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1.  Endozoochory by beetles: a novel seed dispersal mechanism 
Annals of Botany  2011;107(4):629-637.
Background and Aims
Due in part to biophysical sized-related constraints, insects unlike vertebrates are seldom expected to act as primary seed dispersers via ingestion of fruits and seeds (endozoochory). The Mediterranean parasitic plant Cytinus hypocistis, however, possesses some characteristics that may facilitate endozoochory by beetles. By combining a long-term field study with experimental manipulation, we tested whether C. hypocistis seeds are endozoochorously dispersed by beetles.
Methods
Field studies were carried out over 4 years on six populations in southern Spain. We recorded the rate of natural fruit consumption by beetles, the extent of beetle movement, beetle behaviour and the relative importance of C. hypocistis fruits in beetle diet.
Key Results
The tenebrionid beetle Pimelia costata was an important disperser of C. hypocistis seeds, consuming up to 17·5 % of fruits per population. Forty-six per cent of beetles captured in the field consumed C. hypocistis fruits, with up to 31 seeds found in individual beetle frass. An assessment of seeds following passage through the gut of beetles indicated that seeds remained intact and viable and that the proportion of viable seeds from beetle frass was not significantly different from that of seeds collected directly from fruits.
Conclusions
A novel plant–animal interaction is revealed; endozoochory by beetles may facilitate the dispersal of viable seeds after passage through the gut away from the parent plant to potentially favourable underground sites offering a high probability of germination and establishment success. Such an ecological role has until now been attributed only to vertebrates. Future studies should consider more widely the putative role of fruit and seed ingestion by invertebrates as a dispersal mechanism, particularly for those plant species that possess small seeds.
doi:10.1093/aob/mcr013
PMCID: PMC3064545  PMID: 21303784
Beetle; Cytinus hypocistis; Cytinaceae; endozoochory; mutualism, parasitic plant; Pimelia costata; plant–animal interaction; seed dispersal; seed viability; Tenebrionidae
2.  Marcescent corollas as functional structures: effects on the fecundity of two insect-pollinated plants 
Annals of Botany  2010;106(4):659-662.
Background and aims
Persistence of withered corollas after anthesis (‘corolla marcescence’) is widespread in angiosperms, yet its functional significance does not seem to have been explored for any species. This note reports the results of experiments assessing the fecundity effects of marcescent corollas in two southern Spanish insect-pollinated plants, Lavandula latifolia (Lamiaceae) and Viola cazorlensis (Violaceae).
Methods
The effect of marcescent corollas on seed production was evaluated experimentally on wild-growing plants. Newly open flowers were randomly assigned to either control or treatment groups in experimental plants. After anthesis, withered corollas of treatment flowers were removed and those in control flowers were left in place. Fruits produced by treatment and control flowers were collected shortly before dehiscence and the number of seeds counted.
Key Results
In V. cazorlensis, removal of withered corollas had no effect on percentage of fruit set, but mean seeds per fruit increased from 9·5 to 11·4. In L. latifolia, corolla removal had no effect on the number of seeds per fruit, but reduced the proportion of flowers ripening fruit from 60 % to 40 %. The detrimental effect of corolla removal on L. latifolia fecundity resulted from the drastic increase in fruit infestation by seed-predatory cecidomyiid larvae, which occurred in 4 % and 34 % of control and treatment fruits, respectively.
Conclusions
Because of their potential effects on plant fecundity, marcescent corollas should not be dismissed a priori as biologically irrelevant leftovers from past floral functions. The simplicity of the experimental layout required to test for short-term fecundity effects of corolla marcescence should help to achieve a better understanding of the ecological and evolutionary correlates of this widespread but poorly understood trait.
doi:10.1093/aob/mcq160
PMCID: PMC2944983  PMID: 20870656
Corolla marcescence; fecundity; Lavandula latifolia (Lamiaceae); seed predation; Viola cazorlensis (Violaceae)
3.  Yeasts in floral nectar: a quantitative survey 
Annals of Botany  2009;103(9):1415-1423.
Background and Aims
One peculiarity of floral nectar that remains relatively unexplored from an ecological perspective is its role as a natural habitat for micro-organisms. This study assesses the frequency of occurrence and abundance of yeast cells in floral nectar of insect-pollinated plants from three contrasting plant communities on two continents. Possible correlations between interspecific differences in yeast incidence and pollinator composition are also explored.
Methods
The study was conducted at three widely separated areas, two in the Iberian Peninsula (Spain) and one in the Yucatán Peninsula (Mexico). Floral nectar samples from 130 species (37–63 species per region) in 44 families were examined microscopically for the presence of yeast cells. For one of the Spanish sites, the relationship across species between incidence of yeasts in nectar and the proportion of flowers visited by each of five major pollinator categories was also investigated.
