564 S.-Afr.Tydskr. Plantk. , 1989,55(6): 564--573

Vegetative and reproductive phenology of Zjzjphus mucronata subsp. mucronata (Rhamnaceae)

P.C. Zietsman*, A.E. van Wyk and F.C. Botha 'National Museum, P.O. Box 266, Bloemfontein, 9300 Republic of South Africa; Department of Botany, University of Pretoria, Pretoria, 0002 Republic of South Africa and Department of Botany, University of the Orange Free State, Bloemfontein, 9300 Republic of South Africa

Accepted 14 July 1989

Vegetative growth of Ziziphus mucronata Willd. subsp. mucronata (Rhamnaceae) commences in spring and leaf fall starts towards the end of July. Flowering coincides with that of three co-occurring tree species. It shares pollinators only with Olea europaea subsp. africana, but the inconsistency and much shorter duration of flowering minimizes competition with this species. Some Z. mucronata individuals appear to function as males. A population comprises juveniles (vegetative), subadults (males) and adults (fully reproductive). The relation between height and reproductive potential of the individual plants indicates that small individuals in the population have a lower probability of flowering than the larger ones. The monomorphic flowers of Z. mucronata are protandrous and dichogamous. Dichogamy is complete and the flower can furthermore be regarded as heterodichogamous and herkogamous.

Vegetatiewe groei in Ziziphus mucronata Willd. subsp. mucronata (Rhamnaceae) neem 'n aanvang in die lente en blaarval teen die einde van Julie. Z. mucronata blom saam met drie ander boomspesies in die studie­ gebied maar deel bestuiwers met slegs Olea europaea subsp. africana. Kompetisie tussen die twee spesies om bestuiwers word egter tot die minimum beperk, deurdat Olea europaea subsp. africana ongereeld en vir 'n kort tyd blom. Sommige van die Z. mucronata individue tree klaarblyklik as manlike plante op. Die Z. mucro­ nata-populasie bestaan uit onvolwasse (vegetatiewe), half-volwasse (manlik) en volwasse (ten volle reproduk­ tiewe) individue. Die verband tussen hoogte van 'n individu en die voortplantingspotensiaal dui daarop dat groter individue 'n beter kans het om te blom as kleiner individue. Die monomorfiese blom van Z. mucronata is protandries en digogaam. Digogamie is volledig en die blom kan verder ook beskou word as heterodigogaam en herkogaam.

Keywords: Anthesis, breeding system, reproductive phenology, Rhamnaceae, Ziziphus mucronata

'To whom correspondence should be addressed

Introduction restricted to data on the timing and duration of flowering Ziziphus mucronata Willd. subsp. mucronata (Rhamna­ and fruiting. Apparently the only member of the Rham­ ceae), subsequently referred to as Z. mucronata , is one naceae of which the reproductive phenology has of the most abundant trees in the Bloemfontein area. received some attention is Discaria toumatou Raoul, a However, the observation was made that virtually no species from New Zealand (Primack 1980). seedlings of this pioneer species were present in the veld. Primack (1985) emphasized the need of studying Plausible explanations could be specific germination flowering phenology at four levels: the community, the requirements, the production of nonviable seeds population, the individual plant, and the single flower. (Zietsman & Botha 1987) and/or poor seed set. The Phenology has been considered to be the study of recur­ latter possibility can be a result of flowering in Z. ring biological events, the causes of their timing with mucronata which coincides with other species which regard to biotic and abiotic forces and the interrelation offer more attractive pollinator rewards, resulting in among phases of the same or different species (Lieth poor pollination and seed set in Z. mucronata. An 1974). From the available literature it is evident that up understanding of the timing mechanism of the individual to now studies on the reproductive phenology at the organisms, as well as the role of organism interactions in individual level have, especially in southern Africa, the rate and pattern of development in the wider system received scant attention. is therefore essential for interpreting the reproductive biology of a species. Materials and Methods The aim of this study was to determine the possible The study was conducted from July 1984 to August 1987 influence of a number of co-occurring woody species on on three study areas within close proximity of each the reproductive phenology of Z. mucronata and to other, 30 km north of Bloemfontein, South Africa (Grid determine how relevant the phenology of Z. mucronata 2826 CD). In addition to the main study area (Glen 1) on is to its breeding system. which the experimental work was conducted, two other Studies which include phenological data on Z. mucro­ areas were used as control plots for phenological nata are few and mainly concerned with vegetative observations. phenology. Reference to reproductive phenology is Acocks (1975) considered the vegetation of this area S.Afr.J. Bot. , 1989,55(6) 565

