Pollinators, mates and Allee effects: the importance of self-pollination for fecundity in an...

Pollinators, mates and Allee effects: the importanceof self-pollination for fecundity in an invasive lilyJames G. Rodger*1, Mark van Kleunen2 and Steven D. Johnson1

1Centre for Invasion Biology, School of Life Sciences, University of KwaZulu-Natal, Pietermaritzburg 3209, South Africa;and 2Ecology, Department of Biology, University of Konstanz, Universit€atsstrasse 10, D-78457 Konstanz, Germany

Summary

1. Ability to self-fertilize is correlated with invasiveness in several introduced floras, and this

has been attributed to its mitigating effect on fecundity when pollinator visitation and mate

availability are inadequate. Cross-pollination opportunities are expected to be most limited in

isolated individuals and small populations, both typical of the leading edge of an invasion.

Thus, self-pollination may promote invasion in part by mitigating pollen-limitation Allee

effects.

2. We used emasculation and pollen supplementation experiments to test whether the impor-

tance of self-pollination for fecundity increased as plant abundance decreased and isolation

increased, in the hawkmoth-pollinated and autonomously self-pollinating invasive lily Lilium

formosanum, in its introduced range in KwaZulu-Natal, South Africa. As inbreeding depres-

sion is negligible in these populations, seed production through selfing is likely to be demo-

graphically important.

3. In naturalized populations of L. formosanum, varying in size and degree of isolation,

emasculation reduced seed production by two-thirds, indicating strong reliance on self-fertiliza-

tion for fecundity due to inadequate pollinator visitation. However, this was not related to

population size and was only greater for more isolated populations in one of the 3 years in

which the experiment was carried out. Pollen supplementation experiments showed that pollen

limitation was low – 12% on average – and significant in only one of 3 years, demonstrating

that autonomous self-pollination was highly effective.

4. In artificial arrays, consisting of plants placed inside naturalized populations or in pairs iso-

lated (3–702 m) from populations, the effect of emasculation on fecundity was greater in iso-

lated plants than those inside the population in one of two populations. Isolation reduced

fecundity when emasculated plants were placed next to a second emasculated plant, but not

when emasculated plants were partnered with an intact plant, from which they could receive

pollen.

5. We conclude that self-fertilization in L. formosanum compensates for inadequate pollinator

visitation across all levels of population size and for a pollen-limitation Allee effect due to

decreased mate availability in isolated plants, and may thus play an important role in invasion.

Key-words: abundance, aggregation, Baker’s Law, biological invasion, plant breeding

systems, pollen limitation, reproductive assurance, Sphingidae

Introduction

Insufficient fecundity may prevent invasion entirely or

reduce rate of spread of introduced species (Parker 1997),

especially when it arises as an Allee effect (Veit & Lewis

1996; Leung, Drake & Lodge 2004; Taylor et al. 2004). An

Allee effect occurs when low abundance reduces fecundity

or any other aspect of performance, often resulting in pop-

ulation growth rate becoming negative (Stephens, Suther-

land & Freckleton 1999). Inadequate pollen receipt (pollen

limitation) is a common cause of Allee effects in plants

that cannot self-fertilize (Knight et al. 2005; Gascoigne

et al. 2009). One of the main reasons for this is that smal-

ler, sparser and more isolated patches of plants are less

likely to be discovered by animal pollinators and, if discov-

ered, are less profitable for foraging (Sih & Baltus 1987;*Correspondence author. E-mail: [email protected]

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society

Functional Ecology 2013 doi: 10.1111/1365-2435.12093

Feinsinger, Tiebout & Young 1991; �Agren 1996; Groom

1998). Moreover, when a plant species occurs at very low

density, pollinators are likely to carry less or none of its

pollen, even if visitation per plant is not reduced (Duncan

et al. 2004). Thus, ability to self-pollinate may enhance

invasiveness in plants by mitigating Allee effects.

Ability to self-fertilize generally reduces or eliminates

pollen limitation (Kalisz, Vogler & Hanley 2004; Knight

et al. 2005; Eckert, Samis & Dart 2006; Brys et al. 2011).

Ability to self-fertilize should provide an ecological (and

evolutionary) advantage through increased reproduction,

so long as the benefits of selfing in terms of fecundity

(reproductive assurance benefits) outweigh the costs of

inbreeding depression. Inbreeding depression occurs when

progeny arising from selfing performs less well than those

from outcrossing (Jain 1976). As self-fertilization reduces

the availability of ovules and pollen for outcrossing, less-fit

selfed progeny may be produced at the expense of fitter

outcrossed progeny (gamete discounting; Lloyd 1992; Her-

lihy & Eckert 2002). As a result, ability to self-fertilize is

most likely to be advantageous when inbreeding depres-

sion and opportunities for outcrossing are both low.

Herbert Baker proposed that plants that can self-fertilize

should be better colonists than those that cannot, because

selfing would allow single individuals, isolated from mates

and pollinators by long distance dispersal, to found new

populations (Baker 1955, 1967). This principle, known as

Baker’s law or rule, has subsequently been expanded to

include invasive species. As introduced plants have to

reproduce successfully at low abundance along the leading

edge of an invasion, reproductive assurance through self-

fertilization should increase their likelihood of becoming

invasive. In other words, selfing may contribute to inva-

siveness by mitigating pollen-limitation Allee effects (van

Kleunen, Fischer & Johnson 2007; Ward, Johnson &

Zalucki 2012). This idea is consistent with evidence that

ability to self-fertilize is positively correlated with invasive

status and size of invaded range among introduced species

in several floras (van Kleunen & Johnson 2007; van Kleun-

en et al. 2008; Hao et al. 2011; Py�sek et al. 2011).

