Skip to main content
NCBI home page
AoB Plants logoLink to AoB Plants
. 2018 Jan 17;10(1):ply002. doi: 10.1093/aobpla/ply002

The relative contribution of diurnal and nocturnal pollinators to plant female fitness in a specialized nursery pollination system

Giovanni Scopece 1,✉, Lucia Campese 1, Karl J Duffy 1,2, Salvatore Cozzolino 1
PMCID: PMC5800057  PMID: 29435209

Nursery pollination is an unusual plant–insect interaction in which an insect is both pollinator and seed predator. Depending on the abundance of the nursery pollinator and of other pollinators, this interaction can range from mutualism to parasitism and it is thus likely to vary geographically. We investigated this mechanism in the widespread species Silene latifolia in a Mediterranean environment that is likely to offer a rich pollinator community to the plant, thus decreasing the dependence on the nursery pollinator. Surprisingly, we found that although generalist pollinators contribute significantly to plant fitness, the nursery pollinator is still the more efficient.

Keywords: Hadena bicruris, moth pollination, mutualism, nursery pollination, parasitism, pollination syndrome

Abstract

Plants involved in specialized pollinator interactions, such as nursery pollination, may experience trade-offs in their female fitness, as the larvae of their pollinators may also consume seeds produced by the flowers they pollinate. These interactions could potentially shift between mutualism and parasitism, depending on the presence and abundance of both the nursery pollinator and of other pollinators. We investigated the fitness trade-off in a Mediterranean plant (Silene latifolia), which has a specialist nocturnal nursery pollinator moth (Hadena bicruris) and is also visited by several diurnal pollinators. We estimated the pollination rates and fecundity of S. latifolia in both natural and experimental populations in the Mediterranean. We estimated natural pollination rates in different flowering times and with presence/absence of the H. bicruis moth. Then by exposing plants to each pollinator group either during the day or at night, we quantified the contribution of other diurnal pollinators and the specialized nocturnal nursery pollinator to plant female fitness. We found no difference in plant fruit set mediated by diurnal versus nocturnal pollinators, indicating that non-specialist pollinators contribute to plant female fitness. However, in both natural and experimental populations, H. bicruris was the most efficient pollinator in terms of seeds produced per fruit. These results suggest that the female fitness costs generated by nursery pollination can be overcome through higher fertilization rates relative to predation rates, even in the presence of co-pollinators. Quantifying such interactions is important for our understanding of the selective pressures that promote highly specialized mutualisms, such as nursery pollination, in the Mediterranean region, a centre of diversification of the carnation family.

Introduction

The availability and abundance of effective pollinators is a key factor in determining the fitness of animal-pollinated plants (Stephenson 1981; Muchhala 2003; Muchhala et al. 2009). Hence, it has been predicted that plants should evolve towards pollinator specialization by adapting to the more abundant and/or more effective pollinator species (Stebbins 1970; Crepet 1983; Schemske and Horvitz 1984). Despite this prediction, several studies that investigated pollinator-mediated selection on floral traits have demonstrated more complex and sometimes contradictory results (Morse and Fritz 1983; Jennersten 1988; Thompson and Pellmyr 1992; Groman and Pellmyr 1999; Herrera 2000; Young 2002; Wolff et al. 2003). This suggests that most specialized interactions are not a mere adaptation to the most effective pollinator or pollinator functional class (sensuFenster et al. 2004) but selection may also favour floral traits that attract new pollinators without excluding previous ones (Waser et al. 1996; Aigner 2001, 2004; Fenster et al. 2004). This is the case, for instance, in plant species with both diurnal and nocturnal pollinators, which are adapted to main pollinators active in a specific time of the day, but also exploit co-pollinators acting in the alternative day period (Giménez-Benavides et al. 2007). In addition, pollinator availability in geographically widespread plants may vary among different environments (Herrera 1988; Fenster and Dudash 2001), thus producing locally divergent pollinator-mediated selection on already evolved flower traits (Bustamante et al. 2010). Consequently, the overall evolution of floral traits in a species can be the result of adaptation to many pollinators, even though individual populations at any moment in time would be continuously adapting to one or a few local pollinators (Dilley et al. 2000).

