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Keywords:

  • competition;
  • decomposition;
  • foraging;
  • herbivory;
  • host range;
  • community diversity;
  • nutrient cycling;
  • parasitic plants;
  • secondary metabolites;
  • trophic interactions

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References
  • 1
    The hemiparasitic Orobanchaceae (ex-Scrophulariaceae) are characterized by a distinctive suite of ecophysiological traits. These traits have important impacts on host plants and non-host plants, and influence interactions with other trophic levels. Ultimately, they can affect community structure and functioning. Here, we review these physiological traits and discuss their ecological consequences.
  • 2
    The root hemiparasitic Orobanchaceae form a convenient subset of the parasitic angiosperms for study because: they are the most numerous and most widely distributed group of parasitic angiosperms; their physiological characteristics have been well studied; they are important in both agricultural and (semi)natural communities; and they are tractable as experimental organisms.
  • 3
    Key traits include: high transpiration rates; competition with the host for nutrients and haustorial metabolism of host-derived solutes; uptake of host-derived secondary metabolites; dual autotrophic and heterotrophic carbon nutrition; distinct carbohydrate biochemistry; high nutrient concentrations in green leaf tissue and leaf litter; and small (often hairless and non-mycorrhizal) roots.
  • 4
    Impacts on the host are detrimental, which can alter competitive balances between hosts and non-hosts and thus result in community change. Further impacts may result from effects on the abiotic environment, including soil water status, nutrient cycling and leaf/canopy temperatures.
  • 5
    However, for non-host species and for organisms that interact with these (e.g. herbivores and pollinators) or for those that benefit from changes in the abiotic environment, the parasites may have an overall positive effect, suggesting that at the community level, hemiparasites may also be considered as mutualists.
  • 6
    It is clear that through their distinctive suite of physiological traits hemiparasitic Orobanchaceae, have considerable impacts on community structure and function, can have both competitive and positive interactions with other plants, and can impact on other trophic levels. Many community level effects of parasitic plants can be considered analogous to those of other parasites, predators or herbivores.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

Plant groups with a particular suite of ecophysiological traits have the potential to exert specific impacts on the structure and function of the communities in which they occur. The most frequently cited examples are nitrogen fixers, which can enhance soil and ecosystem nitrogen pool size, accelerate nitrogen cycling, increase nitrogen concentration in tissues of co-occurring species, and stimulate growth and above-ground productivity of communities (e.g. Craine et al. 2002; Mulder et al. 2002; Spehn et al. 2002). In this review, we examine the distinctive physiological traits of a group of parasitic plants, the root hemiparasitic Orobanchaceae (ex-Scrophulariaceae) (Olmstead et al. 2001) and consider how these traits impact on hosts and co-occurring species (including those of other trophic levels) and the extent to which these traits explain the impact of root hemiparasites on the structure and function of the communities in which they occur.

The role of parasites and pathogens in natural communities is currently attracting much interest, for example with regard to their role in mediating the performance of invasive species (Mitchell & Power 2003; Torchin et al. 2003) and in the diversification and speciation of hosts or prey (Buckling & Rainey 2002). With regard to parasitic plants, the vast majority of studies have been restricted to interactions between host and parasite, although recent studies are taking a wider perspective by considering multispecies interactions (e.g. Matthies 1996; Pennings & Callaway 1996; Joshi et al. 2000). At the community level, the majority of studies on parasitic plants have been undertaken from a ‘behavioural’ viewpoint (e.g. host preference and selection), rather than an ecophysiological one. The root hemiparasitic Orobanchaceae represent a convenient subset of the parasitic angiosperms to study for a number of reasons: they form the most numerous and most widely distributed group of parasitic angiosperms; their physiological characteristics have been well studied (albeit with a focus on certain genera of importance, e.g. the tropical weed Striga); they are important in both agricultural and (semi)natural communities; and they are tractable as experimental organisms, particularly those with an annual life history.

Parasitic angiosperms are a large and diverse group of plants that are a common and important component of many natural ecosystems. They number > 3000 species (over 1% of land plants) representing c. 270 genera and c. 22 families (Nickrent et al. 1998; Press et al. 1999), but by far the greatest number are found within just one family, the Orobanchaceae (now including the parasitic members of the Scrophulariaceae, Young et al. 1999). This family contains nearly 2000 parasites in 78 genera and can be found across a diversity of ecosystems, extending from the Arctic to the tropics. As with all parasitic plants, they acquire water and solutes (carbon and nutrients) from their host plant(s) via their haustoria. The presence or absence of chlorophyll (hemi- and holoparasites, respectively) provides a clear functional distinction between those species that are partially and completely heterotrophic, respectively. Although the hemiparasitic Orobanchaceae generally constitute a relatively small component of above-ground biomass and occur at high densities only patchily, their impact on host species and communities can be considerable, most notably through the large reduction in host productivity and reproductive output that results from parasitism (Matthies 1995, 1996, 1997). It is of significance, therefore, that among the parasitic angiosperms, the Orobanchaceae display a large host range (for example up to 79 host species for Pedicularis candensis; Piehl 1963) and can simultaneously parasitize multiple hosts.