As invasive plants are frequently visited by pollinators

in the novel range (Richardson et al. 2000; Memmott &

Waser 2002; Py�sek et al. 2011), it is not clear to what

extent those that can self-fertilize actually depend on this

ability for their reproduction. Very few studies have

assessed the benefits of selfing in the introduced range, par-

ticularly in relation to plant abundance (Knight et al.

2005; Eckert, Samis & Dart 2006 although see van Kleun-

en, Fischer & Johnson 2007). It is therefore not generally

known whether animal pollination of invasive plants is less

reliable in small founder populations, such that plants in

these populations rely more on selfing. While mate avail-

ability and pollinator visitation may decline at different

rates as plant abundance decreases, their effects on cross-

pollen receipt are seldom distinguished (although see

Kunin 1993; Duncan, et al. 2004; Elam et al. 2007). A

functional approach incorporating both these processes

would allow us to understand why some plants are more

vulnerable to pollen-limitation Allee effects than others,

and predict in which plants self-pollination is most likely

to be important for fecundity and, in the introduced range,

invasiveness.

Lilium formosanum Wallace (Fig. 1) is an autonomously

self-pollinating and hawkmoth-pollinated geophyte that is

invasive in South Africa. We explored the contributions of

self-fertilization and pollinators to fecundity of this species

in its introduced range in South Africa, asking the follow-

ing specific questions: (i) What is the magnitude of repro-

ductive assurance benefits derived from self-fertilization?

(ii) Are reproductive assurance benefits greater in smaller

and more isolated populations of L. formosanum? (iii) Are

reproductive assurance benefits higher in isolated plants

than those in continuous patches? (iv) Do reproductive

assurance benefits increase with distance from continuous

patches? (v) Is any increase in reproductive assurance

benefits with isolation attributable to reduced pollinator

visitation or mate availability?

Materials and methods

STUDY SPEC IES

Lilium formosanum (Fig. 1) is a bulbous perennial plant with erect,

annual stems. Each stem terminates in an inflorescence of 1–8white, nocturnally scented, trumpet-shaped flowers (Rodger, van

Kleunen & Johnson 2010). In South Africa, its principal pollinator

is the native hawkmoth Agrius convolvuli (Fig. 1b; Rodger, van

Kleunen & Johnson 2010). Populations vary in self-compatibility

in its native range of Taiwan (Sakazono et al. 2012), and it is com-

pletely self-compatible and autonomously self-pollinating in its

introduced range in Japan (Inagaki 2002) and South Africa (Ram-

buda & Johnson 2004). A molecular-marker study in the native

range showed that fixation indices (Fis) of populations range from

0�032 to 0�901, suggesting variation among populations in mating

system (Hiramatsu et al. 2001). As no inbreeding depression is evi-

dent in progeny up to 3 years of age in the introduced range (Rod-

ger, van Kleunen & Johnson 2010; Rodger 2012), the reproductive

assurance benefits attained through selfing are likely to be impor-

tant for population growth and invasive spread.

POPULAT ION S IZE AND ISOLAT ION STUDY

Study region and populations

Experiments were conducted from January to March in 2005,

2006 and 2007 in naturalized populations in KwaZulu-Natal,

South Africa, 10–1700 m above sea level (Table A1, Supporting

information). Observations of hawkmoth scales on stigmas

(Fig. 1c) indicated that visitation of L. formosanum by these

insects occurs throughout the study region (J.G. Rodger, unpub-

lished results). Populations were mainly in disturbed grassland

adjacent to exotic tree plantations or on grassy road verges, with a

few in exotic forests or in otherwise pristine natural grasslands

and indigenous forests. Population size was taken as the number

of flowering stems. We used 50 m as the minimum separation dis-

tance between populations, allowing us to span a large range of

isolation from almost no separation to over 15 km from the near-

est population. An index of population isolation was calculated as

the log10 of the mean distance to the nearest three populations.

© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology

2 J. G. Rodger et al.

Data were obtained from 37 populations in 2005, 20 populations

in 2006 and 22 populations in 2007 (Table A1, Supporting infor-

mation). Most populations were accessible or available in only

one of the three study years, although eight populations were

studied in 2 or 3 years (Table A1, Supporting information).

Reproductive assurance benefits

Emasculation experiments can be used to distinguish between the

importance of self-pollination vs. pollinator-mediated cross-polli-

nation (Lloyd 1992; Eckert, Samis & Dart 2006). The reduction in

fecundity experienced by emasculated relative to intact flowers is a

measure of reproductive assurance benefits – in other words

dependence on self-pollination for fecundity (Schoen & Lloyd

1992; Kalisz & Vogler 2003). Lilium formosanum flowers were

emasculated by opening buds and removing anthers with alcohol-

sterilized forceps. For naturally pollinated controls, buds were

opened and forceps inserted. We considered it unlikely that emas-

culation would affect pollinator visitation to L. formosanum, as

hawkmoths do not forage for pollen and A. convolvuli readily vis-

its emasculated flowers (J.G. Rodger, pers. obs). This was con-

firmed by data that showed that the presence of lepidopteran

scales (Fig. 1c), a measure of pollinator visitation, did not differ

between stigmas of emasculated and intact flowers in three popu-

lations in 2006 and in four populations in 2007 (7–17 flowers per

treatment per population, J.G. Rodger, unpublished results).