to be part of the Transitional Cymbopogon-Themeda (Eckl. & Zeyh.) N.K.B. Robson (P.e. & L. Zietsman Veld, No. 49. It is a relatively dry area with a rainfall of 430) of which only a few scattered individuals occur in 400 to 600 mm per annum (mainly in summer). The the study area. grassland, in which Themeda triandra Forssk. (P. e. The phenological variables were monitored on five Zietsman 54) is the dominant species, is broken by dolor­ randomly chosen branches on different sides of an itic outcrops where drainage lines are formed. Acacia individual tree and for each individual a mean value was karroo Hayne (P. e. & L. Zietsman 42) is the only tree determined. For each observation date the mean of the species associated with the grassland. Of the other data for the individuals of a species was used to indicate woody species common to the area, Osyris lanceolata the average stage of development for the particular Hochst. & Steud. (P. e. & L. Zietsman 1384) and species in the community. Diospyros austro-africana De Winter (P. e. & L. The data were recorded as follows Zietsman 1031) occur on the slopes of the doloritic 0: phenophase absent, outcrops. Along the drainage lines (tributaries of the 1: start of phenophase (leaves and flowers just emerging Modder River) Olea europaea L. subsp. africana (Mill.) from buds, fruits expanding) P.S. Green (P.e. & L. Zietsman 1200) and Rhus lancea 2: leaves, flower buds and/or fruits clearly visible L.f. (P.e. & L. Zietsman 428) are the most common (approximately 50% mature) woody species. On the flood-plain, which is covered by a 3: leaves, flower buds and/or fruits about 75% mature thick layer of well-drained doloritic sands, Z. mucronata 4: mature stage of phenophase when leaves had fully (P. e. Zietsman 58) and Acacia karroo are dominant. All expanded, flowers were receptive and fruits voucher specimens are kept in the herbarium of the dispersable. National Museum, Bloemfontein (NMB). Flowers of a number of Z. mucronata individuals at The control plots are situated on the farms Middel­ Glen 1 were observed over a 24-h period. This was done punt, almost 10 km due south of Glen 1, and Cypress, to determine the longevity of an individual flower of this approximately 10 km west of Glen 1, the latter being species as well as the different stages shown by a flower part of Glen Agricultural College. Both these plots are during anthesis. The height of each population's individ­ close to the Modder River in areas where invasion by uals was measured with a measuring stick and divided Karoo vegetation and Acacia karroo is clearly evident. In into different height classes of I-m intervals. the text these plots will be referred to as Middelpunt and Climatological data was received from Glen Agricul­ Glen 2, respectively. tural College, the weather station closest to the study An aerial photograph (1:50 000) of Glen 1 was divided area. This data was processed as described by Walter into grids of l-cm2 each. Ten points were chosen on the (1963) (Figure 1). intersect of the grid lines using a set of random numbers (Rohlf & Sokal 1969). The position of each point was Results and Discussion located in the veld. The five individuals of Z. mucronata Vegetative phenology nearest to each of these points were clearly marked. Although a number of the species studied are ever­ Each of these 10 groups, consisting of five individuals greens, africana, D. lycioides, G. occidentalis and Z. each, was regarded as a sample plot. e. mucronata are deciduous. In these species vegetative As a control, 10 individuals of Z. mucronata at each of growth commences before the first rain in spring Middelpunt and Glen 2 were monitored. Phenological data were collected twice a month during summer and (Figures 1 & 2). Vegetative growth of Z. mucronata once a month during winter. Whenever 10% of the commences in spring towards the end of September and individuals of a species were in the same phenophase it beginning of October. In the remainder of the species was considered to be indicative of a particular pheno­ studied, vegetative growth starts any time between the phase (van Rooyen et al. 1986a). end of winter in August, up to October in summer. Leaf To record species flowering concurrently with Z. fall of e. africana and D. lycioides starts in May, during mucronata, and thus possibly competing for the same the autumn and continues until July after which the trees pollinators, the approach of Newman & Beard (1962) are without leaves for a period of 1 to 2 months. In G. was followed whereby data was collected on the morpho­ occidentalis and Z. mucro nata leaf fall starts in late logical and physical changes in the structure of the more winter toward the end of July and beginning of August. abundant tree and shrub species. Leaf, flower and fruit These two species are without leaves for a fairly short development were the three basic phenological variables period of 1 month after which a flush of new leaves monitored in this study. In addition to Z. mucronata the commences. eight most abundant woody species were monitored. Onset of vegetative growth of tree species like Z. These are Celtis africana B urm. L (P. e. & L. Zietsman mucronata before the first rains of the season (Figure 2) 473) , Diospyros austro-africana, D. lycioides Desf.(P.e. can be hypothesized to be as follows: during the early & L. Zietsman 1559), Grewia occidentalis L. (P. e. & L. stages of a dry period the water lost by a tree through Zietsman 597), Olea europaea, Osyris lanceolata, Rhus transpiration exceeds the water absorbed through the lancea and R. undulata Jacq. (P.e. & L. Zietsman 587). roots. The water potential of the tree declines and causes Species excluded are Cussonia paniculata Eckl. & Zeyh water stress, leaf senescence and leaf .abscission (Reich (P.e. & L. Zietsman 1713), Ehretia rigida (Thunb.) & Borchert 1982). Since absorption of soil moisture Druce (P. e. Zietsman 290) , and May tenus heterophylla could probably continue at a low rate, this results in a 566 S.-Afr.Tydskr. Plantk., 1989,55(6)