One of the more extraordinary examples of specialized plant–insect interactions is the nursery pollination system, where insects lay eggs and rear larvae in the fruit that resulted from their pollination (Thompson and Pellmyr 1992). This interaction, with varying degrees of specialization, has evolved independently in several plant lineages (Reynolds et al. 2012). In some cases, it is a strictly specialized system in which insect and plant traits are highly co-adapted (e.g. Yucca and Tegeticula, Phyllanthaceae and Epicephala, Ficus and Agaonidae wasps mutualisms; Pellmyr 2003; Kawakita 2010) to the extent that groups of plants and nursery pollinators involved in this interaction show parallel cladogenesis (Kawakita et al. 2004; Althoff et al. 2012; Cruaud et al. 2012). In other cases, plant–insect interactions are more general and reflect a less specialized stage of potential mutualism that can also shift to parasitism depending on the presence of effective co-pollinators (Dufay and Anstett 2003). This latter situation describes the interaction of night-pollinated Silene latifolia with its nursery pollinating Hadena bicruris moth (Brantjes 1976). These two species are widely distributed in Europe and occur in a range of different habitats (Bopp and Gottsberger 2004). However, most studies on S. latifolia have been conducted in non-native regions (mainly the USA) where S. latifolia has been introduced, but H. bicruris does not occur (Young 2002; Castillo et al. 2014), or in the northern part of its distributional range (Jürgens et al. 1996; Bopp and Gottsberger 2004; Dötterl et al. 2006; Burkhardt et al. 2012; Magalhaes and Bernasconi 2014). In these regions, the flowering time of S. latifolia closely matches with the period in which H. bicruris occurs in its adult phase. Indeed, previous work from north European population has shown that S. latifolia relies mainly on H. bicruris (Jürgens et al. 1996; Witt et al. 1999; Bopp and Gottsberger 2004; Dötterl et al. 2006).

In contrast, due to warmer climates in the Mediterranean, S. latifolia has a long flowering time spanning well beyond the emergence period of adult H. bicruris moths (Prieto-Benítez et al. 2017), hence there is a greater abundance of other insect taxa that may visit S. latifolia over its flowering season. Although S. latifolia has a typical moth pollination syndrome (e.g. pale flowers, scent emitted at night), diurnal flower visitors have been frequently recorded on flowers in the Mediterranean, which suggests that diurnal visitors may play a role in the pollination of S. latifolia. Indeed, given that it feeds on developing seeds of S. latifolia, the net effect of H. bicruris on the fitness of S. latifolia should be considered in the light of the pollination provided by other pollinators. As a consequence, the S. latifolia–H. bicruris interaction could potentially shift between mutualism and parasitism, depending also on variation in the services of secondary pollinators (Dufay and Anstett 2003; Giménez-Benavides et al. 2007).

We investigated pollination and reproductive success of S. latifolia in two Mediterranean populations, one with H. bicruris pollinators and one lacking them. Then we induced two pollination regimes at non-overlapping day–night periods in experimental plant populations in order to understand the relative importance of diurnal versus nocturnal pollinators. We compared their effects on plant reproductive success in terms of fruit and seed set. In this study, we specifically addressed the following questions: (i) Do natural populations of S. latifolia predated and non-predated by H. bicruris differ in seed set? (ii) Does the presence of H. bicruris enhance S. latifolia pollination efficiency? (iii) To what extent does S. latifolia depend on diurnal pollinators?

Methods

Study species

The white campion S. latifolia (= Silene alba) (Caryophyllaceae) is a short-lived perennial, dioecious plant native to Eurasia (Delph et al. 2002). Nocturnal insects (moths) and diurnal insects (e.g. hoverflies, bees, beetles) have been recorded as floral visitors. However, the specialist seed predating moth H. bicruris (Lepidoptera) is considered its main pollinator (Jürgens et al. 1996). Typically, female moths lay one egg per flower in female plants; once the larva emerges, it consumes the developing seeds within this primary fruit (i.e. the fruit of the flower in which the egg was laid). To complete development, one larva will consume 2–4 additional secondary fruits (i.e. fruits that the larvae move to and attack after leaving the primary fruit; Elzinga et al. 2005) on the same plant. Thus, only plants that have been primarily attacked experience secondary attacks. Moths discriminate between male and female plants and, as a rule, lay eggs in flowers on females (Brantjes 1976; Labouche and Bernasconi 2010).

Natural populations

Between May and June 2011, we surveyed two natural populations located in Southern Italy (University Campus of Monte Sant’Angelo, Naples, hereafter referred to as MSA and Battipaglia, Salerno, hereafter referred to as BATT). For each randomly sampled individual, we recorded the number of seeds per fruit and the predation by H. bicruris. Predation was evaluated by recording the number of fruits showing presence of H. bircuris larvae. Fruits attacked by H. bicruris can be easily recognized either by the presence of a hole in the side of the fruit (a primary seed fruit) or by the presence of a large round hole on the top (a secondary seed fruit) (Elzinga et al. 2005). Those fruits directly predated by H. bicruris were excluded from seed set comparisons.