A single bud was emasculated on each of three (2005 and 2007)

or 10 (2006) plants per population, and the same number of flow-

ers was similarly allocated as controls, except in four populations

for which we needed measures of within-population variation for

a separate study in 2007 (Table A1, Supporting information).

Control flowers were on separate plants to emasculated flowers in

2005 and on the same plants in other years. Because we emascu-

lated only a single flower per plant, pollinator-mediated geitonog-

amy could have contributed to fecundity of emasculated flowers,

making our estimates of reproductive assurance benefits conserva-

tive. However, this is unlikely to be important as preliminary anal-

yses indicated that fecundity of emasculated flowers was not

positively related to number of flowers per plant (J.G. Rodger,

unpublished results).

Thirty-four populations were used in 2005, 15 in 2006 and 22 in

2007. We chose low levels of replication within populations to

avoid a bias in sampling effort against small populations, first

because analysis of variance is less robust to unequal variance and

non-normality when data are unbalanced (Quinn & Keough 2002)

and secondly because the effective replicate for a relationship

between population attributes and plant performance is the popu-

lation, so statistical power is likely to be increased by maximizing

the number of populations at the expense of sample size per popu-

lation (Quinn & Keough 2002). We calculated the overall repro-

ductive assurance benefit of selfing for each year as the

proportional reduction in fecundity caused by emasculation:

RA = 100 9 (1 � emasculated/control) (Eckert, Samis & Dart

2006) with fecundity defined as seeds per flower (percentage fruit

set 9 mean seeds per fruit). The fecundity values used were grand

means of population means.

Pollen limitation

Pollen supplementation experiments were used to test for pollen

limitation in L. formosanum as autonomous self-pollination is not

necessarily sufficient to fertilize all ovules (Rodger, van Kleunen &

Johnson 2010). The same populations and the same sample-size

regimes were used as for emasculations, but different plants

(Table A1, Supporting information). Supplementation consisted

of saturating the stigma with outcross pollen from a plant at least

5 m away in the same population. Plants sometimes allocate

resources preferentially to flowers that have more fertilized ovules,

which can lead to overestimation of pollen limitation in pollen

supplementation experiments (Knight, Steets & Ashman 2006).

However, as pollen limitation was generally low in this study, any

overestimation would be quite small.

We calculated pollen limitation from seed per flower as

100 9 (1 � control/supplemented) (Larson and Barrett 2000).

(a) (b)

(c)

Fig. 1. Lilium formosanum growing in a

disturbed habitat (a), being pollinated by

the hawkmoth Agrius convolvuli (b) and

stigma showing hawkmoth scales and pol-

len (c). Scale bars are 87 mm (a), 27 mm

(b) and 1�3 mm (c).


Self-pollination mitigates Allee effects 3

Conducting emasculation and supplementation in the same popu-

lations also allowed us to assess how pollen limited L. formosanum

would have been, had it lacked the ability to self-fertilize. This is

termed pollinator failure and is calculated as 100 9 (1 � emascu-

lated/supplemented) (cf Kalisz & Vogler 2003).

Fruit and seed scoring

Fruits were harvested for seed counting at maturity, 10–12 weeks

after flowering. Seeds were counted if they contained an embryo

that was at least half the length of the seed, excluding the wing.

For each fruit, we measured the mass of the entire contents and

the mass and number of seeds in a random subsample containing

approximately 50 seeds and used this information to calculate

seeds per fruit. All seeds were counted in fruits containing fewer

than 50 seeds. Seeds per flower data (fruit set 9 seeds per fruit)

were zero inflated as there were many flowers that did not set

fruit. Fruit set and seeds per fruit were therefore analysed

separately.

Data analyses

Fruit set was analysed as a binomial response variable in general-

ized linear models incorporating a logit link function. Separate

analyses of the effects of emasculation and pollen supplementation

were carried out for each year, as most populations were used in

only 1 year. Fruit set did not need to be analysed for the supple-

mentation experiment in 2007 as there was 100% fruit set in both

treatments. Significance was assessed from quasi-F-statistics in

sequential analysis of deviance, analogous to F-statistics in ANOVA

with type I sums of squares (Payne 2011). Models included floral

manipulation (emasculation or supplementation) as a fixed factor,

population as a random factor, log10 population size and log10population isolation as covariates and population size-by-floral

manipulation and population isolation-by-floral manipulation

interactions. A type I approach was used because of the hierarchi-

cal structure of the data, with replicates occurring within popula-

tions and population size and isolation measured at the

population level. Terms were entered in the same order as they

appear in Tables 1 and 2. The order in which terms are entered

may affect their significance in sequential analyses. Nevertheless,

reversing the order of population size and isolation, and the popu-

lation size 9 floral manipulation and population isolation 9 flo-

ral manipulation interactions gave very similar results to those

presented here and did not affect the conclusions drawn from

them (J.G. Rodger, unpublished results). Population size and iso-

lation were tested against population, and other terms were tested

against the residual. Where models were not overdispersed (i.e.

where residual deviance � residual d.f.) we assumed residual

mean deviance = 1 for the purposes of calculation of quasi-

F-ratios, and when models were overdispersed we used the model-

calculated residual mean deviance (Payne 2011). Model validation

consisted of checking plots of residuals against fitted values for

patterns (Zuur et al. 2009).