In this review the distinctive suite of ecophysiological traits characterizing the hemiparasitic Orobanchaceae will be examined, and the consequence of these traits discussed with respect to impacts on host species, non-host plants, interactions with other trophic levels and community structure–function relations.

Transpiration and water relations

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

Hemiparasitic Orobanchaceae are characterized by high transpiration rates, sometimes exceeding those of their host by an order of magnitude. Stomatal behaviour may also be distinctive, and stomata can remain at least partially open at night (Press et al. 1988) and during water stress (Shah et al. 1987). Smith & Stewart (1990) demonstrated that incubation of isolated epidermal strips from Striga hermonthica under high potassium concentrations resulted in a similar anomalous stomatal response to light (and CO2) to that of stomata in whole leaves of Striga. As high concentrations of potassium are often observed in hemiparasite leaves and potassium plays a central role in maintaining guard cell turgor, it was suggested that the anomalous stomatal behaviour was the result of high leaf potassium concentrations. Further, as high leaf potassium concentrations result from high transpiration rates (and a lack of phloem connections to re-translocate excess ions), enhanced stomatal opening may serve to enhance leaf potassium further (Smith & Stewart 1990). This positive feedback goes some way to explaining the exceptionally high transpiration rates in hemiparasitic Orobanchaceae. Overall, there is a fundamental difference in the significance of stomatal functioning between hemiparasitic Orobanchaceae and fully autotrophic plants; in the latter, stomata function to minimize water loss and to maximize carbon gain, whereas in hemiparasites, water loss is maximized to enhance carbon gain from the host (Press et al. 1988).

In addition, high transpiration rates also affect the energy budgets of leaves, resulting in cooling, particularly in warm environments. Evaporative cooling of Striga hermonthica grown at 40 °C was observed to be a considerable 7 °C (Press et al. 1989). Indeed, in that study, application of antitranspirant to Striga and the resulting decline in evaporative cooling was enough to result in leaf death through over-heating.

The significance of the host xylem as the primary water source can been seen in the dramatic decline in hemiparasite hydraulic resistance observed following attachment (e.g. Rhinanthus minor parasitizing barley; Seel & Jeschke 1999). Conversely, the high hydraulic resistance that occurs without host attachment may be indicative of the typically small root system of hemiparasites and limited access to water. The high hydraulic resistance of unattached hemiparasites may indeed be one reason for their poor growth without a host. Certainly, the immediate response of hydraulic resistance to host attachment is consistent with the rapid increase in growth of hemiparasites observed within 1 or 2 days of haustorial attachment (Klaren & Janssen 1978).

host and community consequences

High rates of transpiration can affect the water relations of the host and may consequently contribute to reduced host productivity. Gurney et al. (1995) and Frost et al. (1997) have observed reduced stomatal conductance, transpiration, water-use-efficiency, photosynthesis and, ultimately, growth in sorghum and maize parasitized by Striga hermonthica and data from the latter study suggest that lower photosynthesis is a consequence, rather than a cause, of lower stomatal conductance. These authors report a doubling of the concentration of abscisic acid in the xylem sap of Striga-infected sorghum compared with uninfected plants, suggesting that this plant hormone may be produced in response to water deficit in the host.

Reduced host productivity can ultimately change the competitive balance between host and non-host individuals in a community, and host plants may also be more susceptible to drought stress (again observed in sorghum infected by Striga; Press et al. 1987). Beyond this, it is yet to be determined whether patches of rapidly transpiring hemiparasites can reduce soil water, although this has been proposed as an outcome of heavy mistletoe infestation (Sala et al. 2001). Should this occur, there could be detrimental impacts on host and non-host plants alike. Community effects may extend beyond such responses, and it is not known, for example, whether the evaporative cooling of hemiparasite leaves can reduce the temperature of the surrounding community canopy. Temperature is the dominant abiotic factor affecting insect herbivores and changes of just a few °C can have major impacts on their development, survival, range and abundance (Bale et al. 2002). However, it is not known whether lower foliar temperatures can cool insect herbivores present on the hemiparasite against the large buffering effect of ambient air temperatures.