cu w a: ::J <~ a: w 0.. :E w ~

1984 1985 1986 1987

TIME (MONTH)

Figure 1 Climate diagram of Glen 1 for the period July 1984 to August 1987. - total monthly rainfall , --- mean monthly air temperature, _ very moist period, ~ moist period, EJ dry period. slow increase in the water potential of the tree due to the photosynthetically active throughout the year (van virtual absence of transpiration. When the water poten­ Rooyen et al. 1986b). The species considered to be tial exceeds a certain threshold value, growth may evergreen in this study are D. austro-africana, Olea euro­ resume even before the first rains (van Rooyen et al. paea, Osyris lanceolata, R. lancea and R. undulata. 1986b). In areas with very dry winters, as in the study area, the Reproductive phenology at the community level rate of leaf fall in trees appears to be strongly correlated Flowering with a decrease in soil moisture and an increase in water Regardless of differences in the year-to-year climatic stress experienced by the plants (Reich & Borchert conditions (Figure 1), anthesis of C. africana, D. austro­ 1982). A rest period could be induced in plants exper­ africana, R. lancea, R. undulata and Z. mucronata iencing seasonal drought, low air humidity and a commences within a relatively constant period of 2 to 3 decrease in daylength and humidity (Huxley & van Eck weeks (Figure 2). In C. africana and Z. mucronata 1974; Alvim & Alvim 1978; Shukla & Ramakrishnan anthesis starts during October and the first half of 1982). November respectively. Anthesis starts during August in Evergreen species are defined as those where leaf fall D. austro-africana, during March in R. undulata and and new growth either occur simultaneously during the during April in R. lancea. Anthesis of D. lycioides starts active growing season and/or those which still bear 50% in September and October during spring while that of of the previous season's leaves when the new leaves start Olea europaea starts at any time during the 3-month to unfold. The leaves of these species are probably period between October and December. Various hypotheses have previously been postulated to explain the relative fixed period in which anthesis, for Cellis afrieana example in the case of Z. mucronata, commences