Seeds per fruit was analysed in restricted maximum likelihood

(REML) analysis of variance to accommodate differences in sam-

ple size between populations. REML analysis of variance used the

same statistical design as the generalized linear model for fruit set

except they also included the population-by-floral manipulation

interaction as a random effect. Significance was evaluated using

Wald F-statistics for the fixed terms. For random terms, the

change in deviance in the models when a term was dropped was

compared with a chi-squared distribution with one degree of

freedom (Payne, Welham & Harding 2011). Residual plots were

examined to check whether assumptions were met.

ARRAY EXPER IMENT

Array layout

To test whether reproductive assurance was greater for plants iso-

lated from continuous patches and, if so, whether this was due to

decreased visitation or mate availability, we created arrays of

emasculated and intact plants transplanted either into central

patches of L. formosanum or similar grassland habitat that was

isolated from the patches. Plants used were sourced from the same

populations. Two populations with discrete patches of L. formosa-

num in open habitat (mainly natural grassland) were selected for

experiments in February and March 2009. At Baynesfield (29

45�162S, 30 21�377E, Alt. 810 m), there was a population consist-

ing of a single large patch of 748 plants. In the Karkloof popula-

tion (29 20�229, 30 17�527, Alt. 1100 m), four patches of 67–610

Table 1. Significance levels from generalized linear models for fruit set and REML analysis for seeds per fruit in emasculation experiments

across a range of populations differing in size and isolation. Full tables are in Appendix S1 (see Supporting information). Test statistics

are Quasi-F-statistics (ratios of mean changes in deviance) for fruit-set analyses, Wald F-statistics for fixed effects in seed-set analyses and

change in deviance (tested against the chi-squared distribution) for random effects (P, P 9 E) in the seed-set analyses. Residual mean

deviance shown in brackets for fruit-set analyses

Effect

Fruit set Seeds per fruit

2005 2006 2007 2005 2006 2007

d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic

PS 1,30 0�03 1, 11 0�44 1, 18 4�24 1, 18 6�19 1, 10 0�6 1, 19 2�61PI 1, 30 1�23 1, 11 4�21 1, 18 8�75** 1, 22 0�49 1, 10 0�01 1, 18 2�85P† 30, 30 1�60 11, 11 1�64 18, 17 0�67 1 3�14 1 27�97*** 1 15�79***E 1, 30 11�45** 1, 11 5�00* 1, 17 6�81* 1, 16 113�13*** 1, 7 7�33* 1, 16 54�26***PS 9 E 1, 30 0�76 1, 11 0�03 1, 17 3�94 1, 16 8�31* 1, 10 0�29 1, 19 0�02PI 9 E 1, 30 5�72* 1, 11 7�14* 1, 17 3�22 1, 20 4�29 1, 6 2�76 1, 17 0�02P 9 E† 1 0�18 1 1�94 1 5�17*Residual 30 (1�20) 11 (0�43) 17 (2�1 9 10�5)

PS, population size; PI, population isolation; P, population; E, emasculation.

P < 0�1; * P < 0�05; ** P < 0�01; ***P < 0�001.†Random effects.



plants were used. The array experiments were conducted from 31

January to 14 February 2009 at Baynesfield and from 28 February

to 10 March 2009 at Karkloof. We obtained data from 87 plants

at Baynesfield and 59 at Karkloof.

Emasculated and intact plants were placed singly inside contin-

uous patches or in isolated pairs outside of these patches (Fig. C1,

Supporting information). Isolated pairs consisted either of two

emasculated plants or an emasculated plant and an intact plant,

1 m apart, to distinguish between effects of isolation on reproduc-

tive assurance benefits through reductions in pollinator visitation

vs. mate availability. This approach is original to this study. Dis-

tances between successive pairs were chosen randomly from

increasing intervals of the log2 scale (2–4, 4–8, 8–16…), so that as

distance away from the central patch increased, density decreased

as well. Distance from central patches ranged from 3 to 702 m at

Baynesfield and 3 to 561 m at Karkloof. After flowering, all trans-

planted individuals were re-excavated and brought back to the

University of KwaZulu-Natal Pietermaritzburg campus and main-

tained in plant pots until fruits were mature.