Heterotrophic carbon and nutrient acquisition

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

The close abutment of host and parasite xylem vessels means that any compound translocated in the host xylem may be transferred to the hemiparasite. Further, while hemiparasitic Orobanchaceae may be xylem-only feeders with no direct links to host phloem (Hibberd & Jeschke 2001), they can access the heterotrophic carbon supply (host photosynthate) that is translocated to host roots and acquired via the host xylem in the form of, for instance, amino acids. The degree to which this xylem supply of carbon meets the parasite's demands varies considerably (Press 1995). In Striga hermonthica, for instance, host-derived carbon ranged from 6% to 30% (Press et al. 1987; Cechin & Press 1993). The end result of carbon acquisition is a considerable increase in growth of the hemiparasite following attachment to a host; indeed, more than 40-fold increases in parasite productivity have been observed (e.g. Matthies 1997). However, the relative importance of enhanced uptake of nutrients, carbon and water has not been evaluated separately.

solute transfer across the host/parasite interface

The mechanisms for transfer of water and solutes across the haustorial interface are of particular interest. Importantly, this may influence community interactions as the ability of the hemiparasite to regulate the form and quantity of solutes transferred from the host should be markedly influenced by whether the transfer occurs as continuous xylem–xylem flow or through actively metabolizing haustorial cells.

The haustorium initially penetrates the host root by either splitting or flattening (crushing) the host root outer cortex (Riopel & Timko 1995; Dörr 1997). The connection between endophyte (as represented by the penetrating part of the haustorium) and host may be continuous but some studies (of Castilleja and Striga) clearly indicate the penetration of digitate, densely cytoplasmic cells between host vascular tissue. These may form ‘oscula’, which pierce through xylem pit membranes into the host-xylem lumen (Dobbins & Kuijt 1973; Dörr 1997) (Fig. 1). In the formation of an osculum, a tube-like cell from the endophyte penetrates through the pit membrane of the host xylem and then degrades, losing its protoplast and tip wall. This creates a hollow cup or trunk-like structure within the host xylem and results in a continuous open water-conducting system from host to parasite (Dörr 1997). Transfer of solutes may therefore occur either across host xylem pit membranes or though these hollow ‘oscula’ to the haustorium. Whether the continuous xylem–xylem transfer holds true for all hemiparasitic Orobanchaceae is unknown. Certainly, the haustoria of this group of plants appear to lack phloem, but in some species, significant numbers of ‘contact’ parenchyma cells, which have close abutment to host xylem, can be found at the host/haustorium interface (e.g. Triphysaria; Heide-Jørgensen & Kuijt 1993). Given their abundance and strategic alignment close to or in contact with major host vessels, their role as the primary solute and water transfer route seems likely, although as yet unproven.

image

Figure 1. Oscula of Striga hermonthica penetrating through the pitted xylem wall of the host Zea mays. Scale bar is 2 µm. Reproduced from Dörr (1997) by permission of Oxford University Press.

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transfer of nutrients

As hemiparasitic Orobanchaceae are partially autotrophic, it is perhaps the supply of nutrients, rather than carbon, from the host xylem stream that is of greater importance. Certainly, attachment to a host can more than double the concentration of mineral nutrients and amino acids in hemiparasite xylem, leading to higher concentrations in foliar tissue (Seel & Jeschke 1999). Indeed, in the case of Rhinanthus minor, it has been suggested that very low tissue phosphorus concentrations in unattached plants may be indicative of growth limitation by phosphorus and that uptake of host xylem phosphate may be the most important factor in enhancing Rhinanthus growth (Seel & Jeschke 1999). This is further supported by greater growth stimulation of unattached Rhinanthus by the addition of inorganic phosphate compared with the minor stimulation resulting from additions of nitrogen and potassium (Seel et al. 1993).

The form in which solutes are transferred is also of considerable interest. Using 15N labelled KNO3Pageau et al. (2003) observed rapid transfer of nitrogen assimilated by sorghum to Striga hermonthica in the form of both amino acids and nitrate. As the amino acid composition of host and parasite xylem sap was similar, it was suggested that the haustorium was relatively inactive in the metabolism of host-derived nitrogen and that transfer of nutrients may be non-selective. However, complete inactive and non-selective transfer seems unlikely. Taylor (2001), for example, demonstrated the presence of the enzymes nitrite reductase, glutamine synthetase and aspartate aminotransferase in haustoria of Striga hermonthica. Furthermore, activities of these enzymes were much higher than in stems and leaves, indicating that haustoria may indeed play an important role in metabolic processing. This is consistent with observations on Olax phyllantha (Olacaceaea; Pate et al. 1994) and Santalum acuminatum (Santalaceae; Tennakoon et al. 1997), where amino acid composition differs markedly between host xylem and both haustorial tissue and parasite xylem, indicating selective uptake and/or considerable metabolic transformation of solutes by haustoria. In fact, as direct xylem–xylem links are not observed in Olax and Santalum, metabolic transformation of solutes may well be expected if uptake occurs through the abundant parenchyma transfer cells (described above) rather than ‘inert’ oscula. Striga may represent the middle ground between non-selective transfer and complete haustorial control as the direct xylem–xylem flow possible through the oscula suggests that direct metabolic transformation by its haustoria could be partially bypassed (despite the presence of nitrogen metabolizing enzymes in certain haustorial cells).

