Functional biology of parasitic plants: a review

Background – Parasitic plants are functionally specialized to acquire at least some essential resources from other plants via specialized organs called haustoria. Parasitism evolved 12 times independently in the evolution of angiosperms of which approximately 1% (4500 species) are parasitic. Not only are parasitic plants diverse in terms of evolutionary origins but also in terms of their physiological functioning and ecological behaviour.Methods – Here, I review the importance of principal functional traits which underlie the physiology and ecology of individual parasitic plants. These include the ability to perform photosynthesis, anatomical details of the vascular connection to the host determining the quality of resources acquired from the host, location of the haustoria on the host, which is closely connected with the parasite life form, and the mode of germination (either triggered by environmental condition or induced by presence of host roots).Results and conclusions – Based on the distribution of all these traits in parasitic plants, I introduce their functional classification into root hemiparasites, root holoparasites, stem parasites and endophytic parasites. In addition to the classification, I also present an evolutionary hypothesis explaining the evolution of advanced parasitic plant forms from root hemiparasites. This hypothesis is based on ecological constraints from which the parasites are released with increasing ability to acquire resources from the host. This evolutionary process also implies increasing host specificity which imposes new constraints on the ability to establish host connection. This explains the evolutionary stability of photosynthetic hemiparasites and their species richness which is one order of magnitude higher than that of holoparasites

Functional biology of parasitic plants: a review

Background – Parasitic plants are functionally specialized to acquire at least some essential resources from other plants via specialized organs called haustoria. Parasitism evolved 12 times independently in the evolution of angiosperms of which approximately 1% (4500 species) are parasitic. Not only are parasitic plants diverse in terms of evolutionary origins but also in terms of their physiological functioning and ecological behaviour.Methods – Here, I review the importance of principal functional traits which underlie the physiology and ecology of individual parasitic plants. These include the ability to perform photosynthesis, anatomical details of the vascular connection to the host determining the quality of resources acquired from the host, location of the haustoria on the host, which is closely connected with the parasite life form, and the mode of germination (either triggered by environmental condition or induced by presence of host roots).Results and conclusions – Based on the distribution of all these traits in parasitic plants, I introduce their functional classification into root hemiparasites, root holoparasites, stem parasites and endophytic parasites. In addition to the classification, I also present an evolutionary hypothesis explaining the evolution of advanced parasitic plant forms from root hemiparasites. This hypothesis is based on ecological constraints from which the parasites are released with increasing ability to acquire resources from the host. This evolutionary process also implies increasing host specificity which imposes new constraints on the ability to establish host connection. This explains the evolutionary stability of photosynthetic hemiparasites and their species richness which is one order of magnitude higher than that of holoparasites

Tracing nitrogen flow in a root-hemiparasitic association by foliar stable-isotope labelling

Background and aims – The resource flows in the host-hemiparasite association have been frequently studied by applying stable isotope techniques. However, these methods of artificial labelling required sophisticated equipment preventing their application to field experiments. Here, we aimed to test the applicability of the 15 N 13 C-urea foliar brushing method in tracing the resource flows between a root hemiparasite, Rhinanthus major, and a host, Triticum aestivum. In addition, the dynamics of the label movement was examined in order to provide an estimate of the most appropriate harvesting time.Methods – Double-labelled urea (98 atom % 15 N, 99 atom % 13 C) solution (2 g dm -3 ) was applied on host plants grown with hemiparasites by a single foliar brushing. Above- and belowground biomass of both species was harvested 3, 7, and 14 d after host labelling and its isotopic composition was analyzed. Final isotopic enrichment of biomass was expressed as the atom percent difference between labelled samples and the mean of corresponding controls.Key results – Our results showed that a single leaf-brushing with 15 N 13 C-urea provided sufficiently 15 N-labelled plant material, but it was insufficient to shift the natural abundance of 13 C in both species. Similar 15 N values were found for the host and hemiparasite biomass already 3 d after labelling, but the 15 N enrichment of attached hemiparasite significantly increased in time. Within a week, 15 N-label gradually dispersed into the host tissues and was simultaneously transferred into the hemiparasite via the root connections.Conclusions – We present foliar brushing by 15 N-urea as a simple and precise labelling method, which can be widely applied in both greenhouse and field experiments to examine the nitrogen flows between root hemiparasites and their host species. The transfer of nitrogen to the hemiparasite is fast and thus an experimental period of 7 d seems largely sufficient for field studies where the equilibrium state of labelling is of interest