In a series of observations carried out during the month of May, we also collected and identified the most common diurnal floral visitors of S. latifolia in MSA. To do this, we randomly selected a patch of S. latifolia individuals and observed them for ~2 h at different times of the day between 8 and 19 h. Insects observed approaching flowers were captured with an insect net, killed and stored for subsequent identification. For all samples, the time of collection was recorded.

In 2013, in the MSA population, we estimated fruit and seed set of S. latifolia in terms of number of fruits produced and number of seeds per fruit during three consecutive months (sampling dates: 21 April, 15 May and 18 June) and recorded the rate of H. bicruris infestation over time. To do this, we quantified the total number of fruits produced and the number of fruits predated by H. bicruris in 21 (April), 19 (May) and 21 (June) plants, respectively. We then randomly selected five fruits on each sampled plant that showed no direct infection of H. bicruris and counted the seeds. In each month, we selected new flowering individuals in order to avoid re-collecting fruits persisting on plants, and to be sure that the collected fruits were produced by flower pollination in the sampling month.

Pollinator exclusion experiment

In 2011, a total of 72 four-month-old S. latifolia plants were grown following Cozzolino et al. (2015) from seeds collected in the MSA population. Only female plants were used to test for the presence and effectiveness of diurnal and nocturnal pollinators by performing three treatments. To examine the effect of diurnal pollinators on female fitness, we covered 18 individuals with a small cage (2 mm mesh) every evening at dusk, and removed it the next morning at 8.00 a.m., repeating this process until all the flowers on those plants had completed flowering. Simultaneously, we performed the opposite experiment to test for nocturnal pollination: covering the nocturnal plants (17 individuals) every morning and removing cages in the evening. A set of 37 plants was used as a control treatment and was exposed to both diurnal and nocturnal pollinators. The rate of H. bicruris predation was measured as outlined above. All mature fruits were counted and collected from plants of the three treatments for subsequent seed counting.

Statistical analyses

In the natural populations (MSA and BATT), we compared plants predated and non-predated by H. bicruris in terms of mean number of seeds per fruit. Further, in the MSA natural population, we compared fruit and seed set among three consecutive months. Finally, we compared fruit and seed set in experimental plant populations exposed to diurnal pollination, nocturnal pollination or open pollination. Mann–Whitney U-tests were used to determine if the differences in the medians of analysed groups were significant. For multiple comparisons, we used a Kruskal–Wallis test with Mann–Whitney U-tests for a posteriori pairwise comparison with the significance level set to 0.01 (Bonferroni correction). All analyses were carried out in SPSS ver. 22 (SPSS Inc., Chicago, IL, USA).

Results

Natural populations

In MSA population, 14 out of 69 plants showed H. bicruris predation. All 21 individuals sampled in the BATT population were non-predated. We found no differences in number of seeds per fruit in predated and non-predated individuals in MSA (U = 2462.0; Z = −0.705; P = 0.481). Fruits from BATT contained significantly fewer seeds compared with both predated (U = 1669.5; Z = −3.190; P = 0.001) and non-predated (U = 7140.0; Z = −4.646; P < 0.001) plants in the MSA population (Fig. 1). Main diurnal floral visitors were Coleopteran (47.4 % mainly belonging to the genus Oedemera), Hymenopteran (42.1 % mainly belonging to the genus Halictidae) and more rarely Dipteran (10.5 %).

Figure 1.

Figure 1.

Open in a new tab

Mean number of seeds per fruit in S. latifolia plants predated (grey boxplots) or non-predated (white boxplots) by H. bicruris in MSA and BATT populations. Different letters indicate significant differences.

Fruit and seed set of S. latifolia varied over its flowering season (3 months) in the MSA population (Kruskal–Wallis test: fruit set χ2 = 9.224; DF = 2; P = 0.01; Kruskal–Wallis test: seed set χ2 = 50.806; DF = 2; P < 0.001). Number of fruits did not differ between April and May (U = 158.0; Z = −1.131; P = 0.270), but lowered in June (U = 139.0; Z = −2.073; P = 0.038 compared with April; U = 94.5; Z = −2.871; P = 0.004 compared with May).