host selection

The extent of dependency on host carbon will vary considerably according to parasite and host species. As discussed below, autotrophic carbon acquisition is a function of host nitrogen supply because greater photosynthetic rates are observed in parasites with higher foliar nitrogen concentrations, which can be gained from nitrogen-rich hosts (such as legumes) (see Press et al. 1987; Cechin & Press 1993). The enhancement of hemiparasite autotrophic nutrition and growth through parasitism of nitrogen-rich hosts is well documented (e.g. Seel & Press 1993; Seel et al. 1993; Matthies 1996) and has led to the assumption that nitrogen-rich plants, especially legumes, are ‘preferred’ hosts (Fig. 2). Certainly, the Fabaceae are a major host group for European hemiparasitic Orobanchaceae (Hodgson 1973; Weber 1976; Gibson & Watkinson 1989).

image

Figure 2. Relationship in Rhinanthus minor between mean light-saturated photosynthesis (A) and final height when parasitizing different host species. Symbols and abbreviated letter for host species and functional types are: □ = unattached (no host); ○ = non-legume dicots (E.v., Echium vulgare; P.l., Plantago lanceolata; G.v., Galium verum); ◆ = grasses (P.al., Poa alpina; F.o., Festuca ovina; B.p., Brachypodium pinnatum; P.an., Poa annua; P.p., Poa pratensis; B.c., Bromus commutatus; P.n., Poa nemoralis); ▵ = legume (T.r., Trifolium repens). Note: greatest light-saturated photosynthesis and height of Rhinathus occurs when parasitizing the nitrogen-rich legume Trifolium repens; Rhinanthus growth and rates of photosynthesis are generally lower when parasitizing non-legume dicots rather than grasses (re-drawn from Seel et al. 1993).

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Some parasitic plants can apparently ‘forage’ for their preferred hosts, as seen in the parasitic dodder (Cuscuta spp. Convolvulaceae), a shoot parasite that lacks roots. This parasite either accepts or rejects a host following stem-stem contact (i.e. this initial contact determines whether or not Cuscuta coils around and penetrates a host stem it touches) (Kelly 1990, 1992; Callaway & Pennings 1998). In hemiparasitic Orobanchaceae, selectivity can operate via chemical cues at the stage of germination (e.g. Striga; Bouwmeester et al. 2003 and references therein) or more commonly at the haustorial initiation stage (e.g. quinone-, flavonoid- and phenolic-induced haustorial development in Triphysaria; Matvienko et al. 2001; Tomilov et al. 2004; but see Westbury 2004). The degree of response to a specific chemical stimulant will vary considerably, even between species of the same genus (Jamison & Yoder 2001). Presumably, such differences can form part of the basis for parasite-specific host preferences, although how such chemical cues relate to host ‘quality’ or whether the parasite can select for high quality hosts is unknown. Additionally, selectivity will be further confounded by host resistance to penetration.

In fact, apparent selection may also be a passive process: a parasitic plant that performs well on a certain host species will have greater survival and longer life, and so become more associated with the suitable host species (Kelly et al. 1988). Apparent selection for the host is therefore an end result of parasite performance rather than an initial response to host suitability. Passive and active selection are not necessarily mutually exclusive, and may act together. While these two processes are yet to be investigated in the Orobanchaceae, both are observed in Cuscuta, where relative host use is a function of its growth and mortality on a specific host (Kelly et al. 1988) and where selection for nutrient-rich hosts can also occur through stem-stem contact (without the apparent need for penetration into the host) (Kelly 1992).