Response of two hemiparasitic Orobanchaceae species to mowing dates: implications for grassland conservation and restoration practice

Background and aims – Rhinanthus major (= R. angustifolius ) and Melampyrum nemorosum are very sensitive to mowing date. As they are annuals without a long-term persistent seed bank and with a poor long-distance dispersal ability, seed loss caused by an unsuitable mowing date could lead to rapid population decline. Since their populations have disappeared from productive grasslands, they have become a focus of conservational management. Rhinanthus is also used in restoration projects as a treatment for reducing biomass, where its permanent populations are desired. We aimed to determine the earliest suitable mowing date for these species in White Carpathians Protected Landscape Area to support its administration to plan the management.Methods – We conducted a mowing experiment with plots mown on 7 and 18 June and 5 July 2012. The number of parasites was counted in central plots before mowing and in the following growing season. The phenology of hemiparasites and co-occurring species was recorded to better understand the effects of mowing date.Key results – Melampyrum showed a significant population decrease after mowing on 7 and 18 June, while the 5 July mowing did not inflict any significant change. The effect on Rhinanthus was not significant, as it was probably obscured by seed dispersal from the close surroundings.Conclusions – Mowing in July is suitable for both species, while June mowing leads to population declines. Mosaic mowing (which includes early mowing in some parts of a site), could therefore gradually eradicate Melampyrum. Rhinanthus metapopulation could compensate for the seed loss by seed dispersal from neighbouring parts, but careful monitoring is necessary. When using Rhinanthus in restoration experiments, postponed mowing is essential to keep its population permanent. Our conclusions are widely applicable, but the particular mowing date must be determined separately for each region, species and ecotype

Tracing nitrogen flow in a root-hemiparasitic association by foliar stable-isotope labelling

Background and aims – The resource flows in the host-hemiparasite association have been frequently studied by applying stable isotope techniques. However, these methods of artificial labelling required sophisticated equipment preventing their application to field experiments. Here, we aimed to test the applicability of the 15 N 13 C-urea foliar brushing method in tracing the resource flows between a root hemiparasite, Rhinanthus major, and a host, Triticum aestivum. In addition, the dynamics of the label movement was examined in order to provide an estimate of the most appropriate harvesting time.Methods – Double-labelled urea (98 atom % 15 N, 99 atom % 13 C) solution (2 g dm -3 ) was applied on host plants grown with hemiparasites by a single foliar brushing. Above- and belowground biomass of both species was harvested 3, 7, and 14 d after host labelling and its isotopic composition was analyzed. Final isotopic enrichment of biomass was expressed as the atom percent difference between labelled samples and the mean of corresponding controls.Key results – Our results showed that a single leaf-brushing with 15 N 13 C-urea provided sufficiently 15 N-labelled plant material, but it was insufficient to shift the natural abundance of 13 C in both species. Similar 15 N values were found for the host and hemiparasite biomass already 3 d after labelling, but the 15 N enrichment of attached hemiparasite significantly increased in time. Within a week, 15 N-label gradually dispersed into the host tissues and was simultaneously transferred into the hemiparasite via the root connections.Conclusions – We present foliar brushing by 15 N-urea as a simple and precise labelling method, which can be widely applied in both greenhouse and field experiments to examine the nitrogen flows between root hemiparasites and their host species. The transfer of nitrogen to the hemiparasite is fast and thus an experimental period of 7 d seems largely sufficient for field studies where the equilibrium state of labelling is of interest