In April, mean number of seeds per fruit was significantly lower compared with May (U = 2230.0; Z = −6.161; P < 0.001) and June (U = 2431.5; Z = −6.286; P < 0.001). Mean number of seeds per fruit in May and June was not significantly different (U = 5234.5; Z = −0.493; P = 0.622) (Fig. 2). There was no predation of plants by H. bicruris in April and equal levels of plant predation in May (8 out of 197 fruits; 4.06 %) and June (9 out of 152 fruits; 5.92 %).

Figure 2.

Figure 2.

Open in a new tab

Comparison of fruit and seed set of S. latifolia plants in MSA population in three consecutive months. (A) Mean number of fruits per plant (in parenthesis the rate of fruits predated by H. bicruris). (B) Mean number of seeds per fruit. Different letters indicate significant differences. Circles represent outliers.

Pollinator exclusion experiment

Ten out of 18 plants (58.8 %) exposed to nocturnal pollinators and 8 out of 37 open-pollinated plants (21.6 %) were predated by H. bicruris. The diurnal-only plant treatment experienced no Hadena infection.

Similar fruit set values were found in plants in the diurnal, nocturnal and open-pollinated treatments (Kruskal–Wallis test: χ2 = 0.06; DF = 2; P = 0.997; Fig. 3A). Number of seeds per fruit varied among treatments (Kruskal–Wallis test: χ2 = 54.597; DF = 2; P < 0.001; Fig. 3B): diurnal plant set produced the lowest amount of seeds per fruits when compared to nocturnal plant set (U = 714.5; Z = −4.546; P < 0.001) and open-pollinated plant set (U = 1970.0; Z = −7.323; P < 0.001); nocturnal plant set and open-pollinated plant set showed similar amount of seeds per fruit (U = 2627.5; Z = −0.395; P = 0.693).

Figure 3.

Figure 3.

Open in a new tab

Comparison of fruit and seed set in experimental populations of S. latifolia with three pollination treatments: diurnal, nocturnal and open pollination. (A) Mean number of fruits per plant, (B) mean number of seeds per fruit and (C) total number of seeds per plant. Different letters indicate significant differences. Circles represent outliers.

The total number of seeds per plant marginally differed between the three treatments (Kruskal–Wallis test: χ2 = 10.51; DF = 2; P = 0.05; Fig. 3C): nocturnal and diurnal plant sets showed similar number of seeds per plant (U = 112.5; Z = −1.337; P = 0.184); number of seeds per plant in open-pollinated plant set did not differ from nocturnal plant set (U = 223.5; Z = −1.695; P = 0.09), but differed from diurnal plant set (U = 159.0; Z = −3.121; P = 0.002).

Discussion

The Silene–Hadena interaction may range from mutualism to parasitism primarily depending on the plant fitness trade-off, although this also depends on the local abundance and efficiency of co-pollinators (Dufay and Anstett 2003). These factors may potentially offer the opportunity for S. latifolia to avoid Hadena pollination (and related seed predation) and increase the importance of a positive balance between seed predation and pollinator service for the evolutionary stability of such nursery interactions (Dufay et al. 2010).

In this study, we investigated the contribution of nocturnal and diurnal pollinators to S. latifolia pollination in the Mediterranean. We found that S. latifolia has similar levels of female reproductive success, even when its primary nocturnal pollinator was excluded from plants. However, plants exposed to nocturnal pollinators (i.e. including H. bicruris) produced more seeds per capsule, thus suggesting a higher efficiency of night pollinators. Overall, our results suggest that S. latifolia in the Mediterranean is less dependent on H. bicruris than has been seen in northern Europe. However, H. bicruris is still the most efficient pollinator, thus partially compensating for their predation costs even in the presence of ‘non-predator’ co-pollinators.

Mediterranean populations of S. latifolia may vary in the frequency and occurrence of H. bicruris as length of flowering season and availability of pollinators differ from northern European populations where most previous studies have been performed. By comparing two natural populations (MSA and BATT) that differed in the presence of H. bicruris, we found that the predated population of MSA produced more seeds per fruits than non-predated BATT population, indicating a higher pollination efficiency in the former population. Further, in MSA population, predated plants have a comparable number of seeds to non-predated plants suggesting that the pollination advantage was not exclusive of predated individuals. Since we compared only two natural populations (MSA and BATT), we cannot rule out other potential explanations for our findings including the presence of more pollinators or more co-pollinators or local differences in resource limitation.

