BlOTROPlCA 36(2): 148-1 55 2004

Factors Contributing to Variation in Seed Production among Remnant Populations of the Endangered Daisy Gerbera aurantiacal

Steven D. Johnsonz, Carine L. Collin3

School of Botany and Zoology, University of KwaZulu-Natal, P. Bag XO1 Scottsville, Pietermaritzburg 3209, South Africa

H. Jorgen Wissrnan4, Erika Halvarsson

School of Botany and Zoology, University of KwaZulu-Natal, P. Bag XOl Scottsville, Pietermaritzburg 3209, South Africa, and Department of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavagen 14, SE-752 36 Uppsala, Sweden

and

Jon Agren

Department of Plant Ecology, Evolutionary Biology Centre, Uppsala University, Villavagen 14, SE-752 36 Uppsala, Sweden

ABSTRACT The species-rich mist-belt grasslands of southern Africa have been severely reduced in extent as a result of commercial afforestation, thus confining many endemic plants and animals to small populations in habitat fragments. We inves- tigated the influence of various environmental factors on seed production and seedling recruitment in remnant pop- ulations of the endangered grassland herb Gerbera aurantiaca (Asteraceae). Experiments with color traps showed that Eriesthis beetles, which appear to be the primary pollinators of G. aurantiaca, were most abundant in the two largest extant populations. Seeds are produced in a very small proportion (typically <lo%) of the ca 80 female florets in a capitulum. The mean number of seeds produced in undamaged capitula was found to be significantly lower in small than in large populations. Pollen limitation was evident from a significant overall increase in seed set after supplemental pollination in three populations over two seasons. The proportion of capitula containing seed predators did not differ markedly among populations or years, but lepidopteran larvae, which destroy all of the seeds in a capitulum, were most abundant in the two largest populations in 2003. The presence of juvenile plants varied markedly among populations, but this could not be linked firmly to estimates of seed production. Clonal growth is likely to contribute to the persistence of small isolated populations of G. aurantiaca, even when seed production is severely compromised by pollen limitation and predation.

K2y word: itation; seed prehion; Ephritihe.

beetle pollination; Gerbera aurantiaca; grassland habitat jagmentation; Helicoverpa; Hopliini; pollen lim-

HABITAT FRAGMENTATION POSES ONE OF THE GREAT-

EST CURRENT THRFATS TO BIODIVERSITY. For plants, habitat fragmentation may lead not only to reduc- tion in population size and isolation, with the at- tendant risk of extinction due to demographic and genetic factors (4 Lande 1988), but may also dis- rupt key mutualisms with animal pollinators and seed dispersers (Kearns et al. 1998).

Small isolated plant populations are expected

’ Received 8 December 2003; revision accepted 12 Feb- ruary 2004.

Corresponding author; e-mail: Johnsonsd@nu.ac.za Current address: Laboratoire d’Ecologie, Systtmatique

et Evolution, UMR 8079, Universid Paris-Sud (XI), BB- timent 360, F-91405 Orsay cedex, France. * Current address: Department of Conservation Biology, Swedish University of Agriculture Sciences, Box 7002, SE-750 07 Uppsala, Sweden.

to be less attractive to pollinators than large pop- ulations ( k r e n 1996). Moreover, pollinator pop- ulations themselves may decline when floral re- sources decline or larval habitats are altered or de- stroyed (Kearns et al. 1998 and references therein). As a result, rates of pollinator visitation and seed production may often be lower in small than in large populations of animal-pollinated plants (Wid- i n 1993, Agren 1996, Groom 1998, Morgan 1999).

Expansion of commercial forestry has resulted in large-scale transformation of the mist-belt grass- lands of KwaZulu-Natal in South Africa. The soils and climate that support this vegetation type are ideal for commercial plantations of fast-growing ex- otic trees (particularly Eucalyptus, Pinus, and Aca- cia). As a result, it is estimated that less than 1 percent of this vegetation type, scattered as tiny

148

Reproductive Success in Fragmented Populations 149

FIGURE 1. (A) A single clone of Gerbera aurantiaca, illustrating how leaves and inflorescences sprout from a woody underground rootstock. (B) Male phase capitulum visited by the monkey beetle Erierthir vulpina. Scale bar: 10 mm.

fragments in a sea of tree plantations, remains in pristine condition (Scott-Shaw 1999).