Diospyros !:1 11'1111 11 11111 ~ 111'1 1 1111111 ~ 1111111' 1 (Figure 2). Alvim & Alvim (1978) attribute the phenom­ austro-africana enon where plant species flower on mOre or less the Diospyros e:='IIIIIIII::;:llllll lll lIlIll ll llb ~'1 11111I1I1 1 1I 11 &1 same date each year to the possibility that these species Iycioides may be strongly influenced by environmental variables Grewia such as photoperiod of which the annual variation is oeeidentalis hilt!"" ',',",' :",':' :oi" """':;"" '/\ ~ 'I :;;:"I never erratic. Opler et al . (1976) ascribe this flowering 1 11 ::.:i 1 1 11111 1 11111111111 1 11111 ~1 1111:I, I *II"II :'1111111III Olea europaea phenomenon in some tropical trees to an endogenous rhythm which most probably will also involve a setting of Osyris lanceolata E'I""" 11.I,I:_,I, _ , I:,I.I ~'t'Z!tt!tfE: I,IIIII,:' I , II . "I.. II:ljj'I ,"I_'," ,1,1,1,', ,",1 the rhythm by a constant factor, such as the Rhus lancea = lii jii!lli!ii:::: ' jjlli !li jljj!i%!;! i j!ji l jii! ! ~ photoperiod .. Borchert (1983) states that the triggering of anthesis mainly involves the release from an inhibitory Rhus undulata =""'~ " " I""""" gg "i" ll" """"" l ' l ' *""'l endogenous or environmental condition, usually water stress or low temperature, which prevents flower buds ZiziphuS rl l" :::::;: J II ::£! I IIIIII II ~1' 1 :::II, IIII I' 1 mucronata from completing their development. Furthermore he , t , , ! , , , , , ! , ! , , , ! believes that anthesis in tropical trees is primarily, if not NFMAN FMAN FMA 1984 1985 1986 1987 exclusively, prevented by water stress within the tree crown. Rathcke & Lacey (1985) regard photoperiod, Figure 2 Phenograms of the most abundant tree and shrub temperature and moisture to be the three major species at Glen 1. _ leaves, _ flowers, ~ fruits . environmental factors that may influence anthesis. S.Afr.J. Bot. , 1989, 55(6) 567

Flowering peaks As G. o cciden talis, Olea europaea and Osyris Most of the species studied flower mainly from October lanceolata flower concurrently with Z. mucronata, which to January with a peak during November (Figure 3) . is pollinated by two dipteran species (Musca domestica After the usually higher rainfall during the latter part of L. and a Sarcophaga species) (Zietsman 1988), one February and most of March, flowering in the tree and could expect a degree of competition for pollinators. shrub population peaks again in April after which it Flowering in G. occidentalis is very erratic, and has drops significantly. There is not a single month in the coincided twice for very short periods with that of Z. year during which there are no trees in flower in the mucronata. Due to this erratic flowering it is unlikely study area. that G. occidentalis could pose a constant problem in the Although Osyris lanceolata flowers throughout the pollination of Z. mucronata. If bees that have been seen year, its peak flowering period is during April. Osyris to visit flowers of G. occidentalis are its pollinators, lanceolata, G. occidentalis and Olea europaea are competition between this species and Z. mucronata apparently very sensitive to moisture stress and abort would not exist. their flowers after a short spell of drought (Figures 1 & Except for a brief period during January and/or 2). During the 3 years of this study G. occidentalis, as February Osyris lanceolata flowers concurrently with Z. well as Olea europaea, had one very successful season, mucronata. Although Herrera (1985) found that the during 1984, when a number of individuals flowered insects visiting Osyris quadripartita Salzm. ex Decne profusely (Figure 2). During the 1985/86 season the were mainly small and medium-sized flies, no flies were flowering period of G. occidentalis was reduced to two seen visiting flowers of Osyris lanceolata during this peaks (late December 1985 and early March 1986) and to study. Furthermore, this species is associated with the a single short peak during the 1986/87 season (November surrounding hillocks, while Z. mucronata is associated 1986). with the drainage lines and floodplains. Bearing this in In comparing the flowering periods of the co-occurring mind, it is unlikely that Osyris lanceolata exercises any species closely with that of Z. mucronata (Figure 4a- h), detrimental effect on the pollination of Z . mucronata. it is evident that O. occidentalis, Olea europaea and With the exception of 1986/87 the flowering period of Osyris lanceolata flower concurrently with Z. mucronata. Olea europaea overlapped with the flowering in Z . The flowering pattern of the nine woody species mucronata and can therefore compete directly with Z. studied (Figure 3) corresponds very well with that of mucronata for pollinators. Although individuals of this woody species in Tanzania (Scott 1934), Botswana species have been monitored to determine the presence (Miller 1949), parts of the Transvaal (van Rooyen et al. of any possible pollinators, neither of the two dipteran 1986b) and with that of savanna trees in Malawi (Hall­ species that are responsible for the pollination of Z. Martin & Fuller 1975). mucronata have been seen to visit flowers of Olea The period of approximately 4 to 5 months during the europaea. However, the possible involvement of flies in year in which Z. mucronata flowers, does not coincide the pollination of this species cannot be ruled out. with the peak flowering period for the co-occurring Studies conducted in the Transvaal and the Cape Prov­ woody species in the community. Receptive flowers are ince revealed that, amongst other insects, Musca borne by Z. mucronata during that part of the summer domestica seems to pollinate Olea europaea. However, when the lowest percentage of the associated woody the inconsistency and much shorter duration of flowering species in the study area flowers, thereby possibly in the latter species probably minimizes competition with minimizing competition for pollinators through time. Z. mucronata.