In the Mediterranean, S. latifolia typically flowers almost all year, with a blooming peak from April to July, only partly overlapping with the flight period of adult H. bicruris. To test whether pollination success (in terms of seed and fruit number) was related to H. bicruris presence in the predated population of MSA, we estimated fruit and seed set and the occurrence of H. bicruris, in three consecutive months corresponding to the main blooming peak of S. latifolia. We detected the presence of H. bicruris both in May and June (as expected according with its emergence time in the Mediterranean) but not in April. Nevertheless, fruit set did not differ between April and May and decreased in June, indicating that in April pollinators other than H. bicruris actively contributed to Silene pollination. However, the number of seeds per fruit (a proxy of pollinator efficiency) was significantly higher in May and June than in April, matching the occurrence of H. bicruris in the MSA population. Taken together, these results suggest that predated and non-predated natural populations have comparable fruit set. Based on our results, we infer that this is due to contribution of other pollinators. However, S. latifolia has higher seed set when H. bicruris is present. This is in agreement with previous studies that found that moth visitors transfer pollen to stigmas more effectively than diurnal visitors (Young 2002; Reynolds et al. 2009).

The nocturnal/diurnal exclusion experiment demonstrated that both diurnal and nocturnal pollinators may potentially perform similar pollinator service in terms of seed set. However, the two pollination regimes differ in terms of fruit set and seed contents. Diurnally pollinated S. latifolia plants produce a comparable number of fruits to nocturnal and open-pollinated plants, suggesting that number of visitors/visits did not vary between treatments. However, night-pollinated S. latifolia plants (partly predated by H. bicruris) had a higher number of seeds per fruit than diurnal plants, thus suggesting a higher pollination efficiency of night pollinators (as H. bicruris). There were no significant differences between night-pollinated plants and open-pollinated plants; the latter plants benefitted from the pollination by both diurnal and nocturnal pollinators. This finding suggests a strong contribution of night pollination to the female fitness of the open-pollinated plants. Interestingly, similar findings were found a related Silene ciliate–Hadena consparcatoides nursery pollination system (Giménez-Benavides et al. 2007), suggesting a general trade-off trend for this type of pollination mechanism. Results from experimental populations with manipulated pollination regimes correspond well with those from the MSA population where the highest number of seeds per fruit was found when H. bicruris moths were present (i.e. on May and June).

Diurnal pollination has been widely reported in Silene (Giménez-Benavides et al. 2007; Reynolds et al. 2009) and in S. latifolia in particular (Young 2002). In a previous study carried out on the same population of MSA, seed set differed significantly between open-pollinated and hand-pollinated flowers, indicating that open-pollinated plants are pollen-limited (Cozzolino et al. 2015). Thus, there should be a selective pressure to increase seed set by exploring alternative (even less efficient) pollinators, such as diurnal ones. This may become particularly relevant when Silene plants are already blooming but Hadena is not available yet, as typically occurs in the Mediterranean climate. Indeed, our results show that before the appearance of Hadena (MSA population in April), or in the absence of Hadena (BATT population), Silene plants still achieve good pollination success. Although we cannot rule out the presence of nocturnal pollinators other than Hadena, these high levels of pollination success are likely the result of the contribution of diurnal pollinators.

The ecological context in which species interact may impose different selection pressures than those that initially led to the evolution of particular floral traits (Giménez-Benavides et al. 2007). Comparable female fitness of S. latifolia due to the availability of diurnal pollinators, even in the absence of its specialized nursery pollinator, suggests that net selection may sometimes promote a shift to diurnal pollinators and the exclusion of the nocturnal pollinating seed predator. Indeed, in the Mediterranean, the flowering of S. latifolia is not synchronous with H. bicruris emergence and abundance, but when available, H. bicruris does contribute to S. latifolia female fitness. We infer that the higher pollination efficiency of specialized pollinators may outweigh the potential contribution of short-term selective forces to avoid the nursery pollination, thereby allowing maintenance of S. latifolia–H. bicruris interaction in the Mediterranean. Although our study investigated cost and benefits of the pollinator relationships only for the female function, Hadena can also provide a benefit for male function, which is even more dependent on pollinator efficiency (Waelti et al. 2009; Litto et al. 2015). Potential conflicting selection between male and female flower functions may also help to explain why H. bicruris pollination is maintained also in the presence of other pollinators (Prieto-Benítez et al. 2017).