One of the casualties of commercial afToresta- tion has been the “Hilton daisy” Gerbera aurantiaca Sch. Bip. (Asteraceae; Fig. 1). Once common, this self-incompatible perennial herb is now confined to nine extremely isolated populations in the tim- ber-growing region of South Africa, all but two in habitats with an area of less than 1 ha (Scott-Shaw 1999). A further five populations are known to have been recently extirpated by forestry or farming activities. It is currently listed as a red-data species with an “endangered status according to Scott- Shaw (1999).

Our preliminary observations in several popu- lations indicated that the bright red capitula of G. aurantiaca are visited primarily by the pollen-feed- ing monkey beetle Eriesthis uulpina Burmeister (Scarabaeidae: Hopliini). These beetles become densely coated in Gerbera pollen and make effective contact with the reproductive parts of the flowers (Fig. lB), making them likely candidates to be pol- linators. Similar pollination systems involving scar- ab beetles that visit unscented (to the human nose)

yellow, orange, or red flowers have been docu- mented in the Cape region of South Africa and in Mediterranean Europe (Goldblatt et al. 1998, Bernhardt 2000, Johnson & Midgley 2001).

The species forms large clones with a massive underground rootstock that allows resprouting when grasslands are burned (Hilliard 1977). Flow- ering occurs in early summer (September-Novem- ber) after the vegetation has been burned during the previous winter. Flowering is thus sporadic and may be diminished in years when the vegetation is not burned (Hilliard 1977). Our preliminary ob- servations indicated that seed production and seed- ling recruitment occur at very low levels in G. au- rantiaca populations. We also noted that herbivores destroy many capitula of G. aurantiaca during their seed production phase.

The aim of this study was to investigate the factors influencing seed production in populations of G. aurantiaca. In particular, we addressed the following questions: (1) Does the abundance of Eriesthis beetles vary among Gerbera populations?; (2) Is seed set positively related to the size of pop- ulations?; (3) Is seed set pollen-limited?; (4) Does seed predation vary among populations?; and (5) Are fewer juvenile plants found in small isolated populations?

MATERIALS AND METHODS

STUDY sITEs.-Six of the nine known populations of G. aurantiaca were studied between 1999 and 2003. The attributes and localities of these popu- lations are given in Table 1.

POPULATION SIZE AND DEMOGRAPHIC STRUCTURE.-

Plants of G. aurantiaca form large clones up to 2 m in diameter. Clones can be identified by their clumped growth pattern and the consistent color and morphology of the ray florets. In 1999, we counted the total number of flowering clones in each population. This was not repeated in 2003, as surveys in one population (Victoria Club) have shown no change in the number of clones over the past five years (Scott-Shaw, pers. comm.). To de- termine the size class distribution in the popula- tions, we counted the number of clones belonging to four diameter size classes (0-1 cm, i.e. seedling; 1-50 cm; 50-150 cm; and >150 cm) within one large (50 x 50 m) plot in each population. The area of habitat fragments containing G. aurantiaca populations was determined from aerial photo- graphs.

150 Johnson, Collin, Wissman, Halvarsson, and Agren

TABLE 1. Localities and cbararteristics of six Gerbera aurantiaca populations in KwaZulu-Natal, South Ajica.

Study site

Umvoci Railway Victoria Club World's View Byrne Valley Umvori Heights Lake Merthley

Coordinates (Lac, Lon)

29"07', 30"27' 29"34', 30"19' 29"34', 30"20' 29"48', 3O"ll' 29"08', 30"27' 29"02', 30"03'

Number Population Clones/ of clones area (ha) m2

56 0.12 0.05 75 1.30 0.006

100 0.90 0.01 300 2.50 0.01 445 0.25 0.18

5475 3.38 0.16

Surrounding habitat

Pine plantations Golf course and roads Eucalyptzu plantations and residential areas Indigenous forest and pine plantations Pine plantations Pine plantarions

BEETLE -rRArrING.-We used color traps (Johnson & Midgley 2001) to estimate the abundance of Eriesthis beetles in four G. aurantiaca populations (Victoria Club, Byrne Valley, Umvoti Heights, and Lake Merthley). We used traps consisting of red plastic Partypack@ bowls. Using the spectrometry apparatus described by Johnson and Anderson (2002), it was established that spectral reflectance of the traps approximated that of G. aurantiaca ray florets (Fig. 2). During the peak flowering period, eight traps were placed in each population. Traps were arranged 10 m apart from each other along a single transect. We used small (10 cm diam) traps in 1999 and large (17.5 cm diam) traps in 2003. Traps were filled with water in 1999, while in 2003 we carried out two experiments, the first using wa- ter-filled traps and the second using traps lined with the clear sticky substance Plantex@. Water- filled traps were left in the field for two days while the sticky traps were left for ca ten days. All insects caught in the traps were counted and identified. Those still alive in the water traps were released after identification.