Isolation

To test whether reproductive assurance compensated for reduced

cross-pollen receipt in isolated plants, we compared fecundity in

emasculated and intact plants placed inside central patches and in

isolated pairs. Statistical analyses of fruit set and seeds per fruit

were again conducted separately. Reproductive assurance indices

were calculated for plants inside patches. Fruit set was analysed

in generalized linear models as before, but with number of flow-

ers (per plant) as the binomial total in an events/trials structure

(Payne 2011). Using a type I analysis allowed us to test for the

effect of distance from central patch after accounting for the

effect of isolation (inside vs. outside patches). Terms in order of

entry were isolation, distance from patch (log10 transformed),

emasculation (intact vs. emasculated), emasculation-by-isolation,

emasculation-by-distance. Distance was scored as zero for plants

inside patches. For seeds per fruit, mean values were calculated

for each plant, log10-transformed to improve homogeneity of var-

iance and analysed in REML analysis of variance as sample sizes

were unbalanced. The same model was used as described previ-

ously for fruit set. Terms were sequentially added to a model,

and the significance of these terms was evaluated from Wald

F-statistics.

Mate availability

To distinguish between effects of reduced mate availability vs. pol-

linator visitation on reproductive assurance benefits in isolated

plants, we compared fecundity of emasculated plants inside popu-

lations, isolated and paired with another emasculated plant or iso-

lated and paired with an intact plant as a test for the effect of mate

availability. Fruit set and seeds per fruit were analysed using gen-

eralized linear models and REML analysis of variance as described

above. Analyses included mate presence as a fixed factor, distance

as a continuous variable and the mate presence-by-isolation dis-

tance interaction. As appreciable heterogeneity of variance

remained for seeds per fruit, even after transformation, we con-

ducted pairwise comparisons between groups with Mann–Whitney

U-tests. Although corrections for multiple comparisons are some-

times applied for pairwise comparisons, we have not done so

because in this case each comparison tests a different hypothesis,

so the multiple comparisons do not inflate type 1 error.

Scale and pollen deposition

We also addressed the question of whether isolated plants experi-

enced decreased pollinator visitation or mate availability by scoring

emasculated flowers for the presence of lepidopteran scales, an indica-

tion of visitation, and presence of pollen on stigmas, an indication of

successful pollination, using a 20X hand lens. Each plant was scored

once, 3–4 days after transplanting, for all flowers that had been open

for at least one night. Scale and pollen deposition were analysed in

general linear models for binomial data with a logit link function

including isolation as a fixed factor and distance as a covariate.

All statistical analyses were performed in Genstat 12.1 (VSN

International, Hemel Hempstead, UK).

Results

POPULAT ION S IZE AND ISOLAT ION STUDY

Reproductive assurance benefits

Emasculation significantly reduced fruit set and number

of seeds per fruit in naturalized populations in all 3 years,

Table 2. Significance levels from generalized linear models for fruit set and REML analysis for seeds per fruit in pollen supplementation

experiments across a range of populations differing in size and isolation. Full tables are in Appendix S1 (see Supporting information). Test

statistics are Quasi-F-statistics (mean change in deviance) for fruit set analyses, Wald F-statistics for fixed effects in seed-set analyses and

change in deviance (tested against the chi-squared distribution for random effects in the seed-set analyses. Residual mean deviance shown

in brackets for fruit-set analyses. 2007 data were not analysed for fruit set as all replicates of both treatments set fruit in this experiment

Effect


2005 2006 2005 2006 2007

d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic

PS 1, 32 4�19* 1, 12 1�37 1, 25 0�77 1, 12 1�21 1, 14 0�21PI 1, 32 0�24 1, 12 3�11 1, 27 2�01 1, 10 0�54 1, 15 2�87P† 32, 32 2�37** 12, 12 0�78 1 7�70** 1 19�18*** 1 28�09***S 1, 32 0�03 1, 12 0�02 1, 74 5�86* 1, 138 1�71 1, 134 0�26PS 9 S 1, 32 4�33* 1, 12 0�77 1, 75 2�04 1, 139 2�13 1, 134 0�03PI 9 S 1, 32 1�21 1, 12 2�36 1, 76 0�02 1, 138 0�48 1, 134 0�98P 9 S† 1 0�00 1 0�00 1 0�00Residual 32 (20�29) 12 (3�7 9 10�4)

PS, population size; PI, population isolation; P, population; S, supplementation.

*P < 0�05; **P < 0�01; ***P < 0�001; †, random effects.



with a mean reduction in total fecundity (reproductive

assurance benefits) of 67%: 90% in 2005, 45% in 2006

and 66% in 2007 (Table 1; Fig. B1, Supporting informa-

tion). The effect of emasculation was not greater in

smaller or more isolated populations except that there

was a greater effect of emasculation in more isolated

populations for fruit set in 2005 (Table 1; Figs 2 and 3).

In other cases where there were significant population

size-by-emasculation and isolation-by-emasculation inter-

actions, these were not attributable to fruit set or seeds

per fruit declining more for emasculated than control

flowers as population size decreased or isolation increased

(Table 1; Figs 2 and 3).

Pollen limitation

Pollen supplementation increased fecundity (indicating

pollen limitation) by an average of 12% (16% in 2005,

11% in 2006 and 10% in 2007), but this was only signifi-

cant in 2005 (Table 2; Fig. B1, Supporting information).

A significant supplementation-by-population size interac-

tion in this year showed that supplementation increased

fruit set only in smaller populations (Table 2; Fig. B2,

Supporting information). There was no evidence for any

effect of population isolation on pollen limitation as the

interaction between population isolation and pollen sup-

plementation was never significant (Table 2; Fig. B3, Sup-

porting information). Pollinator failure was estimated as

92% in 2005, 48% in 2006 and 72% in 2007.