Taken together, our data suggest that S. latifolia is not obligately dependent on its nursery pollinator in the Mediterranean. In the absence of H. bicruris, S. latifolia has comparable female fitness to that observed when H. bicruris is present. This is particularly relevant as the flowering time of the plants significantly extends beyond the emergence H. bicruris, and generalist diurnal pollinators may provide S. latifolia with reproductive assurance during periods when the nursery pollinator is rare or absent. Nevertheless, Mediterranean S. latifolia plants use other (diurnal) pollinators but without excluding its specialized nursery pollinator despite cost of predation. This is a different outcome than seen in other Silene species. For example, pollination by S. alba in northern Europe is exclusively by specialized nocturnal pollinators. Silene noctuiflora is night-pollinated in its European range, yet also uses diurnal pollinators in its introduced range in North America (Witt et al. 1999). Several studies have shown the conditions that promote selection for nocturnal moth pollination and/or the switch to diurnal pollination in Caryophyllaceae (Jennersten 1988; Jennersten and Morse 1991; Shykoff and Bucheli 1995; Young 2002; Barthelmess et al. 2006).

Conclusions

By showing that nursery pollination may incur female fitness costs that can be overcome through higher pollination rates relative to predation rates, our results provide an extra dimension to our understanding of dynamics of specialized plant–pollinator interactions and the cost/benefit balance of nursery pollination. Specialized pollinators are not always available, and some populations may co-opt generalist pollinators when they are abundant. These results emphasize the need to conduct such investigations on populations representing the distributional and diversity centres of the species under study (e.g. the Mediterranean for Silene; Giménez-Benavides et al. 2007), where pollinator abundance and diversity is likely to be high.

Sources of Funding

This research was carried out in the frame of Programme STAR, financially supported by UNINA and Compagnia di San Paolo.

Contributions by the Authors

G.S. conceived and designed the experiments, performed the experiments and wrote the paper; L.C. analysed the data and prepared figures and tables; K.J.D. contributed to data analysis and reviewed drafts of the paper; S.C. conceived and designed the experiments and reviewed drafts of the paper.

Conflict of Interest

None declared.

Acknowledgements

Authors thank M. Litto for help with field work. They also thank the Associate Editor and two anonymous reviewers for providing helpful comments on a previous version of the manuscript.