Duration of flowering and fruiting periods The flowering period of just less than 2 months of Celtis ------1 ~------I----~I ,..---.. africana was the shortest of all the species investigated. 40 On the other hand Osyris lanceolata flowered

III throughout the year with a short lapse during February W 30 , ,I when there were no mature (receptive) flowers present. U .. , , , W , 0- Ripe fruits were recorded throughout the season with a III "ri 'ifl. 20 peak during May and June (Figure 3). It has already been demonstrated in a number of species that fruits are 10 generally more likely to mature from the first rather than later-pollinated flowers (Stephenson 1980; Wyatt 1980; 0 Bertin 1982). It can therefore be expected that in this J A S 0 NDJ FMAMJ regard competition for pollinators during the last month TIME (MONTHS) of flowering of Z. mucronata is unlikely to have too Figure 3 Mutual distribution of flowering (-) and fruiting much of an effect on fruit set of this species. Competition (- - -) in the nine most abundant woody species at Glen 1. H for pollinators during the earlier stages of the flowering months during which Ziziphus mucronata bears receptive period should therefore be regarded as having a more flowers, ~ - ~ months during which Ziziphus mucronata bears negative effect on the reproductive success of Z. mucro­ ripe fruits . nata than competition at the end of the flowering period. 568 S.-Afr.Tydskr. Plantk. , 1989,55(6)

a b 4 4 r--- I , I '/ I I / I, 1/ / \I 1/ / I 2 ~ 2

o o

c d 4 4

, W 2 f 2 CJ ~ fA -I 0 0 ~ ~ CJ 0 -I e f 0 Z 4 4 , W , J: a. f 2 2 I / / / / o 0

9 h 4 4 r-+-~ ~ , I , " I , I ~ ~ I I f I 2 I 2 I / I I I f I I o 0 o J A J 0 J A J 0 J A 0 J A J 0 J A J 0 J A 1986 1987 1984 1985 1986 1987 1984 1985 TIME (MONTHS) TIME (MONTHS)

Figure 4 Flowering period of Ziziphus mucronata (-) and the eight co-occurring woody species (- - -) at Glen 1: Grewia occiden­ talis (a) , Osyris LanceoLata (b), OLea europaea subsp. africana (c) , Celtis africana (d) , Diospyros austro-africana (e) , D. Lycioides (f) , Rhus unduLata (g) and R . Lancea (h).

