

The data relating to the frequency of flower visitors, the number of flowers visited in unit time, the amount of pollen picked in their visits, helped to distinguish the pollinators as major and minor ones (Baker et al. 1971). Accordingly, the bees A. florea, Ceratina sp., Trigona sp., the flies C. megacephala, Sarcophaga sp., and the wasp R. spatulata could be the major pollinators and the remaining the minor ones in the first season. The fly species were less frequent in the second season. A. c. indica, noted for its efticacy a s a pollinator (Mehrotra 1983), was found to be efficient in picking up pollen and is relatively more mobile. However, its frequency was very low in the first season but relatively high in the second, and is therefore of significance in that seagon.


Insect species proved to be the major pollinators might not be so throughout the distributional range of Z. mauritiana. It is because these insects vary in their abundance from site to site, and the variation could be retated to the variation in habitat factors, which in turn cause variation in the availability of nesting sites for bees and wasps, breeding sites for flies, and their food plants. Tropical environments are known for their heterogeneity at the micro-level (Ashton 1969), and the reproductive success of this taxon, in spite of the conservative breeding system, is assured by the promiscuity of flowers which are visited and pollinated by diverse insects. Thus different bee, wasps and fly species assume different degrees of importance at different localities depending on their availability.

4.5 Pollination management

In India, the hive bee A. c. indica is usually recommended for managing pollination. It is doubtful that this bee could concentrate and be conditioned on Z. mauritiana flowers which secrete nectar in traces. The study" proved that the flies C. megacephala, M. domestica and Sarcophaga sp., can pollinate this taxon effectively. These could be managed easily for achieving maximum pollination. A suitable habitat for their survival, breeding and proliferation can be created near the orchards through providing moisture, dung and decaying organic matter. The little bee A. florea, if managed, could also be an effective pollinator.

Acknowledgement

The authors are thankful to Prof. R W Cruden, Department of Botany, University of Iowa, Iowa, USA for helpful suggestions.

References

Ackerman W L 1960 Flowering, pollination, sclf-fertility and seed development of Chinese jujube; Aro. Soc. Hortic. Sci. Proc. 77 265-269

Ashton P S 1969 Speciation among tropical forest trees: some deductions in the light of recent evidence; Biol. J. Linn. Soc. 1 155-196

Baker H G 1976 'Mistake' pollination a s a reproductive system with special reference to the Caricaceae; in Tropical trees: Variation, breeding and conservation [eds) J Burley and B T Styles (London: Academic Press) pp 161-170

Baker H G and Baker I 1973 Some anthecological aspects of the evolution of nectar-producing flowers, particularly amino acid production in nectar; in Taxonomy and ecology (ed.) V H Heywood (London: Academic Press) pp 243-264

Baker H G, Cruden R W and Baker I 1971 Minor parasitism in pollination biology and its community function: the case of Ceiba acuminata; BioScience 21 1127-1129

Chundawat B S, Srivastava H C and Bishla S S 1979 Studies on blossom biology of ber (Zizyphus mauritiana Lam.); lndian J. Hortic. 36 158-163

Corbet S A 1978 Bees and the nectar of Echium vulgare; in The pollination offlowers by insects (ed.) A J Richards (London: Academic Press) pp 21-30

Cruden R W 1977 Pollen-ovule ratios: A conservative indicator of breeding systems in flowering plants; Evolution 31 32--46

Darwin C 1876 The different forms of flowers on plants of the same species (London: John Murrey) Ewusie J Y 1980 Elements of tropical ecology (London: Heinemann Educational Books Ltd.) Faegri K and Pijl L Van Der 1979 The principles ofpollination ecology (London: Pergamon Preso

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Feinsinger P 1978 Ecological interactions between plants and humming birds in a successional tropical community; Ecol. Monoor. 48 269-287

Galil J and Zeroni M 1967 On the pollination of Zizyphus spina-christi (L.) Willd in Israel; Israel J. Bot. 16 15-20

Hagerup O 1932 On pollination in extremely hot air of Timbuctu; Dan. Bot. Ark. 8 1-20 Harborne J B 1973 Phytochemical methods (London: Chapman and Hall) Kirby E G and Stanley R G 1976 Pollen handling techniques in forest genetics with special reference to

incompatibility; in Modern methods in forest genetics (ed.) J P Miksche (Berlin: Springer-Verlag) pp 229-243

Knuth P 1906 Handbook offlower pollination: Trans. J R Ainsworth Davis (Oxford: Clarendon Press) Mehrotra K N 1983 Second International Conference on Apiculture in Tropical Climates, IARI

(New Delhi: Yugantar Press) Pijl Van Der L 1978 Reproductive integration and sexual disharmony in floral functions; in The

pollination offlowers by insects (ed.) A J Richards (London: Academic Press) pp 79-88 Proctor M and Yeo P 1972 The pollination offlowers (New York: Taplinger Publishing Company) Singh D, Bakshi J C and Singh K 1970 Flowering and fruiting behaviour of ber Cv. Banarasi karaka

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(Zizyphus mauritiana Lam.), I. Floral biology; Punjab J. Hortic. 3 60-70 Teaotia S S and Chauhan R S 1963b Flowe¡ pollination, fruit set and fruit drop studies in ber

(Zizyphus mauritiana Lam.), II. Pollination, fruit set, fruit development and fruit drop; lndian J. Hortic. 21 40--45

Thomas C C 1924 The Chinese jujube; U.S. Dept. Agric. Bull. No. 1215 Webb C J 1985 Protandry, pollination and self-incompatibility in Discaria toumatou; N. Z. J. Bot. 23

331-335

proc. lndian acad. sci. (plant so.), vol. 99, no. 3, june

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