Key Results
Yeasts occurred regularly in the floral nectar of many species, where they sometimes reached extraordinary densities (up to 4 × 105 cells mm−3). Depending on the region, between 32 and 44 % of all nectar samples contained yeasts. Yeast cell densities in the order of 104 cells mm−3 were commonplace, and densities >105 cells mm−3 were not rare. About one-fifth of species at each site had mean yeast cell densities >104 cells mm−3. Across species, yeast frequency and abundance were directly correlated with the proportion of floral visits by bumble-bees, and inversely with the proportion of visits by solitary bees.
Conclusions
Incorporating nectar yeasts into the scenario of plant–pollinator interactions opens up a number of intriguing avenues for research. In addition, with yeasts being as ubiquitous and abundant in floral nectars as revealed by this study, and given their astounding metabolic versatility, studies focusing on nectar chemical features should carefully control for the presence of yeasts in nectar samples.
doi:10.1093/aob/mcp026
PMCID: PMC2701759  PMID: 19208669
Bumble-bees; floral nectar; microbial communities; pollination; yeasts
4.  The ant-pollination system of Cytinus hypocistis (Cytinaceae), a Mediterranean root holoparasite 
Annals of Botany  2009;103(7):1065-1075.
Background and Aims
The genus Cytinus is composed of rootless, stemless and leafless parasites whose flowers are only visible during the reproductive period when they arise from the host tissues. Most of the taxa occur in Madagascar and South Africa, where mammal pollination has been suggested for one species. There is only one species in the Mediterranean region, and its pollination system has been unknown. Here, a long-term field observation study is combined with experimental pollination treatments in order to assess the pollination biology and reproductive system in the Mediterranean species Cytinus hypocistis.
Methods
Field studies were carried out in six populations in southern Spain over 4 years. Temporal and spatial patterns of variation in the composition and behaviour of floral visitors were characterized. Pollen loads and pollen viability were observed, and exclusion and controlled-pollination treatments were also conducted.
Key Results
Cytinus hypocistis is a self-compatible monoecious species that relies on insects for seed production. Ants were the main visitors, accounting for 97·4 % of total floral visits, and exclusion experiments showed that they act as true pollinators. They consistently touched reproductive organs, carried large pollen loads and transported viable pollen, although the different ant species observed in the flowers differed in their pollination effectiveness. The abundance of flying visitors was surprisingly low, and only the fly Oplisa aterrima contributed to fruit production and cross-pollination.
Conclusions
Mutualistic services by ant are essential for the pollination of Cytinus hypocistis. Although this parasite does not exhibit typical features of the ‘ant-pollination syndrome’, many other characteristics indicate that it is evolving to a more specialized ant-pollination system. The striking interspecific differences in the pollination systems of Mediterranean Cytinus (ant-pollinated) and some South African Cytinus (mammal-pollinated) make this genus an excellent model to investigate the divergent evolution of pollination systems in broadly disjunct areas.
doi:10.1093/aob/mcp049
PMCID: PMC2707910  PMID: 19258337
Ant; breeding system; Cytinus hypocistis; Cytinaceae; insects; flies; Mediterranean Basin; parasitic plant; pollination; Rafflesiaceae
5.  Geographical Structuring of Genetic Diversity Across the Whole Distribution Range of Narcissus longispathus, a Habitat-specialist, Mediterranean Narrow Endemic 
Annals of Botany  2008;102(2):183-194.
Background and Aims
High mountain ranges of the Mediterranean Basin harbour a large number of narrowly endemic plants. In this study an investigation is made of the levels and partitioning of genetic diversity in Narcissus longispathus, a narrow endemic of south-eastern Spanish mountains characterized by a naturally fragmented distribution due to extreme specialization on a rare habitat type. By using dense sampling of populations across the species' whole geographical range, genetic structuring at different geographical scales is also examined.
Methods
Using horizontal starch-gel electrophoresis, allozyme variability was screened at 19 loci for a total of 858 individuals from 27 populations. The data were analysed by means of standard statistical approaches in order to estimate gene diversity and the genetic structure of the populations.
Key Results
Narcissus longispathus displayed high levels of genetic diversity and extensive diversification among populations. At the species level, the percentage of polymorphic loci was 68 %, with average values of 2·1, 0·11 and 0·14 for the number of alleles per locus, observed heterozygosity and expected heterozygosity, respectively. Southern and more isolated populations tended to have less genetic variability than northern and less-isolated populations. A strong spatial patterning of genetic diversity was found at the various spatial scales. Gene flow/drift equilibrium occurred over distances <4 km. Beyond that distance divergence was relatively more influenced by drift. The populations studied seem to derive from three panmictic units or ‘gene pools’, with levels of admixture being greatest in the central and south-eastern portions of the species' range.