The fruiting pattern in the community (Figure 3) is in the species with mature fruits decline during the dry agreement with the results of studies on the fruiting period of the season. The same phenomenon was obser­ phenology of trees in the tropics (Frankie et at. 1974a, b; ved during the present study where the fruits of C. Milton et at. 1982), suggesting that most species exhibit africana, G. occidentatis and Z. mucronata mature some degree of intraspecific synchronization in flower­ during winter and disperse towards its end. Fruits of the ing/fruiting phenology. On a community-wide basis remaining species either mature in winter and are there are clear peak periods in the number of tree dispersed in summer or mature and disperse in summer. species producing fruits. These fluctuations very often The only species of the community in which mature appear to be correlated with environmental factors such fruits were available for most of the year IS Osyris as rainfall (Frankie et at. 1974a, b; Milton et at. 1982). lanceolata . Frankie et at. (1974a, b) furthermore found that most of the tropical species studied matured their fruit during The fruiting peak in September is a result of the the dry part of the season. At one of their study sites second flowering peak during April (Figure 3), while the they not only found fruiting in every month, but also that more prominent first flowering period reflects in the S.Afr.J. Bot., 1989,55(6) 569 second fruiting period of the community during early variation for the flowering time within populations and winter. species have been documented for numerous species The profuse flowering and fruit set of G. occidentalis (McMillan 1967; Harris 1970; McIntyre & Best 1978). during 1984 was followed by two consecutive years of Many species differ in flowering patterns over geograph­ poor flowering and fruit set (Figure 2). This could ical areas and even between microsites (Jackson 1966; possibly be a case of mast flowering and fruiting (Harper Harris 1970; Hodgkinson & Quinn 1978). 1977). The same phenomenon was , to a much smaller Additional phenograms of these populations were degree, observed in Olea europaea and D. lycioides. compiled by using the average value of the phenological However, this may also be a result of the unusually wet stage for each month of the year during the 3-year study period during January and February 1984 (Figure 1). period (Figure 6) . These phenograms do not show the Since frugivorous birds are common in the study area lack of successful fruiting in the Glen 2 and Middelpunt and all of the species studied have, to a certain degree, populations during 1985/86 and that of the Middelpunt fleshy fruits, one would expect at least some species to population during 1986/87. The absence of fruits during be adapted to seedlfruit dispersal by birds or smaller 1986 and the abortion of immature fruits during 1987 at mammals. Of the species studied, Z. mucronata is the Middelpunt, was to a large extent due to predation by only one which to some extent advertises (Frankie et al. Apopnictus cf. zizyphi Marshall (Coleoptera: Curculioni­ 1974a, b) its ripe fruits during winter and spring. During dae: Anthonominae). The weevils lay their eggs in the this period dead leaves remain on some of the trees. The immature fruit, probably during phases 1 and/or 2, after mature fruits which are reddish brown in colour, stand which the different instars develop inside the immature out against the cream colour of the dead leaves. Birds fruit. During this period the fruit continues to grow. that have been observed consuming the ripe fruits are Despite the utilization of the ovules by the instars the Creatophora cineria (Meuschen) (Wattled Starling) and fruit expands until it reaches 75% maturity when the Picnonotus nigricans (Vieillot) (Redeyed Bulbul). adult insect emerges. By the time the adult weevils Unlike flowering, the fruiting period of Z . mucronata emerge, the pericarp is all that is left of the fruit. coincides with the peak fruiting period of the commu­ This association between Apopnictus cf. zizyphi and Z. nity, thereby probably minimizing post-dispersal mucronata apparently results in some populations being predation. heavily attacked by predators. This may cause the size of the fruit crop to be depleted to such an extent that there Reproductive phenology at the population level are no fruits left to disperse. Harper (1977) considers such specialized short-lived seed eaters as predispersal In comparing the phenograms of the three study areas predators. Infestation of immature fruits by these (Figure 5) it is clear that although flowering at Glen 2 weevils differs between years and has been recorded at and Middelpunt commences earlier than at Glen 1 there all three populations. A random check on material are no major differences between the three populations during 1986 showed 100% weevil infestation at Middel­ of Z. mucronata. However, one difference that did occur punt, 20% at Glen 2 and no infestation at Glen 1. was that some individuals at the Glen 1 population Bearing in mind that the pattern of fruit production fruited successfully every year during the study, while has only been monitored for three consecutive years , the 1984/85 season was the only successful year for some one can expect a repetition of a successful fruiting season individuals at Glen 2 and Middelpunt. at Middelpunt such as the one of 1984/85. According to The difference in onset of flowering between the three Murphy (1968) this unpredictability of seed production populations of Z . mucronata (Figure 5) can probably be can be seen as a defence against predation. explained by Glen 2 and Middelpunt being on the banks of the Modder River where a higher ground-water level may prevail. According to Borchert (1983), a high level GLEN 1 of ground-water could influence the time of flowering. However, the existence of environmental and genetic

rlllllllll~IIIII'~11111111111111111111111111111I1 GLEN 1 GLEN 2 ,•. :.: ••.•.:.:.;..: •.~ .•::< .•:ZiG2 C...... ,.... .,." ...... :...... c::: .•,".c '.' :':"

GLEN2 /""!:."" ,"': '." <'::att::"" ""E

MIDDELPUNT r' II ;"" ""."" ""' ."':£'" * """"""" ful lIII I:tEil¥:1 1111 1'/ J A SOND J FMAMJ

Figure 6 Diagram of average phenological data for each 1984 1985 1986 1987 month of the 3-year study period of the three different popula­ Figure 5 Phenograms of the three different populations of tions of Ziziphus mucronata. IlIIlTIl leaves, _ flowers, EiJ Ziziphus mucronata. IIIIIllD leaves, _ flowers, cg fruits. fruits. 570 S.-Afr.Tydskr. Plantk., 1989, 55(6)