A further advantage of wide host range seen in the Orobanchaceae is that parasite performance may be enhanced on a mixed diet, i.e. when multiple hosts of different species are parasitized (rather than multiple hosts of the same species) (Govier et al. 1967). Marvier (1998a), for example, observed that growth and reproductive effort of Castilleja wightii was greatest when parasitizing a mixed diet of a legume and a non-legume (Lupinus arboreus and Eriophyllum stachaedifolium, respectively) rather than two hosts of the same species, even though parasitism of two legume hosts resulted in greater hemiparasite nitrogen content. The proposed mechanism for the benefit of multiple hosts is that a better balance of resources may be acquired and potential toxins from one particular host may not be acquired in damaging quantities. Further, while in the above example the legume has higher nitrogen content, its roots are more lignified and are therefore likely to be more difficult to penetrate than roots of the non-legume (Marvier 1998a). Other mixed diet benefits could occur from parasitism of species with access to spatially and temporally different resources. Certainly, Olax phyllanthi (Olacaceae) has improved water acquisition when parasitizing both shallow- and deep-rooted hosts in a dry SW Australian heath (Pate et al. 1990).

It is interesting to speculate that the benefit of a mixed diet may have allowed (or maintained) the evolution of a wide host range in hemiparasitic Orobanchaceae. However, the benefits of mixed diet are not always apparent (see Marvier 1998a and Matthies 1996). Certainly more work is needed to determine the extent to which mixed diets may improve hemiparasite performance, whether mixed diets are selected for or occur by chance, and whether parasitism of one host species first influences later selection of other host species.

host consequences

Surprisingly, the considerable uptake of solutes from host plants does not necessarily lead to large reductions of their concentrations in host xylem or leaf tissue (Press 1998) and modest increases in host xylem sap solute concentrations have been reported (Seel & Jeschke 1999). However, a lack of change in host tissue nutrient concentrations should not be seen as indicative of a non-detrimental impact, as nutrient concentrations may be maintained by reduced growth of the host. Indeed, a reduction in host growth and reproductive effort (flowering and fruiting) following attachment of a hemiparasite is extensively documented (e.g. Melampyrum arvense parasitizing Linum usitatissimum or Lolium perenne, Matthies 1996; Castilleja integra, C. chromosa, C. miniata, Orthocarpus purpurascens, Rhinanthus serotinus, R. minor, R. alectorolophus or Odontites rubra parasitizing Medicago sativa or Lolium perenne, Matthies 1995, 1997; Davies & Graves 1998; Matthies & Egli 1999).

Interestingly, Seel & Jeschke (1999) observed that parasitism of barley and clover by R. minor not only reduced the amino acid concentration in host xylem sap, but also changed the predominant transport amino acid in R. minor xylem from glutamine to asparagine. The mechanism of change appeared to be host specific; in clover, asparagine was the main xylem amino acid whether parasitized or not, and this was transferred to R. minor. In barley, glutamine was the principal amino acid when not parasitized, but parasite attachment induced asparagine as the principle amino acid, which was again then the predominantly transferred amino acid. This suggests that if the preferred transfer amino acid is not already dominant in the host, it can be induced by the parasite. Asparagine is also the amino acid transported in Striga-host association. Asparagine has a high N/C ratio, and its relative abundance further emphasizes the importance of N rather than C to the parasite.

community consequences

The physiological characteristics of hemiparasitic Orobanchaceae ultimately result in community level effects, largely but not exclusively mediated via their impacts on hosts. Of popular debate is their role in regulating ecosystem productivity and diversity. Through altering the competitive balance between host and non-host species, parasitic angiosperms can affect community structure, vegetation cycles and zonation (e.g. Gibson & Watkinson 1992; Pennings & Callaway 1996; Davies et al. 1997; Callaway & Pennings 1998; Marvier 1998b; Westbury & Dunnet 2000). Typically, parasitism by hemiparasitic Orobanchaceae reduces productivity of vegetation (Pennings & Callaway 2002) because the inefficient use of host nutrients means that reduced host biomass is not compensated for by the increase in parasite biomass (e.g. Matthies 1995, 1996, 1997; Matthies & Egli 1999). Davies et al. (1997) observed a biomass productivity depression of between 8% and 73% by Rhinanthus species across European ecosystems and comparable observations have been reported in restored grassland by Westbury & Dunnet (2000). Similarly, total host community biomass of a California coastal prairie was 14% greater in plots where Triphysaria pusilla had been removed (Marvier 1998b).

Additionally, there is much evidence to indicate that hemiparasitic Orobanchaceae can regulate ecosystem diversity. Whether diversity is enhanced or reduced appears to depend on whether the preferred hosts are dominants or not. In the examples of Davies et al. (1997), Westbury & Dunnett (2000) and Marvier (1998b), Rhinanthus or Triphysaria showed preference for grass hosts. As these were competitive dominants, their suppression by the parasitic plants allowed the expansion of (subordinate) forb species and therefore enhanced vegetation diversity. Conversely, in marshland and sand dune communities, Rhinanthus showed preference for competitively subordinate species and therefore helped to suppress system diversity (Gibson & Watkinson 1992). Removal of Rhinanthus therefore allowed the competitive subordinate species to expand and hence increased ecosystem diversity.