Response of two hemiparasitic Orobanchaceae species to mowing dates: implications for grassland conservation and restoration practice

Background and aims – Rhinanthus major (= R. angustifolius ) and Melampyrum nemorosum are very sensitive to mowing date. As they are annuals without a long-term persistent seed bank and with a poor long-distance dispersal ability, seed loss caused by an unsuitable mowing date could lead to rapid population decline. Since their populations have disappeared from productive grasslands, they have become a focus of conservational management. Rhinanthus is also used in restoration projects as a treatment for reducing biomass, where its permanent populations are desired. We aimed to determine the earliest suitable mowing date for these species in White Carpathians Protected Landscape Area to support its administration to plan the management.Methods – We conducted a mowing experiment with plots mown on 7 and 18 June and 5 July 2012. The number of parasites was counted in central plots before mowing and in the following growing season. The phenology of hemiparasites and co-occurring species was recorded to better understand the effects of mowing date.Key results – Melampyrum showed a significant population decrease after mowing on 7 and 18 June, while the 5 July mowing did not inflict any significant change. The effect on Rhinanthus was not significant, as it was probably obscured by seed dispersal from the close surroundings.Conclusions – Mowing in July is suitable for both species, while June mowing leads to population declines. Mosaic mowing (which includes early mowing in some parts of a site), could therefore gradually eradicate Melampyrum. Rhinanthus metapopulation could compensate for the seed loss by seed dispersal from neighbouring parts, but careful monitoring is necessary. When using Rhinanthus in restoration experiments, postponed mowing is essential to keep its population permanent. Our conclusions are widely applicable, but the particular mowing date must be determined separately for each region, species and ecotype

Root hemiparasites suppress invasive alien clonal plants: evidence from a cultivation experiment

Alien invasive plants threaten biodiversity by rapid spread and competitive exclusion of native plant species. Especially, tall clonal invasives can rapidly attain strong dominance in vegetation. Root-hemiparasitic plants are known to suppress the growth of clonal plants by the uptake of resources from their below-ground organs and reduce their abundance. However, root-hemiparasites’ ability to interact with alien clonal plants has not yet been tested. We explored the interactions between native root-hemiparasitic species, Melampyrum arvense and Rhinanthus alectorolophus and invasive aliens, Solidago gigantea and Symphyotrichum lanceolatum. We investigated the haustorial connections and conducted a pot experiment. We used seeds from wild hemiparasite populations and those cultivated in monostands of the invasive plants to identify a possible selection of lineages with increased compatibility with these alien hosts. The hemiparasitic species significantly suppressed the growth of the invasive plants. Melampyrum inflicted the most substantial growth reduction on Solidago (78%), followed by Rhinanthus (49%). Both hemiparasitic species reduced Symphyotrichum biomass by one-third. Additionally, Melampyrum reduced the shoot density of both host species. We also observed some transgenerational effects possibly facilitating the growth of hemiparasites sourced from subpopulations experienced with the host. Native root hemiparasites can effectively decrease alien clonal plants’ biomass production and shoot density. The outcomes of these interactions are species-specific and may be associated with the level of clonal integration of the hosts. The putative selection of lineages with higher performance when attached to the invasive novel hosts may increase hemiparasites’ efficiency in future biocontrol applications

Interactions between hemiparasitic plants and their hosts

Hemiparasitic plants display a unique strategy of resource acquisition combining parasitism of other species and own photosynthetic activity. Despite the active photoassimilation and green habit, they acquire substantial amount of carbon from their hosts. The organic carbon transfer has a crucial influence on the nature of the interaction between hemiparasites and their hosts which can oscillate between parasitism and competition for light. In this minireview, we summarize methodical approaches and results of various studies dealing with carbon budget of hemiparasites and the ecological implications of carbon heterotrophy in hemiparasites