Reproductive phenology at the individual level (1980) considers abortion, the regulation of flower and In comparing the two sets of phenograms of the three fruit numbers, to be an adjustment of maternal invest­ populations of Z. mucronata (Figures 6 & 7) , it is evident ment to match available resources. that a phenogram based on average values for each month of the year fails to indicate the year-to-year differences in any population. Such a presentation would fail to indicate the possibility of mast years in D. a lycioides, G. occidentalis, Olea europaea and R. 4 undulata. However, both methods use an average value for the phenological stage of a number of individuals in 3 the population. In using these methods, the data pertain­ ing to the breeding system of the species being investi­ 2 gated, is concealed in an average. Based on the phenological data of flowering and fruiting of the 50 Z. mucronata individuals at Glen 1, the population can be o divided into four groups of which a single representative example is given for each group (Figure 7a-d). The first group (Figure 7a) comprising 14% of the population, consists of individuals that did not flower in b any of the three flowering seasons monitored during the 4 study. These individuals grew vegetatively only, and only two of them had flower buds during anyone of the 3 seasons monitored. These flower buds aborted before reaching maturity. w 2 The second and largest group, which comprises 60% of the population (Figure 7b) , consists of trees that en~ ..J flower every season but fail to produce mature fruits. o Approximately 8% of the trees in this group bear fruits ~ C; that abort for no apparent reason before reaching 9 maturity. o z c The third group, 14% (Figure 7c), consists of trees w that flower every year and each having produced at least l: 4 c. one batch of mature fruits during the study period but 3 not every year. The fourth group (Figure 7d) consists of the remaining 2 12% of the population and includes trees that flower and fruit successfully each year. In comparison a very different system was found at Middelpunt and Glen 2 (Figure 8). At the latter, the o population fits into two of the above-mentioned groups. Only 10% of the population appeared to be functionally male plants (group 2, Figure 7b), while the remainder d fits into group 3 (Figure 7c). Although no trees failed to 4 ~ ••••• tt ,.., ~ .... flower in the 3 years of this study, not one fruited , , ' , I, , successfully in any other season than 1984/85. At I 3 ••• Middelpunt, the population shows virtually the same tendency as at Glen 2, the only difference being that 2 10% of the population fits into group 1, the vegetative group (Figure 7a), and 80% into group 3, the intermed­ iate group (Figure 7c). Despite several authors ascribing fruit abortion mainly o due to the lack of successful pollination, the continuous OJAJOJAJOJAJ abortion of immature fruits in many species suggests that 1984 1985 1986 1987 abortions do not only result from inadequate pollination, TIME (MONTHS) but that other factors may also be involved (Primack 1979; Webb 1979; Lloyd 1980; Wiens et al. 1987). Janzen Figure 7 Flowering (-) and fruiting (- - -) patterns of repre­ (1978) regards flower and fruit abortion as possibly being sentatives of each of the four different reproductive groups. (a) the outcome of choice of parentage by the female group 1 - vegetative individuals, (b) group 2 - functionally genome or the discarding of flowers produced only for male plants, (c) group 3 - intermediate group, (d) group 4- pollen or pollinator attraction. On the other hand Lloyd fully reproductive plants. S.Afr.J. Bot., 1989,55(6) 571

100 100.------.

