lower pollinator efficiency overcome by overwhelmingly higher visitation frequency. Oecologia 156: Parker, I. M Pollinator limitation
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1 Pollination Diego P. Vázquez 1, 2 and Carolina L. Morales 3 1. Instituto Argentino de Investigaciones de las Zonas Áridas, CONICET 2. Instituto de Ciencias Básicas, Universidad Nacional de Cuyo 3. Laboratorio Ecotono, INIBIOMA, CONICET Universidad Nacional del Comahue Pollination is the transfer of pollen grains, which contain male gametes, to the receptive part of the ovule bearing organ of seed plants (the mycropyle in gymnosperms and the stigma in angiosperms). Pollination, a crucial step in sexual reproduction of seed plants, can occur through abiotic vectors (wind, water) and biotic vectors (insects, birds, other vertebrates). Introduced species may influence pollination either directly, when the alien is a plant or a pollinator, or indirectly, when the alien is another kind of species that influences the pollination process by affecting the plant, the pollinator or both. In addition, pollination can modulate the establishment and spread of introduced plant species. I. Plant invaders A. Impact of alien plants on the pollination of native plants Alien plants can influence the pollination of native plants through competition for pollinators and interspecific pollen transfer. Competition for pollinators occurs when an alien plant draws pollinators away from the native plant, particularly when pollinators are scarce. The native plant may then suffer from decreased male (pollen dispersal) and female (seed production) reproductive success. Traits that may make alien plants likely to compete with native plants for pollinator visits include rich floral rewards, showy floral colors, high population size and density, high degree of generalization in the interactions with pollinators, and high phenotypic similarity in floral traits with native plants. There are several documented cases of reduced reproduction of native species owing to pollinator mediated competition with plant invaders. A well known example is the Himalayan balsam (Impatiens glandulifera, Balsaminaceae), which has invaded many river banks in Europe and North America. Floral nectaries of this species produce sugar at a rate higher than any other European plant, which attracts pollinators away from co flowering species, reducing their seed set. Although evidence suggests that most animal pollinated alien plants have negative effects on the pollination of native co flowering species, effects are highly contingent on species identities and the ecological context. For instance, the dandelion (Taraxacum officinale), a weed of European origin, reduces the pollination and reproductive success of native Taraxacum species in Japan. However, in central Chile it affects native high Andean species Hypochaeris trinchioides and Perezzia carthamoides only when growing at high densities. Likewise, in mountain meadows in Colorado, USA, removal of T. officinale has not influenced the visitation and reproductive success of native Delphinium nuttallianum. In addition to competition for pollinators, alien animal pollinated plants can influence the pollination of native plants through interspecific pollen transfer the transport of pollen from anthers of one species to the stigma of another species. Interspecific pollen transfer occurs when pollinators switch between flowers of different species while foraging. Thus, even if alien plants do not compete for pollinators, they can still affect native species either by depositing alien pollen on stigmas of native species or by wasting native pollen on alien flowers. For instance, the alien thistle Carduus nutans frequently invades highly disturbed forests in the southern Argentine Andes, where it co occurs with the endemic herb Alstroemeria aurea. Bumblebees visit flowers of both species (Fig. 1), depositing alien pollen on stigmas of A. aurea and reducing the deposition and germination 1
2 of conspecific pollen. [Place Figure 1 near here] Although the amounts of heterospecific pollen deposited in nature are often too low to affect reproduction, when native and alien species are closely related even small amounts of heterospecific pollen may have devastating reproductive consequences for native species through hybridization. This is what happens in Canadian red mulberry (Morus rubra) forests invaded by the alien white mulberry (Morus alba). In highly invaded areas, the availability of alien or hybrid pollen may be an order of magnitude greater than that of native pollen, negatively affecting both male and female reproductive success of the native mulberry. B. The role of pollination on the establishment and spread of alien plants One can also ask whether pollination can be a barrier to the establishment of an alien plant. The relatively low degree of specialization of most plant pollinator interactions makes this possibility unlikely, because most alien species find suitable pollinators in the invaded community. There are, however, a few cases of extreme specialization, such as figs and yuccas, for which pollination may indeed limit spread. For example, of the sixty species of Ficus introduced to Florida, USA, only three have become invasive, and they have done so only after the accidental introduction of their specific wasp. Even if pollination does not limit establishment, it may limit the rate of spread of alien plants when their reproduction is highly pollen limited. For example, in Washington State, USA, pollinators limit population growth rate of Scotch broom (Cytisus scoparius) in recently invaded habitats, which in turn limits the broom's rate of spread into new habitats. II. Pollinator invaders Alien pollinators can influence pollination particularly when their morphology, behavior and phenology/activity period is different from the native pollinators of the plants they visit. For example, an exotic bumblebee introduced to Australia, Bombus terrestris, is a much less effective pollinator of the native Eucalyptus globules than the main native pollinator, the swift parrot Lathamus discolour, mainly because the bumblebee moves