ARRAY EXPER IMENT

Isolation

Fruit set and seeds per fruit were significantly lower in

emasculated than in intact plants for both the Baynesfield

and Karkloof sites (Table 3; Fig. 4). Indices of reproduc-

tive assurance were 75% for plants inside continuous

patches and 96% for isolated plants at Baynesfield; 80%

inside patches and 84% for isolated plants at Karkloof. At

Baynesfield, emasculation reduced seeds per fruit more

strongly in isolated plants than those in populations [sig-

nificant isolation-by-emasculation interaction – with a

nonsignificant trend in the same direction for fruit set

(Table 3; Fig. 4a,b)]. However, at Karkloof, the effect of

emasculation on fruit set and seeds per fruit was not

related to isolation (Table 3; Fig. 4c,d). The effect of emas-

culation on fruit set and seeds per fruit did not increase

0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0

0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0 0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0 0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0

0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0 0·0 0·5 1·0 1·5 2·0 2·5 3·0 3·5 4·0

Pro

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on fr

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et

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

1·2

(a)

2005PSns

E**PS . Ens

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

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EmasculatedControl

(b)

2006PSns

E*PS . Ens

(c)

2007

PS†

E*PS.E†

(d)PS*E***PS . E*

(e)PSns

E*PS . Ens

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

1·2

(f)PSns

E***PS . Ens

See

ds p

er fr

uit

0

200

400

600

800

1000

1200

1400

1600

Log10 population size

0

200

400

600

800

1000

1200

1400

1600

0

200

400

600

800

1000

1200

1400

1600

Fig. 2. Fruit set (model adjusted, a–c) and seeds per fruit (d–f) of emasculated and intact, naturally pollinated plants in relation to popula-

tion size for 3 years. PS, population size, E, emasculation; ns, nonsignificant; †P < 0�1; *P < 0�05; **P < 0�01; ***P < 0�001. Circles repre-sent predicted values for populations for fruit set (adjusted for population isolation) and mean populations values for seeds per fruit.

Regression lines shown for seeds per fruit.



with distance of isolation in either population (Table 3;

Fig. C2, Supporting information). Although the distance-

by-emasculation interaction was significant for seeds per

fruit at Baynesfield, the effect of emasculation actually

decreased with distance due to an outlier (Fig. C2,

Supporting information).

Mate availability

Mate availability had a significant effect on fruit set at

Baynesfield (Table 3): isolated emasculated plants with no

mates available (i.e. with an emasculated partner) had sig-

nificantly lower fruit set than those inside populations

(two-tailed t-tests; t = 2�96, d.f. = 48, P = 0�009) or iso-

lated with a potential mate (intact partner, t = 2�07,d.f. = 48, P = 0�044). Isolated plants with intact partners

did not differ significantly from those in continuous popu-

lations (t = 1�08, d.f. = 48, P = 0�286). In isolated plants

at Baynesfield, seeds per fruit was not affected by mate

availability although it did increase with isolation distance

(Table 3; Fig. 5), contrary to the expectation of decreased

pollen transfer in more isolated plants (Table 3; Fig. C3,

Supporting information). At Karkloof, mate availability

had a significant effect on seeds per fruit (Table 3;

Fig. 5d): emasculated plants with no mates available

(emasculated partner) had fewer seeds per fruit than those

inside populations (Mann–Whitney U-test u = 0�5,P = 0�019, n = 4, 6) or isolated with a potential mate(u = 0�0, P = 0�016, n = 4, 5). Isolated plants with intact part-ners did not differ significantly from those in continuouspopulations (u = 13, P = 0�792, n = 6, 5).

Scale and pollen deposition

Scale deposition was not related to isolation or distance at

either Baynesfield or Karkloof (Table 3). Isolated plants

had significantly lower pollen receipt than those in the

main patch at Baynesfield (Table 3), but not at Karkloof

(Table 3).

Discussion

These results show that L. formosanum relies heavily on

self-fertilization for fecundity even though it has an effective

hawkmoth pollinator in its invasive range (Rodger, van

Kleunen & Johnson 2010). On average, reproductive assur-

ance benefits from self-pollination, as assessed by floral

emasculations, accounted for 67% of the total fecundity of

naturally occurring plants, but this did not vary according

to population size, contrary to expectations from other

2·5 3·0 3·5 4·0 4·5

2·5 3·0 3·5 4·0 4·5 2·5 3·0 3·5 4·0 4·5 2·5 3·0 3·5 4·0 4·5

2·5 3·0 3·5 4·0 4·5 2·5 3·0 3·5 4·0 4·5

Pro

porti

on fr

uit s

et

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

1·2

1·4

2005

PIns

E**PI . E*

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

1·2

1·4

2006

PIE*PI . E*

2007

PI**E*PI.E

PIns

E***PI . E

PIns

E*PI . Ens

–0·2

0·0

0·2

0·4

0·6

0·8

1·0

1·2

1·4

EmasculatedControl

PIns

E***PI . Ens

See

ds p

er fr

uit

0

200

400

600

800

1000

1200

1400

1600

Log10 population isolation

0

200

400

600

800

1000

1200

1400

1600

0

200

400

600

800

1000

1200

1400

1600

(a) (b) (c)

(d) (e) (f)