80 80 rn ....I oCt ;:) 60 60 C > C 40 40 ~ 'if. 20 20 o o GLEN 1 GLEN 2 MIDDELPUNT 2 3 4 REPRODUCTIVE GROUPS SAMPLE PLOTS Figure 8 Flowering and fruiting patterns of individuals in the Figure 9 Comparison of the different reproductive groups three populations of Ziziphus mucronata. _ individuals that with regard to height of Ziziphus mucronata trees. _ 1 m ~ have not flowered in any of the seasons monitored (group 1), individuals < 2 m, ~ 2 m ~ individuals < 3 m, 0 ~ m ~ ~ individuals that flowered every season but failed to individuals < 4 m, ~ individuals?: 4 m. produce mature fruits during any of the seasons (group 2), 13 individuals that flowered every season and that have produced at least one batch of mature fruits (group 3), ~ However, much more phenological data collected over a individuals that flowered and fruited successfully every season much longer period is needed to confirm this hypothesis. (group 4). Reproductive phenology of individual flowers Individual trees of Z. mucronata can be divided into The existence of the four reproductive groups amongst early- and late-flowering groups (Figure 10). Anthesis individuals of Z. mucronata, including functionally male starts at 07hOO in the early-flowering group (group A), and fully reproductive groups, suggests that the lack of and at llhOO in the late-flowering group (group B). In successful pollination may not be the only cause of fruit approximately 85% of the trees in the Glen 1 population abortion. Other possible causes may include resource anthesis starts in the early morning. The sequence of limitations (which have not received any attention events during anthesis is the same in these two groups. during this study) and sexual selection which attributes Anthesis can be divided into three main phases. The abortions to conflicts inherent in the optimization of first is an asexual phase, lasting approximately 2 h, male and female reproductive success. followed by a male phase which lasts for up to 4 h and a Z. mucronata individuals were grouped into five female phase which may last for 21 h. The longevity of different height classes (not shown). Most of the an individual flower is approximately 26 h. The mono­ individuals (39%) were between 1 and 2 m high while morphic flowers of Z. mucronata are protandrous and only 2% of the individuals monitored during this study dichogamous. Dichogamy is complete and the flowers were smaller than 1 m. In relating height to reproductive can furthermore be regarded as heterodichogamous potential (Figure 9), it is evident that the vegetative (Lloyd & Webb 1986) and herkogamous. group (group 1) consists mainly of individuals smaller Although varying between years and study sites, than 2 m, while 50% of the trees in the fully reproductive approximately between 0% and 2% of the flowers of Z. group (group 4) are individuals of which the height is mucronata were infested by a weevil, Aplemonis ziziphi between 3 and 4 m. There are therefore indications that (Coleoptera: Apionidae). The infested flower buds were the shorter individuals in the population have a lower extraordinarily big, approximately three times the size of probability of flowering than the taller ones. There can, a normal bud, and only aborted after the adult weevil however, be a number of reasons, including differences had emerged. The larval instars of this weevil utilize the between microsites. Although it is not, with the available reproductive organs of the immature flower (Aplemonis data, entirely possible to relate this trend to the age ziziphi must not be confused with Apopnictus cf. zizyphi, structure of the individuals in the population, there a fruit predator). Due to its low intensity, it is doubtful seems to be enough evidence in the literature to postu­ whether the up to 2% insect infestation of flower buds of late that such a system may occur in Z. mucronata Z. mucronata has a significant influence on flowering of (Hillman 1962; Primack 1979; Shannon & Wyatt 1986). this species.

EARLY GROUP c c

TIME OF DAY 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

LATE GROUP c c

Figure 10 Schematic representation of anthesis in the two different groups of Ziziphus mucronata flowers over a period of 24 h. 572 S.-Afr.Tydskr. Plantk. , 1989, 55(6)

In conclusion, Olea europaea is the only co-ocurring HUXLEY, P.A . & VAN ECK, W.A. 1974. Seasonal changes woody species in the study area which competes against in growth and development of some woody perennials near Z . mucronata for Musca domestica and a Sarcophaga Kampala Uganda. l . Ecol. 62: 579- 592. species as pollinators. The erratic flowering pattern of JACKSON, M.J. 1966. Effects of microclimate on spring Olea europaea and its short period of overlap with that of flowering phenology. Ecology 47: 407--415 . Z . mucronata appears to minimize competition between JANZEN, D .H. 1978. Seeding patterns of tropical trees. In: these species. The importance of studying phenology on Tropical trees and living systems, eds. Tomlinson, P.B. & Zimmermann, M.H., Proc. 4th Cabot Symp. Harvard the individual level proved to be indispensible for estab­ Forest, Petersham, Massachusetts, April 1976, Cambridge, lishing a clear understanding of the breeding system of London. the species. Probably the most important consequence of LlETH, H . 1974. Phenology and seasonality modeling. this approach, as applied in this study, is the recognition Ecological studies 8, Springer-Verlag, New York. of some Z. mucronata individuals that appear to be LLOYD, D.G. 1980. The distribution of gender in four primarily pollen donors and therefore functionally angiosperm species illustrating two evolutionary pathways males. to dioecy. Evolution 34: 123-134. LLOYD, D.G. & WEBB, c.J. 1986. The avoidance of Acknowledgements interference between the presentation of pollen and stigmas We are indebted to the Directors and Council of the in angiosperms. T. Dichogamy. N.Z. 1. Bot. 24: 135-162. National Museum, Bloemfontein, for financing this McINTYRE, G .I. & BEST, K.F. 1978. Studies on the research, the Director of Glen Agricultural College for flowering of Thlaspi arvense L. IV. 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