SEED rRoDUcrIoN.-Reproductive shoots of G. au- rantiaca terminate in a single gynomonoecious ca-

- 60 - 8 8 Y

4 0 - c 0 9) G 9)

20-

o i

Gerbera aurantiaca Red traps ---

300 400 500 600 700

Wavelength (nm)

pitdum (flower head). Female ray and disk florets from the outer whorls are receptive before pollen is presented by central morphologically hermaph- roditic, but functionally male, disk florets. During 2003, in the Victoria Club, Byrne Valley, Umvoti Heights, and Lake Merthley populations, we sam- pled 16-19 capitula at the beginning of the male phase on different clones and counted the number of female and hermaphroditic florets.

In these four populations, natural levels of seed production were determined (in 1999 and 2003) from 18 to 44 randomly selected capitula, each tak- en from a different clone. Seed production data were also collected in the World's View population in 1999, but not in 2003 when flowering did not take place due to a lack of fire in the preceding winter. Capitula were collected prior to seed shed- ding and the number of plump seeds in each ca- pitulum was recorded.

POLLEN SUPPLEMENTATION.-TO determine if seed production was limited by insufficient pollination, pollen supplementation experiments were conduct- ed in 1999 and 2003 at three sites (Victoria Club, Byrne Valley, and Lake Merthley) and in 2002 at the Victoria Club site. Two flowering shoots were selected on each of 20 to 30 clones at each site and randomly allocated to either the control (unmanip- dated) or the pollen supplementation treatment. Capitula in the pollen supplementation treatment were pollinated in the female stage using pollen from another clone at least 30 m away to avoid matings between close relatives. Capitula were col- lected two to three weeks after pollination and the number of plump seeds within each capitulum was counted. Capitula damaged by seed predators were excluded from analyses. For each population, we calculated an index of pollen limitation, L = 1- (number of seeds produced by control capitula/ number of seeds produced by hand-pollinated ca- pitula), following Larson and Barrett (2000).

FIGURE 2. Spectral reflectance of ray florets of Gdera aurantiaca and the traps used to capture Eriestbis beetles.

sEED PREDA-,.,ON.-~e identified seed predators by rearing larvae from capitula in the lab. To quantib

Reproductive Success in Fragmented Populations 151

FIGURE 4. The number of individual insects captured in red color traps placed in Gerbera aurantiura popula- tions.

FIGURE 3. Size-class distributions in six populations of Gerbera aurantiacu. The median size class in each pop- ulation is indicated by an asterisk. Plants with a diameter less than 1 cm were considered seedlings.

analyses were performed with JMP version 3.1.5 (SAS 1995).

the levels of predation, we determined the propor- tion of capitula with resident seed predators for 30 to 82 plants in each of four populations. In 1999, this was done at a late stage of development, pre- cluding identification of seed predators; in 2003, capitula were examined at an earlier stage, making it possible to distinguish between moth and fly lar- vae.

STATISTICAL AN.aYsEs.-We compared the mean number and proportion of female florets within ca- pitula among the four populations using ANOVA. Natural levels of seed production (natural log trans- formed) were compared among years and popula- tions with a Ill-factorial two-way ANOVA. The World's View site, which did not flower in 2003, was excluded from this analysis. The relationship between the log transformed number of flowering clones in each population and mean seed set per capitulum was analyzed using linear regression. Data from the pollen supplementation experiment were analyzed using a full-factorial three-way ANOVA (population, year, and treatment as fac- tors). Variation among populations and years in the frequency of seed predation in capitula was ana- lyzed with logistic regression. Contrasts within ANOVA were performed with the critical level ad- justed according to sequential Bonferroni correc- tion (Rice 1989). Throughout the paper, we pre- sent means and standard errors of the means. All

RESULTS POPULATION SIZE AND DEMOGRAPHIC STRUCTURE.-

The number of flowering clones per population varied from 56 at Umvoti Railway to 5475 at Lake Merthley, which was by far the largest population (Table 1). Populations differed dramatically in the size-class distributions of individuals (Fig. 3). Very large clones (>150 cm) were found at Victoria Club and Lake Merthley. No seedlings were found at the Victoria Club site. On the other hand, there were many small plants and no very large clones at the Umvoti Heights, Umvoti Railway, and World's View sites (Fig. 3).