Literature Cited

  1. Aigner PA. 2001. Optimality modeling and fitness trade-offs: when should plants become pollinator specialists?Oikos 95:177–184. [Google Scholar]
  2. Aigner PA. 2004. Floral specialization without trade-offs: optimal corolla flare in contrasting pollination environments. Ecology 85:2560–2569. [Google Scholar]
  3. Althoff DM, Segraves KA, Smith CI, Leebens-Mack J, Pellmyr O. 2012. Geographic isolation trumps coevolution as a driver of yucca and yucca moth diversification. Molecular Phylogenetics and Evolution 62:898–906. [DOI] [PubMed] [Google Scholar]
  4. Barthelmess EL, Richards CM, McCauley DE. 2006. Relative effects of nocturnal vs diurnal pollinators and distance on gene flow in small Silene alba populations. The New Phytologist 169:689–698. [DOI] [PubMed] [Google Scholar]
  5. Bopp S, Gottsberger G. 2004. Importance of Silene latifolia ssp. alba and S. dioica (Caryophyllaceae) as host plants of the parasitic pollinator Hadena bicruris (Lepidoptera, Noctuidae). Oikos 105:221–228. [Google Scholar]
  6. Brantjes NB. 1976. Prevention of superparasitation of Melandrium flowers (Caryophyllaceae) by Hadena (Lepidoptera). Oecologia 24:1–6. [DOI] [PubMed] [Google Scholar]
  7. Burkhardt A, Ridenhour BJ, Delph LF, Bernasconi G. 2012. The contribution of a pollinating seed predator to selection on Silene latifolia females. Journal of Evolutionary Biology 25:461–472. [DOI] [PubMed] [Google Scholar]
  8. Bustamante E, Casas A, Búrquez A. 2010. Geographic variation in reproductive success of Stenocereus thurberi (Cactaceae): effects of pollination timing and pollinator guild. American Journal of Botany 97:2020–2030. [DOI] [PubMed] [Google Scholar]
  9. Castillo DM, Kula AAR, Dotterl S, Dudash MR, Fenster CB. 2014. Invasive Silene latifolia may benefit from a native pollinating seed predator, Hadena ectypa, in North America. International Journal of Plant Sciences 175:80–91. [Google Scholar]
  10. Cozzolino S, Fineschi S, Litto M, Scopece G, Trunschke J, Schiestl FP. 2015. Herbivory increases fruit set in Silene latifolia: a consequence of induced pollinator-attracting floral volatiles?Journal of Chemical Ecology 41:622–630. [DOI] [PubMed] [Google Scholar]
  11. Crepet WL. 1983. The role of pollination in the evolution of the angiosperms. In: Real L, ed. Pollination biology. Orlando, FL: Academic Press, 29–50. [Google Scholar]
  12. Cruaud A, Rønsted N, Chantarasuwan B, Chou LS, Clement WL, Couloux A, Cousins B, Genson G, Harrison RD, Hanson PE, Hossaert-McKey M, Jabbour-Zahab R, Jousselin E, Kerdelhué C, Kjellberg F, Lopez-Vaamonde C, Peebles J, Peng YQ, Pereira RA, Schramm T, Ubaidillah R, van Noort S, Weiblen GD, Yang DR, Yodpinyanee A, Libeskind-Hadas R, Cook JM, Rasplus JY, Savolainen V. 2012. An extreme case of plant-insect codiversification: figs and fig-pollinating wasps. Systematic Biology 61:1029–1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Delph LF, Knapczyk FN, Taylor DR. 2002. Among‐population variation and correlations in sexually dimorphic traits of Silene latifolia. Journal of Evolutionary Biology 15:1011–1020. [Google Scholar]
  14. Dilley JD, Wilson P, Mesler MR. 2000. The radiation of Calochortus: generalist flowers moving through a mosaic of potential pollinators. Oikos 89:209–222. [Google Scholar]
  15. Dötterl S, Jürgens A, Seifert K, Laube T, Weissbecker B, Schütz S. 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. The New Phytologist 169:707–718. [DOI] [PubMed] [Google Scholar]
  16. Dufay M, Anstett MC. 2003. Conflicts between plants and pollinators that reproduce within inflorescences: evolutionary variations on a theme. Oikos 100:3–14. [Google Scholar]
  17. Dufay M, Lahiani E, Brachi B. 2010. Gender variation and inbreeding depression in gynodioecious-gynomonoecious Silene nutans (Caryophyllaceae). International Journal of Plant Sciences 171:53–62. [Google Scholar]
  18. Elzinga JA, Turin H, van Damme JM, Biere A. 2005. Plant population size and isolation affect herbivory of Silene latifolia by the specialist herbivore Hadena bicruris and parasitism of the herbivore by parasitoids. Oecologia 144:416–426. [DOI] [PubMed] [Google Scholar]
  19. Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD. 2004. Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution and Systematics 35:375–403. [Google Scholar]
  20. Fenster CB, Dudash MR. 2001. Spatiotemporal variation in the role of hummingbirds as pollinators of Silene virginica. Ecology 82:844–851. [Google Scholar]
  21. Giménez‐Benavides L, Dötterl S, Jürgens A, Escudero A, Iriondo JM. 2007. Generalist diurnal pollination provides greater fitness in a plant with nocturnal pollination syndrome: assessing the effects of a Silene–Hadena interaction. Oikos 116:1461–1472. [Google Scholar]
  22. Groman JD, Pellmyr O. 1999. The pollination biology of Manfreda virginica (Agavaceae): relative contribution of diurnal and nocturnal visitors. Oikos 87:373–381. [Google Scholar]
  23. Herrera CM. 1988. Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Biological Journal of the Linnean Society 35:95–125. [Google Scholar]