Beyond this, uptake of host solutes influences community level interactions of hemiparasites with other organisms. This may be especially true for organisms that consume host plants (such as herbivores and parasitic nematodes; Pennings & Callaway 2002) and are therefore in direct competition for the host resource. To date, however, this has been little studied in the Orobanchaceae, though Puustinen et al. (2001) have observed effects of dual parasitism by both Rhinathus serotinus and the cyst nematode Heterodera trifolii on the host Trifolium pratense. In this case the nematode appeared to be the ‘stronger’ parasite, as attachment to the Trifolium host did not enhance Rhinanthus growth if the host was also parasitized by Heterodera, while parasitism by Rhinanthus did not reduce the number or size of cysts produced by Heterodera.

Flowering of hemiparasitic Orobanchaceae is enhanced when they are attached to suitable hosts, leading to potential three-way interactions involving pollen or nectar feeders. Certainly, such interactions are observed in mistletoe (Phoradendron, Viscaceae) parasitizing juniper. Here, the mistletoe (a more reliable fruit source than its juniper host) attracts more avian frugivores, which disperse seeds of both host and parasite, resulting in enhanced juniper seedling recruitment (van Ommeren & Whitham 2002).

Autotrophic nutrition

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

photosynthesis

While hemiparasitic Orobanchaceae acquire carbon from the xylem stream of their host(s), members of this group are also represented among the most autotrophically active of hemiparasitic plants, and some annuals can complete their life cycle and successfully reproduce in the absence of a host. This is rarely seen in nature, however, because the severely stunted plants are likely to be out-competed by more vigorously growing neighbours (Press 1995). Rates of light-saturated photosynthesis are in the lower range for C3 plants and are influenced heavily by the host (particularly the host's nitrogen content). This was well documented by Seel et al. (1993) working with Rhinathus minor. In this species, light-saturated photosynthesis ranged from approximately 1 µmol CO2 g−1 DW min−1 when unattached, to 5.1 µmol CO2 g−1 DW min−1 when parasitizing Echium vulgare (the ‘poorest’ of 11 hosts), to 22.5 µmol CO2 g−1 DW min−1 when parasitizing Trifolium pratense. Photosynthetic rates in Rhinathus correlated with its own foliar nitrogen and chlorophyll a and b concentrations.

As hemiparasitic Orobanchaceae can photosynthesize, the uptake of nitrogen from the host transpiration stream is of dual importance because it not only enhances growth of the plant, but further serves to enhance the parasite's own carbon fixation through investment in Rubisco and photosynthetic pigments.

carbohydrate storage

The soluble carbohydrate reserves formed by hemiparasites differ from those of the host. In particular, high concentrations of polyols (polyhydric alcohols) occur in their tissue, either as cyclic polyols (cyclitols) such as inositol, or as acyclic polyols (alditols) such as mannitol (Press 1995). The particular polyol that accumulates in hemiparasitic Orobanchaceae is species dependent; in Rhinanthus spp. it is mannitol, whereas species of Euphrasia, Odontites and Pedicularis also contain some (athough less) galactitol. Parentucilla spp. contain approximately equal amounts of mannitol and galactitol, whereas in Melampyrum spp., there is no mannitol, only galactitol (Lewis 1984). Polyols lower the water potential of the hemiparasite to aid solute flow from the host and may act as compatible solutes counterbalancing the high concentrations of inorganic ions in the vacuole and conferring increased stability to enzymes and membranes. While these roles of polyols relate directly to the parasitic habit, numerous benefits have been attributed to polyols in other plants (e.g. in conferring drought, salt and freezing tolerance) (Adams et al. 1992; Karakas et al. 1997), yet to date the extent to which such benefits are conferred to hemiparasites remains unknown.

host and community consequences

The partial autotrophic nutrition of hemiparasitic Orobanchaceae could be expected to reduce the demand on host carbon compared with holoparasites, though in reality the source-sink relationship between host and parasite is not as simple as this. Most strikingly, hemiparasites tend to have a negative impact on host carbon gain, for example by reducing stomatal conductance, production of leaf area and Rubisco content (Watling & Press 2001). It has been suggested that the autotrophic capacity of root hemiparasites may in fact be the reason why they are generally confined to relatively nutrient-poor, low productivity communities (Matthies 1995), because partial reliance on their own photosynthesis means that they cannot compete effectively where shading by host species would be considerable (i.e. in nutrient-rich, high productivity habitats). Interestingly, reduction of host productivity by parasitism will serve to reduce above-ground competition for light (Matthies 1995) and in this way may be beneficial to the hemiparasite. However, as hemiparasite photosynthesis may saturate at low photon flux densities (Seel et al. 1993) the full impact of such shading needs further investigation.