BEETLE TRAPPING.-ErhthiS beetles were readily at- tracted to, and alighted in, the red plastic bowls in the same manner that they alight on the capitula of G. aurantiaca. Approximately 100 individuals were captured, while the only other insect species trapped were four Monochelus hopliniid beetles and three honeybees (Fig. 4). We trapped significantly more beetles in the large Umvoti Heights and Lake Merthley populations (Fig. 4).

SEED PRoDucrroN.-The mean number of female florets per capitulum varied significantly among the four sites (F3, 63 = 7.65, P = 0.0002). In partic- ular, plants at Victoria Club had significantly fewer female florets per capitulum (69.5 t 2.8, N = 16) than plants at Umvoti Heights (90.2 t 4.6, N =

152 Johnson, Collin, Wissman, Halvarsson, and i\gren

T

z 0 F

cn 9

a cn

Y

Y J

16 . Y = -3.6 + 4.4 (l0g.x)

P = 0.037 R2 I O . 9 8

12.

8 - BV (25)

vc (29)

100 lo00 1M)o

Population size (log,,)

FIGURE 5. Relationship between the mean number of seeds per capitulum (5SE) and Gerbera aurantiaca pop- ulation size (loglo transformed number of flowering clones). Linear regression is based on mean values of seed set in non-attacked capitula (filled circles). Seed set after predation (open triangles), estimated from proportions of capitula damaged by moth and tephritid fly larvae, and the mean number of seeds remaining in capitula after damage by these seed predators (Fig. 4) did not show a significant relationship with population size. Populations with sample sizes in parentheses are as follows: VC- Victoria Club, WV-World‘s View, BV-Byrne Valley, UH-Umvoti Heights, LM-Lake Merthley.

19) and Lake Med ley (92.7 ? 3.8, N = 19), while the Byrne Valley population (81.1 ? 3.2, N = 16) was intermediate. The overall proportion of female florets within capitula was 0.43 ? 0.01, and this did not vary significantly among populations

Seed set (the number of seeds per capitulum) varied significantly among populations ( 4 1 9 4 = 10.88, P < O.OOOl), with the Lake Merthley pop- ulation consistently showing the highest seed set and the Victoria Club site the lowest seed set (Fig. 5). The magnitude of variation in seed set among populations was lower in 2003 (significant year x population effect in ANOVA, F3, 194 = 5.40, P = 0.0014). The mean number of seeds produced in capitula (before predation is taken into account) was significantly positively related to population size (log number of flowering clones) in both years (Fig. 5 ) , but was not significantly related to habitat area or the density of clones in either of the years (univariate linear regressions, P > 0.5).

(F3, 59 = 1.51, P = 0.22).

FIGURE 6. The effect of pollen supplementation on the number of seeds produced per capitulum ( x 5 SE) in three populations of Gerbera aurantiara in 1999 and 2003. Sample sizes are given above the bars. See Table 2 for statistical analysis.

POLLEN SUPPLEMENTATION.-supp~ementa~ hand- pollination increased seed production in all popu- lations (Fig. 6 and Table 2), although the magni- tude varied among populations (significant polli- nation treatment x population interaction in ANO- VA; Table 2). The mean number of seeds per capitulum was 5.28 (? 1.27) for control plants ver- sus 13.56 (?3.02) for hand-pollinated plants (ag- gregate means based on population means for ca- pitula in each category). In 2002, hand-pollinated capitula at Victoria Club produced a median of 12.5 seeds (range = 2-22, N = 5 plants), signifi- cantly more than the median of 0 seeds (range = 0-2, N = 10 plants) produced by naturally polli- nated control capitula (Mann-Whitney U-test, Z = 3.21, P = 0.0013). Although the sample size of hand-pollinated plants in 2002 was small because of premature seed release in hot and dry weather, these results are consistent with those observed in 1999 and 2003 when larger sample sizes were used. The mean index of pollen limitation was highest in the Victoria Club population and lowest in the Lake Merthley population (Fig. 6).

SEED rREDArroN.-Caterpillars collected from ca- pitula of G. aurantiaca were reared into adult moths in the laboratory and identified as Helico- verpa armigera (Hubner, 1809), the African boll- worm, whereas tephritid flies, Crmpedoxantba mar-

Reproductive Success in Fragmented Populations 153

TABLE 2. ANOVA of the number of see& produced per capitulum of G. aurantiaca following control and suppkmental pollination treatments at threc sites (Victoria Club, Byrne Vallty and Lake Merthley) in I999 and 2003 (Fig. 6).