  24. Herrera CM. 2000. Flower‐to‐seedling consequences of different pollination regimes in an insect‐pollinated shrub. Ecology 81:15–29. [Google Scholar]
  25. Jennersten O. 1988. Pollination of Viscaria vulgaris (Caryophyllaceae): the contributions of diurnal and nocturnal insects to seed set and seed predation. Oikos 52:319–327. [Google Scholar]
  26. Jennersten O, Morse D. 1991. The quality of pollination by diurnal and nocturnal insects visiting common milkweed, Asclepias syriaca. The American Midland Naturalist 125:18–28. [Google Scholar]
  27. Jürgens A, Witt T, Gottsberger G. 1996. Reproduction and pollination in central European populations of Silene and Saponaria species. Plant Biology 109:316–324. [Google Scholar]
  28. Kawakita A. 2010. Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biology 25:3–19. [Google Scholar]
  29. Kawakita A, Takimura A, Terachi T, Sota T, Kato M. 2004. Cospeciation analysis of an obligate pollination mutualism: have Glochidion trees (Euphorbiaceae) and pollinating Epicephala moths (Gracillariidae) diversified in parallel?Evolution 58:2201–2214. [DOI] [PubMed] [Google Scholar]
  30. Labouche AM, Bernasconi G. 2010. Male moths provide pollination benefits in the Silene latifolia–Hadena bicruris nursery pollination system. Functional Ecology 24:534–544. [Google Scholar]
  31. Litto M, Scopece G, Fineschi S, Schiestl FP, Cozzolino S. 2015. Herbivory affects male and female reproductive success differently in dioecious Silene latifolia. Entomologia Experimentalis et Applicata 157:60–67. [Google Scholar]
  32. Magalhaes IS, Bernasconi G. 2014. Phenotypic divergence and inter-specific trait correlation in a plant-pollinator/seed predator mutualism. Evolutionary Ecology 28:905–922. [Google Scholar]
  33. Morse DH, Fritz RS. 1983. Contributions of diurnal and nocturnal insects to the pollination of common milkweed (Asclepias syriaca L.) in a pollen-limited system. Oecologia 60:190–197. [DOI] [PubMed] [Google Scholar]
  34. Muchhala N. 2003. Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of Burmeistera cyclostigmata and B. Tenuiflora (Campanulaceae). Oecologia 134:373–380. [DOI] [PubMed] [Google Scholar]
  35. Muchhala N, Caiza A, Vizuete JC, Thomson JD. 2009. A generalized pollination system in the tropics: bats, birds and Aphelandra acanthus. Annals of Botany 103:1481–1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Pellmyr O. 2003. Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri Botanical Garden 90:35–55. [Google Scholar]
  37. Prieto-Benítez S, Yela JL, Giménez-Benavides L. 2017. Ten years of progress in the study of Hadena-Caryophyllaceae nursery pollination. A review in light of new Mediterranean data. Flora 232:63–72. [Google Scholar]
  38. Reynolds RJ, Kula AA, Fenster CB, Dudash MR. 2012. Variable nursery pollinator importance and its effect on plant reproductive success. Oecologia 168:439–448. [DOI] [PubMed] [Google Scholar]
  39. Reynolds RJ, Westbrook MJ, Rohde AS, Cridland JM, Fenster CB, Dudash MR. 2009. Pollinator specialization and pollination syndromes of three related North American Silene. Ecology 90:2077–2087. [DOI] [PubMed] [Google Scholar]
  40. Schemske DW, Horvitz CC. 1984. Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225:519–521. [DOI] [PubMed] [Google Scholar]
  41. Shykoff J, Bucheli E. 1995. Pollinator visitation patterns, floral rewards and the probability of transmission of Microbotryum violaceum, a veneral disease of plants. Journal of Ecology 83:189–198. [Google Scholar]
  42. Stebbins GL. 1970. Adaptive radiation of reproductive characteristics in angiosperms, I: pollination mechanisms. Annual Review of Ecology and Systematics 1:307–326. [Google Scholar]
  43. Stephenson AG. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12:253–279. [Google Scholar]
  44. Thompson JN, Pellmyr O. 1992. Mutualism with pollinating seed parasites amid co‐pollinators: constraints on specialization. Ecology 73:1780–1791. [Google Scholar]
  45. Waelti MO, Page PA, Widmer A, Schiestl FP. 2009. How to be an attractive male: floral dimorphism and attractiveness to pollinators in a dioecious plant. BMC Evolutionary Biology 9:190. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Waser NM, Chittka L, Price MV, Williams NM, Ollerton J. 1996. Generalization in pollination systems, and why it matters. Ecology 77:1043–1060. [Google Scholar]
  47. Witt T, Jürgens A, Geyer R, Gottsberger G. 1999. Nectar dynamics and sugar composition in flowers of Silene and Saponaria species (Caryophyllaceae). Plant Biology 1:334–345. [Google Scholar]
  48. Wolff D, Braun M, Liede S. 2003. Nocturnal versus diurnal pollination success in Isertia laevis (Rubiaceae): a sphingophilous plant visited by hummingbirds. Plant Biology 5:71–78. [Google Scholar]
  49. Young HJ. 2002. Diurnal and nocturnal pollination of Silene alba (Caryophyllaceae). American Journal of Botany 89:433–440. [DOI] [PubMed] [Google Scholar]

Articles from AoB Plants are provided here courtesy of Oxford University Press

RESOURCES