Uptake of secondary metabolites

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

As a result of the apparent low selectivity of solute uptake, further opportunity for interactions between the hemiparasite, its hosts and other organisms results from the uptake of host secondary metabolites. Of particular interest are those compounds with antiherbivory, allelopathic (allelogenic) or pathogenic qualities, especially because host secondary metabolites may be transferred to all parts of the parasite (Marko & Stermitz 1997).

In general, hemiparasites should benefit from this uptake. The similar basic physiology of host and parasite (i.e. they are both higher plants) means that the toxic action of the secondary metabolite should be limited, at least in comparison with their impacts on an insect herbivores (Pennings & Callaway 2002). The uptake of these secondary metabolites occurs without cost (at least not over and above the cost of parasitizing the plant for water and other solutes) and these compounds need not then be synthesized by the parasite.

In practice, determining the metabolic cost to the host and conversely the metabolic saving to the parasite is complex and difficult; for example calculating the cost of maintaining a particular metabolic pathway. It is accepted that resistance to herbivores or pathogens must have an appreciable cost in general, otherwise all plants would either develop resistance or become extinct under selection pressure (Strauss et al. 2002). In reality, the cost to the plant (usually determined as impact on plant fecundity or growth) of producing defence secondary metabolites varies from no apparent cost (Vrieling & Van Wijk 1994; Adler et al. 1995) to considerable cost (e.g. flowering reduced by 25–30%, Thaler 1999; annual growth reduced by 25–54%, Pavia et al. 1999). Presently, we can only speculate that the benefit or metabolic ‘saving’ to the parasite of acquiring host secondary metabolites is equally as varied.

Transfer of secondary metabolites between host and hemiparasitic Orobanchaceae has been quantified on a number of occasions, particularly the transfer of alkaloids (compounds known for their antiherbivory, pathogenic and allelopathic action). For example, Stermitz & Harris (1987) detected pyrrolizidine and quinolizidine alkaloids in natural populations of Castilleja sulphurea on alkaloid-containing hosts (e.g. the lupin Lupinus argenteus ssp. rubricaulis). Numerous other examples of alkaloid uptake by hemiparasitic Orobanchaceae have been observed, for instance: between the hosts Senecio, Thermopsis, Lupinus and Pinus to Pedicularis species (Stermitz et al. 1989; Schneider & Stermitz 1990; Mead & Stermitz 1993); from Delphinium, Senecio, Lupinus and Liatris to Castillleja species (Stermitz & Harris 1987; Mead et al. 1992; Stermitz & Pomeroy 1992; Marko & Stermitz 1997); and from Lupinus to Orthocarpus (Boros et al. 1991). Further, Stermitz et al. (1993) observed iridoid glycoside transfer between a host and hemiparasite (Penstemon teucriodes and Castellija integra, respectively). Additionally, there is evidence to suggest non-selective uptake of these secondary metabolites as the spectrum of alkaloids found in parasites can match well with that found in the host (Marko & Stermitz 1997).

parasite–host–community interactions

Because host secondary metabolites can be transferred to many parts of the parasitizing plant, this may maximize the potential for the secondary metabolites to affect the parasite's own herbivores or parasites. In one example, Adler (2000) studied Castellija indivisa parasitizing either ‘sweet’ (containing only trace alkaloids) or ‘bitter’ (alkaloid producing) lines of Lupinus albus. Castellija indivisa, which itself does not produce alkaloids, acquired lupin alkaloids (principally lupanine) from parasitized bitter hosts but not from sweet hosts. Most significantly, Castellija parasitizing bitter lupins were less damaged by herbivory, and as a result were also more visited by pollinating hummingbirds and ultimately produced more seed than those parasitic on sweet lupins. Similarly, Marko & Stermitz (1997) observed that Castilleja sulphurea containing norditerpenoid alkaloids assimilated from Delphinium occidentale was highly toxic to two species of lepidopteran insect larvae (Euphydryas anicia and Trichoplusia ni), while pyrrolizidine alkoloids in Castilleja integra assimilated from Liatris punctata could affect early instar larvae of Thassalia leanira (Mead et al. 1992). Despite the apparent advantage of acquiring beneficial host secondary metabolites, there is no evidence to date for the evolution of selection for such hosts: while hemiparasitic Orobanchaceae appear to prefer nutrient-rich hosts, a preference for alkaloid-containing hosts has not been determined.