~

Source of variation ~

df MS F P Pollination treatment 1 27.98 18.5 <0.0001 Population 2 10.73 7.1 0.001 Year 1 11.28 7.5 0.007 Poll. treatment x Population 2 5.73 3.8 0.025 Poll. treatment X Year 1 0.67 0.4 >0.5

Poll. treat X Pop. X Year 2 0.81 0.5 >0.5 Error (@ = 0.29, P < 0.0001) 174 1.51

Population X Year 2 17.65 11.7 <0.0001

ginalis (Wiedemann, 18 18), emerged from puparia found in capitula in all of the populations. Capit- ula with resident caterpillars wilted prematurely and did not set any viable seeds ( N = 20); however, tephritid flies lay a single egg in the middle of each capitulum and larvae feed on ovules until pupation (S. D. Johnson, pers. obs.). The aggregate mean for the number of seeds in capitula containing tephritid fly pupae in 2003 was 4.06 2 1.46 versus 7.98 2 1.9 ( N = 218 capitula in 4 populations) for capitula without seed predators, thus indicating that flies destroyed, on average, 50.1 percent of the seeds within the capitula that they occupied.

The mean percentage of capitula occupied by seed predators across the four populations was slightly higher (57.3 +_ 2.9%, N = 295) in 2003 than in 1999 (48.3 2 3.5%, N = 205), but this difference was not statistically significant (Walds x2 = 2.8, P = 0.09). The relative levels of seed pre-

FIGURE 7. The proportion of capitula containing seed-feeding insect larvae in four populations of Gerbera aurantiaca in 1999 and 2003. Most seed predators were identified in 2003 but not in 1999.

dation in different populations varied among years (significant year x population interaction, Wald’s x2 = 9.2, P = 0.03). Seed predation was significantly higher in the Umvoti Heights population than in the other populations in 2003 (x2 = 10.2, P = 0.0004), while no significant among-population variation in seed predation was recorded in 1999 (x2 = 1.19, P = 0.754). Predation by moth larvae, which destroy all seeds in capitula, was markedly higher in the Umvoti Heights and Lake Merthley populations than in the other populations in 2003

For the 2003 data, it was possible to estimate the effect of predation on the final levels of seed set by multiplying mean natural seed set in non- attacked capitula by the proportion of capitula oc- cupied (Fig. 5) and average proportion of seeds de-

The estimated percentage of seeds destroyed by predators was 22.4 percent at Byrne Valley, 26.9 percent at Victoria Club, 34.0 percent at Lake Merthley, and 59.1 percent at Umvoti Heights. Es- timated seed set after predation in the four study populations was not significantly related to popu- lation size (Fig. 5).

a 73 m 0

r (Fig. 7). 5 a 9 5 z

m

stroyed by moths and tephritid flies, respectively.

DISCUSSION

Our results show that seed set was low in all rem- nant populations of G. aurantiaca. Importantly, given that almost all populations of G. aurantiaca are known to have been drastically reduced in size by human alteration of the landscape (Scott-Shaw 1999, pers. comm.), the mean number of seeds produced by undamaged capitula was significantly lower in smaller populations, both in 1999 and 2003 (Fig. 5). This pattern suggests that pollina- tion processes in G. aurantiaca are negatively af- fected in small populations. Indeed, significantly fewer beetles were trapped in the two smallest pop-

154 Johnson, Collin, Wissrnan, Halvarsson, and Agren

ulations (Victoria Club and Byrne Valley; Fig. 4). The higher levels of seed set in large populations were mostly counterbalanced by their increased lev- els of seed predation. As a consequence, the esti- mated final number of seeds dispersed from capit- ula did not show a significant relationship with population size in 2003 when detailed seed pre- dation data were available (Fig. 5).

Reduced seed production in small populations has been reported in many other studies, although the exact causes are not often well understood (cf &,en 1996, Ktry et al. 2000; Brys et crl. 2004). Morgan (1999) studied eight populations of the endangered self-incompatible Australian daisy Ru- tidosix leptorrbyncboides and found strong positive effects of population size on seed set in two of three years. Similarly, Widtn (1993) found that seed set in the self-incompatible daisy Senecio intergrifolius was positively associated with the size of popula- tions in Sweden.