less frequently between plants and therefore transfers less outcross pollen than the native parrot does. However, as for plant invaders, pollinator invaders do not necessarily disrupt pollination of native plants. The exotic bumblebee Bombus ruderatus is less effective than its native congener B. dahlbomii as pollinator of Alstroemeria aurea, a herb endemic to the southern Andes of Argentina and Chile (Fig. 2). Yet, in many areas B. ruderatus is replacing the native bumblebee, which makes it nowadays the most reliable pollinator of A. aurea. In some cases, the alien pollinator may be even more effective than native pollinators. For example, the introduced Africanized honeybee (Apis mellifera scutellata) is more effective than native pollinators in pollinating isolated individuals of Dinizia excelsa, a tree native to the Amazonian forest; the greater effectiveness of the honeybee is due to its greater flight distances, which increase gene flow among isolated D. excelsa individuals. [Place Figure 2 near here] III. Reciprocal facilitation between alien plants and alien pollinators Alien species interact not only with native species via pollination but also among themselves, sometimes facilitating each other's establishment and spread (i.e., an invasional meltdown). The establishment of Ficus and its specialist wasp pollinators in Florida discussed above is one striking example. But extreme reciprocal specialization is not a precondition for reciprocal facilitation between alien plants and pollinators. In California, introduced Apis mellifera strongly increases the reproductive output of the weedy thistle Centaurea solstitialis. Likewise, visitation by 2
3 the European Bombus terrestris enhances reproduction of Lupinus arboreus, a North American species introduced to Tasmania. Although L. arboreus is currently a minor weed in Tasmania, the recent introduction of B. terrestris is facilitating its spread, making it likely to become as problematic as in New Zealand now that it has an effective pollinator. IV. Other types of invaders Other types of alien species besides seed plants and animal pollinators can affect pollination. Introduced predators, parasites and diseases of pollinators are one possibility. A dramatic example is the introduction of avian malaria to the Hawaiian islands, where it contributed to the extinction of a substantial fraction of the native birds, some of which were pollinators of native plants. Some plant species, most notably those in the Campanulaceae, are believed to have gone extinct owing to pollination failure. Plant consumers can interfere with pollination by directly consuming flowers or, indirectly, by causing changes in flower attractiveness. For example, the eradication of introduced possums Trichosurus vulpecula and wallabies Petrogale penicillata from some islands in New Zealand has resulted in significant increases in the flowering of two plant species, pohutukawa (Metrosideros excelsa) and rewarewa (Knightia excelsa). More subtly, decreased plant population density caused by introduced herbivores can also affect pollinator visitation frequency and the extent of interspecific pollen transfer. For example, trampling by introduced cattle in Nahuel Huapi National Park, Argentina drastically decreases the population density of the herb Alstroemeria aurea; this effect on population density in turn results in increased rates of interspecific pollen transfer, because its generalist pollinators (mainly bumblebees) visit other species more frequently than in denser, cattle free A. aurea populations. See also the following articles Bees; Competition, Plant; Dispersal Ability, Plants; Breeding Systems (Plant); Horticulture; Hybridization and Introgression; Invasional Meltdown; Mutualism. Glossary female reproductive success the success of a plant in producing seeds interspecific pollen transfer transport of pollen from the anthers of one species to the stigma of other species male reproductive success the success of a plant in siring seeds with its own pollen pollinator an animal vector that carries pollen from anthers to stigmas, usually of different flowers. pollinator limitation limitation of seed production by insufficient pollinator visitation. Further reading Barthell, J. F. R., J. M. Randall, R. W. Thorp, and A. M. Wenner Promotion of seed set in yellow star thistle by honey bees: evidence of an invasive mutualism. Ecological Applications 11: Bjerknes, A., Ø. Totland, S. Hegland and A. Nielsen Do alien plant invasions really affect pollination success in native plant species? Biological Conservation 138: Brown, B. J., R. J. Mitchell and S. A. Graham Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83: Burgess, K. S.; M. Morgan and B. C. Husband Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytologist. 177: Madjidian, J., C. L. Morales and H. Smith Displacement of a native by an alien bumblebee: 3
4 lower pollinator efficiency overcome by overwhelmingly higher visitation frequency. Oecologia 156: Parker, I. M Pollinator limitation of Cytisius scoparius (Scotch broom), an invasive exotic shrub. Ecology 78: Richardson, D. M., N. Allsopp, C. M. D'Antonio, S. J. Milton and M. Rejmánek Plant invasions the role of mutualisms. Biological Reviews 75:
5 Figure captions Figure 1. Plant pollinator interactions involving native and alien species in southern Argentine Andes. Left: Native bumblebee Bombus dahlbomii visiting the alien thistle Carduus nutans, a frequent invader of highly disturbed forests in the southern Argentine Andes. Photo credit: Néstor Vidal. Right: Introduced bumblebee Bombus ruderatus visiting a flower of the endemic herb Alstroemeria aurea. Photo credit: Carolina L. Morales. Figure 2. Differences between the native bumblebee Bombus dahlbomii and the alien B. ruderatus in their per visit effectiveness as pollinators of the endemic herb Alstroemeria aurea in Nahuel Huapi National Park, Argentina. The alien B. ruderatus is less effective both in terms of total pollen grains and of the proportion of viable (germinated) pollen deposited in flower stigmas. Adapted from Madjidian et al. (2008), Oecologia 156:
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