Fig. 3. Fruit set (model adjusted, a–c) and seeds per fruit (d–f) of emasculated and intact naturally pollinated plants in relation to popula-

tion isolation for 3 years. PI, population isolation [mean distance (m) to nearest three populations], E, emasculation; ns, nonsignificant;†P < 0�1; *P < 0�05; **P < 0�01; ***P < 0�001. Circles represent predicted values for populations for fruit set (adjusted for population

size) and mean populations values for seeds per fruit. Curves for fruit set were fit in generalized linear models using logit-transformed data

and back-transformed.



studies that show component Allee effects via a decrease in

animal-mediated pollination in small populations (�Agren

1996; Groom 1998; Brys et al. 2011). The 71% average esti-

mate of pollinator failure shows that L. formosanum would

be highly pollen limited if it was self-incompatible.

Although we have previously documented variation in the

ability of L. formosanum to self-pollinate autonomously in

the study region, the fact that pollen supplementation

increased fecundity by only 12% on average indicates that

most populations have high levels of autofertility.

There was no evidence for an effect of population size on

reproductive assurance benefits in the survey of natural pop-

ulations, indicating that population size did not affect polli-

nator visitation (Table 1; Fig. 2). However, reproductive

assurance mitigated a detectable Allee effect for isolated

plants lacking nearby mates in the array experiment

Frui

t set

0·0

0·2

0·4

0·6

0·8

1·0

Frui

t set

0·0

0·2

0·4

0·6

0·8

1·0

8

9

19

9 12

812

16

Inside patch Isolated


Mea

n se

eds

per f

ruit

0

200

400

600

800

IntactEmasculated

8

17

7

6

Mea

n se

eds

per f

ruit

0

200

400

600

800

1000

1200

9

11

6 10



Isol *Dist *Emas ***E × I nsE × D ns

Isol nsDist nsEmas ***E × I nsE × D ns

Isol nsDist nsEmas ***E × I *E × D *

Isol nsDist nsEmas ***E × I nsE × D ns

(a) (b)

(c) (d)

Fig. 4. Fruit set and seeds per fruit for

emasculated and intact plants in array

experiment at Baynesfield (a, b) and Kark-

loof (c, d). For fruit set (a, c), bars repre-

sent means of fruit-set values for individual

plants. For seeds per fruit (b, d), back-

transformed means and error bars are plot-

ted. Numbers above bars are numbers of

plants.

Table 3. Significance levels from generalized linear models for fruit set, scale deposition and pollen deposition and REML analyses for

seeds from array experiments on Lilium formosanum. Test statistics are Quasi-F-statistics (mean change in deviance) for fruit-set, pollen

and scale analyses, Wald F-statistics for fixed effects in seed-set analyses and change in deviance (tested against the chi-squared distribu-

tion) for random effects in the seed-set analyses. Residual mean deviance shown in brackets for fruit-set, pollen and scale analyses

Effect


Baynesfield Karkloof Baynesfield Karkloof

d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic d.f.

Test

statistic

Emasculation analyses

Isolation 1, 46 4�49* 1, 35 0�23 1, 32 0�37 1, 30 0�02Distance 1, 46 4�93* 1, 35 0�24 1, 32 0�3 1, 30 1�34Emasculation 1, 46 80�41*** 1, 35 16�37*** 1, 32 31�07*** 1, 30 23�32***E 9 I 1, 46 1�36 1, 35 0�04 1, 32 7�31* 1, 30 0�15E 9 D 1, 46 0�02 1, 35 0�305 1, 32 6�54* 1, 30 0�01Residual 46 (1�02) 35 (1�1)Mate availability analyses

Distance 2, 46 5�28** 2, 30 0�84 2, 17 0�38 2, 10 7�09*Donor presence 1, 46 0�06 1, 30 0�58 1, 17 5�67* 1, 10 0�03DP 9 D 1, 46 0�00 1, 30 0�60 1, 17 0�03 1, 10 0�17Residual 46 (1�72) 30 (1�52)Pollen and scale analyses

Scales Pollen

Isolation 1, 26 0�03 1, 22 1�08 1, 26 25�88*** 1, 22 0�01Distance 1, 26 0�51 1, 22 0�02 1, 26 0�00 1, 22 1�31Residual 26 (2�67) 22 (1�47) 26 (0�65) 22 (1�77)

*P < 0�05; **P < 0�01; ***P < 0�001



(Fig. 5). Reproductive assurance benefits were greater for

isolated plants than those placed in continuous populations

at only one of the two sites (Baynesfield, Fig. 4a,b). How-

ever, in both populations, emasculated plants that were iso-

lated with no potential mate (i.e. placed next to another

emasculated plant) had lower fecundity than those isolated

with a single intact plant nearby, or placed in continuous

populations. This shows that the greater reproductive assur-

ance benefits for isolated plants at Baynesfield were due to

decreased mate availability, not reduced pollinator visita-

tion (Table 3, Fig. 5a,d). Findings of lower stigmatic pollen

deposition on isolated than on nonisolated plants at Baynes-

field and the lack of effect of isolation on lepidopteran scale

deposition on stigmas (Table 3) support this conclusion.