Conclusions
In addition to documenting a case of high genetic diversity in a narrow endemic plant with naturally fragmented populations, the results emphasize the need for dense population sampling and examination of different geographical scales for understanding population genetic structure in habitat specialists restricted to ecological islands.
doi:10.1093/aob/mcn086
PMCID: PMC2712358  PMID: 18556752
Allozymes; genetic diversity; geographical scale; habitat isolation; Narcissus longispathus; Mediterranean endemism; mountain range; natural fragmented distribution
6.  Ecological Context of Breeding System Variation: Sex, Size and Pollination in a (Predominantly) Gynodioecious Shrub 
Annals of Botany  2007;100(7):1547-1556.
Background and Aims
Species that exhibit among-population variation in breeding system are particularly suitable to study the importance of the ecological context for the stability and evolution of gender polymorphism. Geographical variation in breeding system and sex ratio of Daphne laureola (Thymelaeaceae) was examined and their association with environmental conditions, plant and floral display sizes, and pollination environment in a broad geographic scale was analysed.
Method
The proportion of female and hermaphrodite individuals in 38 populations within the Iberian Peninsula was scored. Average local temperature and precipitation from these sites were obtained from interpolation models based on 30 years of data. Pollination success was estimated as stigmatic pollen loads, pollen tubes per ovule and the proportion of unfertilized flowers per individual in a sub-set of hermaphroditic and gynodioecious populations.
Key Results
Daphne laureola is predominantly gynodioecious, but hermaphroditic populations were found in northeastern and southwestern regions, characterized by higher temperatures and lower annual precipitation. In the gynodioecious populations, female plants were larger and bore more flowers than hermaphrodites. However, due to their lower pollination success, females did not consistently produce more seeds than hermaphrodites, which tends to negate a seed production advantage in D. laureola females. In the northeastern hermaphroditic populations, plants were smaller and produced 9–13 times fewer flowers than in the other Iberian regions, and thus presumably had a lower level of geitonogamous self-fertilization. However, in a few southern populations hermaphroditism was not associated with small plant size and low flower production.
Conclusions
The findings highlight that different mechanisms, including abiotic conditions and pollinator service, may account for breeding system variation within a species' distribution range and also suggest that geitonogamy may affect plant breeding system evolution.
doi:10.1093/aob/mcm254
PMCID: PMC2759233  PMID: 17933844
Daphne laureola; environmental gradients; floral display; geographic variation; geitonogamy; gynodioecy; pollination success; sex ratio; Thymelaeaceae
7.  Intra-plant Variation in Nectar Sugar Composition in Two Aquilegia Species (Ranunculaceae): Contrasting Patterns under Field and Glasshouse Conditions 
Annals of Botany  2007;99(4):653-660.
Background and Aims
Intra-specific variation in nectar chemistry under natural conditions has been only rarely explored, yet it is an essential aspect of our understanding of how pollinator-mediated selection might act on nectar traits. This paper examines intra-specific variation in nectar sugar composition in field and glasshouse plants of the bumblebee-pollinated perennial herbs Aquilegia vulgaris subsp. vulgaris and Aquilegia pyrenaica subsp. cazorlensis (Ranunculaceae). The aims of the study are to assess the generality of extreme intra-plant variation in nectar sugar composition recently reported for other species in the field, and gaining insight on the possible mechanisms involved.
Methods
The proportions of glucose, fructose and sucrose in single-nectary nectar samples collected from field and glasshouse plants were determined using high performance liquid chromatography. A hierarchical variance partition was used to dissect total variance into components due to variation among plants, flowers within plants, and nectaries within flowers.
Key Results
Nectar of the two species was mostly sucrose-dominated, but composition varied widely in the field, ranging from sucrose-only to fructose-dominated. Most intra-specific variance was due to differences among nectaries of the same flower, and flowers of the same plant. The high intra-plant variation in sugar composition exhibited by field plants vanished in the glasshouse, where nectar composition emerged as a remarkably constant feature across plants, flowers and nectaries.
Conclusions
In addition to corroborating the results of previous studies documenting extreme intra-plant variation in nectar sugar composition in the field, this study suggests that such variation may ultimately be caused by biotic factors operating on the nectar in the field but not in the glasshouse. Pollinator visitation and pollinator-borne yeasts are suggested as likely causal agents.
doi:10.1093/aob/mcl291
PMCID: PMC2802931  PMID: 17259227
Abiotic environment; Aquilegia pyrenaica subsp. cazorlensis; Aquilegia vulgaris subsp. vulgaris; biotic factors; field conditions; glasshouse; Iberian Peninsula; inter- and intra-specific variation; nectar-sugar composition; nectary; variance components

Results 1-7 (7)