Seed set in G. aurantiaca was clearly pollen- limited, with supplemental hand-pollination lead- ing to an overall two-fold increase in seed set (Fig. 6 and Table 2). Fewer Eriestbis beetles were trapped in the Victoria Club and Byrne Valley populations than in the larger Umvoti Heights and Lake Merthley populations (Fig. 4). Variation in the abundance of these beetles helps to explain why the two smaller populations had lower seed set (Fig. 5) and higher indices of pollen limitation than the large Lake Merthley population (Fig. 6); however, seed production at the Umvoti Heights site was fairly low in 1999 and 2003, despite many Eriestbis beetles being trapped at that site. This suggests ei- ther that conditions were unusually favorable dur- ing the trapping periods or that factors other than pollen receipt limited seed formation at that site. The trapping results suggest that honeybees may have contributed to the higher seed set of G. au- rantiaca at the Victoria Club site in 2003 compared to 1999. More work is clearly needed on the con- tribution of different insects to seed set in G. au- rantiaca.

Although seed set was pollen limited, the mean number of seeds following supplemental pollina- tion (ca 14) was far below the maximum potential as determined by the number of female florets (ca 80; Fig. 6) . Possible explanations include inefficient hand-pollinations, resource limitation, inbreeding depression, and limited availability of mating types when populations contain few SI alleles (4 Byers & Meagher 1992, Demauro 1993).

There have been few studies on the combined effects of habitat fragmentation on pollination and

seed predation. Costin et al. (2001) recorded a weak but significant positive effect of population size on seed predation in the self-incompatible dai- sy Leucochrysum albicans, but overall seed produc- tion was not significantly related to population size. Wolf et al. (1 999) found no differences in the rate of seed predation by moths among populations of the daisy Heliantbus exilis, but predation by teph- ritid flies was lower in the most isolated popula- tions. Populations, regardless of isolation, showed moderate levels of pollen limitation (supplemental pollination increased seed production by 1 1.7%). Steffan-Dewenter et al. (2001) found that seed pre- dation of the daisy Centaura jacea by microlepi- doptera and tephritid flies declined in habitats that were less natural (as assessed by the number of seminatural habitats in a 250 m radius). Seed pro- duction was unaffected by the naturalness of the habitat because the effect of seed predators was counterbalanced by more pollinator visits in the relatively natural habitats. A similar situation may occur in G. aurantiaca, as the two large populations (Lake Merthley and Umvoti Heights) had relatively high incidences of capitula occupation by moth lar- vae, which are the most destructive seed predators (Fig. 7). As a consequence, the estimated final seed output was not related to population size in 2003 (Fig. 5) .

Populations of G. aurantiaca showed pro- nounced differences in their demographic structure (Fig. 3), even though seed production per capitu- lum (after predation is taken into account) did not differ drastically among populations in 2003 (Fig. 5). Recruitment of juveniles can be strongly influ- enced by several factors (Turnbull et al. 1999). For example, the lack of recruitment at the Victoria Club site may have been related to low levels of seed production during some years (Fig. 5) or to annual burning of the grassland in the past (Scott- Shaw, pers. comm.), which may not allow seedlings enough time to develop the critical mass of root- stock needed for successful resprouting after fire. The abundance of juveniles at the Umvoti Railway site is possibly related to regular disturbance, which creates ideal conditions for seedling establishment.

The outlook for the remaining small popula- tions of G. aurantiaca is uncertain. Like Morgan (1999) and WidCn (1993), we suspect that non- genetic demographic factors are likely to have a major influence on the persistence of small popu- lations of self-incompatible plants such as G. au- rantiaca (Givnish 2001). Seed set in G. aurantiaca is clearly limited by both levels of pollen receipt and seed predation; however, more work would be

Reproductive Success in Fragmented Populations 155

needed to establish whether or not levels of seed production have an influence on the population dynamics of G. aurantiaca. T h e clonal growth and

tions of short-lived self-incompatible daisies (6 Morgan 1999).

- extensive underground rootstock of G. aurantiaca are likely to act as buffers against rapid decline in ACKNOWLEDGMENTS populations characterized by low levels of seed pro- duction; however, since habitat fragmentation is mostly irreversible, extinction may eventually be in- evitable, as has been predicted for small popula-

We thank I. Johnson and M. van Kleunen for comments on the manuscript, Dr. R. Miller for identification of the tephritid flies, D ~ . M. &sger for identification of N ~ ~ - tuidae, and H. Dombrow for identification of the beetles.

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