As pollen limitation of self-incompatible plants is gener-

ally higher in the introduced than in the native range

(Burns et al. 2011), it can be expected that invasive plants

obtain substantial reproductive assurance benefits from

selfing. However, no reproductive assurance benefits were

found in hummingbird pollinated Nicotiana glauca plants

invasive in North America (Schueller 2004), while large

reproductive assurance benefits were found in hawkmoth-

pollinated Lilium formosanum (RA = 67%, this study) and

Datura stramonium (RA = 83%, van Kleunen, Fischer &

Johnson 2007). Clearly, more studies spanning a range of

pollination systems, geographic areas and life forms are

needed before it will be possible to assess the importance

of selfing for fecundity of introduced plants generally.

Mitigation of increased mate limitation by selfing in iso-

lated plants, as demonstrated in the array experiment

(Fig. 5), could be especially important for invasion of L.

formosanum, given that reproduction by isolated individu-

als should have a dramatic impact on the invasion process

(Kot, Lewis & Driessche 1996; Clark, Lewis & Horvath

2001). We are not aware of any previously published stud-

ies showing that selfing mitigates mate-limitation Allee

effects in invasive species, and only one for a native species

(Brys et al. 2011). Indirect evidence from some studies of

the effect of plant abundance on fecundity suggests that

mate limitation may generally be more important than

reduced pollinator visitation in reducing cross-pollen

receipt of isolated individuals (Kunin 1993; Duncan, et al.

2004; Elam et al. 2007). This is one of the first studies to

distinguish between mate availability and pollinator visita-

tion components of Allee effects, yet this approach is

essential for deriving the functional understanding that

would allow us to predict which plants should be most vul-

nerable to Allee effects, and to allow more refined predic-

tions about the effects of reproductive assurance and

pollen limitation on invasiveness.

The absence of a detectable effect of plant abundance on

hawkmoth visitation to L. formosanum is consistent with

some other studies of hawkmoth-pollinated plants (e.g.

Johnson, Torninger & �Agren 2009) and contrasts with

results for plants with other pollinators (�Agren 1996;

Groom 1998; Brys et al. 2011). This could be because

hawkmoths are more nomadic in their movements and

opportunistic in their foraging than other pollinators (as

suggested by Johnson, Torninger & �A 2009) or because

foraging primarily by olfactory rather than visual cues ren-

ders them less capable of assessing population size prior to

arrival in populations.

Conclusions

We have used a functional approach to assess the relation-

ship between plant abundance and reproductive assurance

benefits in L. formosanum, distinguishing between effects

of pollinator visitation and mate availability as well as

between isolation and population size. Although we found

Frui

t set

0·0

0·2

0·4

0·6

0·8

1·0

Frui

t set

0·0

0·2

0·4

0·6

0·8

1·0

19

15

9

9

Single None

See

ds p

er fr

uit

0

100

200

300

400

500

7

3

See

ds p

er fr

uit

0

50

100

150

200 5

4

Single None

Mate **Dist nsD × M ns

Mate nsDist nsD × M ns

Mate nsDist *D × M ns

12

6

9

8

Many Single NoneMany

Single NoneManyMany

Mate *Dist nsD × M ns

Mate availability

(a) (b)

(c) (d)Fig. 5. Fruit set (a, c) and seeds per fruit

(b, d) of emasculated plants at different lev-

els of mate availability in array experiment

at Baynesfield (a, b) and Karkloof (c, d).

For fruit set, bars represent means of fruit

set values for individual plants. For seeds

per fruit, back-transformed means and

standard errors of plant means on log2scale shown. Numbers above bars are num-

bers of plants. For seeds per fruit, all fruits

had at least one seed.



no evidence that pollinator visitation was related to abun-

dance, our finding that selfing mitigated decreased mate

availability in isolated plants is, to the best of our knowl-

edge, the first evidence that selfing may contribute to inva-

siveness by mitigating an Allee effect. Because of this

finding, because reproductive assurance benefits are high

even in the absence of Allee effects, and because progeny

trials have revealed almost no evidence for inbreeding

depression in L. formosanum in South Africa (Rodger, van

Kleunen & Johnson 2010; Rodger 2012), reproductive

assurance benefits may well translate into a demographic

advantage. This makes it likely that ability to self-pollinate

contributes to the invasiveness of L. formosanum. Demo-

graphic analysis will be required to assess the effect of sel-

fing on invasiveness, and the relative importance of its

compensating for generally inadequate pollinator visitation

vs. mate limitation in isolated individuals.

Acknowledgements

Thanks to Dalton Nyawo for assistance with seed counting, Wade Shrives

for assistance with floral manipulations and Ben Khumalo for help setting

up the arrays. We are grateful to Craig Morris, Mike Ramsey and Law-

rence Harder for statistical advice and to Karl Duffy, Chris Eckert, Eliza-

beth Elle, Taina Witt and Lorne Wolfe for comments on previous drafts of

this manuscript. We also thank Baynesfield Estates, the Engelbrechts and

the Shaws for permission to work on their properties and UKZN Botanical

Garden for space to maintain plants. This study was supported by the

DST-NRF Centre of Excellence for Invasion Biology (CIB).

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Received 10 October 2012; accepted 25 February 2013

Handling Editor: Diane Campbell

Supporting Information

Additional Supporting Information may be found in the online

version of this article:

Appendix S1. Supplementary tables and figures.



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