Interestingly, parasitism could have implications for the herbivore defence of the host. In a study by Puustinen & Mutikainen (2001), it was observed that Rhinanthus serotinus grew equally well on cyanogenic and acyanogenic Trifolium repens. However, while cyanogenesis greatly reduced herbivory of Trifolium by the snail Arianta arbustorum, this reduction was less when Trifolium was parasitized, i.e. Rhinanthus appeared to reduce the herbivore defence advantage of cyanogenic Trifolium over acyanogenic Trifolium. Such a loss of defence advantage should be considered as energetically costly to the Trifolium (in addition to the cost of increased herbivory) as cyanogenesis is known to reduce reproductive investment (cyanogenic Trifolium produce fewer flowers).

Beyond this it is interesting to speculate whether such transfer of metabolites has consequences for non-hosts. It may be predicted that if the productivity of the hemiparasite population is increased through greater protection by acquired secondary metabolites, then the plants may compete more effectively with host and non-host species for light. Further, uptake of secondary metabolites by hemiparasitic plants may also influence herbivory of neighbouring plants. While this has yet to be studied in the case of hemiparasites, the palatability of neighbouring plants is known to be influenced by herbivory on associated species (Tahvanainen & Root 1972; Hjältén et al. 1993; Frid & Turkington 2001), either through less palatable species acting as herbivore repellents for neighbouring palatable species (repellent plant hypothesis) or by palatable species attracting herbivores away from neighbouring species (attractant-decoy hypothesis) (Atsatt & O'Dowd 1976).

Root functioning

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

Hemiparasitic Orobanchaceae generally possess only small root systems (Press 1989) that can lack root hairs and may not form mycorrhizal associations (Fitter & Hay 1987; Harley & Harley 1987). Assimilation from the soil will be further limited following attachment to a host when this results in reduced biomass allocation to roots (e.g. Rhinanthus serotinis, Odontites rubra and Castilleja parasitizing Medicago, Matthies 1996; Matthies 1997; but see Matthies 1997 for an example of increased root allocation by Castilleja when parasitizing Lolium). It is therefore unsurprising that they have a limited capacity to assimilate nutrients from the soil (Seel et al. 1993). Indeed, this root structure (small, hairless, non-mycorrhizal) and functioning perhaps explains why growth of Rhinanthus minor appears to be most limited by phosphorus (Seel et al. 1993; Seel & Jeschke 1999) given its limited mobility in soil.

root functioning: host and community consequences

In addition to reducing the overall productivity of the host, hemiparasitic Orobanchaceae can alter host allometry and both higher and lower dry matter allocation to roots has been reported (e.g. Matthies 1995, 1997; Watling & Press 1997). However, the impacts on host roots go further and there is increasing evidence to show that parasitic angiosperms influence the mycorrhizal associations of host plants. Davies & Graves (1998), for example, observed that the percentage root length colonized in Lolium perenne by arbuscular mycorrhizal (AM) fungi was reduced by about 30% when parasitized by Rhinanthus minor (Lolium growth was also reduced by about 50%). This reduction in colonization may be explained if the mycorrhizal fungus is a weaker competitor for host carbon than the hemiparasite. Further, Rhinanthus growth and reproductive output was greater by 58% and 47%, respectively, when parasitizing mycorrhizal Lolium compared with non-mycorrhizal Lolium, indicating that the host's AM fungi may enhance availability of nutrients to the hemiparasite. Indeed, since the mycorrhizal stimulation of plant productivity was much greater for the hemiparasite than for the host, this indicates that any increase in nutrient supply was a direct effect of mycorrhizal uptake, rather than an indirect effect of mycorrhizal infection increasing host size (and therefore its nutrient source size to the hemiparasite). Hemiparasite–mycorrhiza interactions have also been reported by Salonen et al. (2000), where the hemiparasite Melampyrum had greater growth and produced more flowers when parasitizing Pinus sylvestris colonized by ecto-mycorrhizal (EM) fungi than when parasitizing non-mycorrhizal Pinus. EM symbiosis increased the growth of Pinus and thus greater resources could be made available to Melampyrum not just through nutrient uptake by the EM fungi, but also through greater photosynthetic leaf area of the larger mycorrhizal Pinus.

Foliar nutrients and retention during senescence

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

Two physiological traits that ultimately may have considerable impacts on ecosystems containing hemiparasites are the luxuriant use of host nutrients and very low nutrient retention rates in senescing parasite leaves. As a result, both living foliar tissue and leaf litter of hemiparasites have very high nutrient concentrations, generally much greater than concentrations found in co-occurring (host and non-host) species. In an extensive study of sub-Arctic species, Quested et al. (2003a) determined that foliar nitrogen concentration was on average 36 and 31 mg g−1 DW for annual and perennial hemiparasitic Orobanchaceae, respectively, compared with between 15 and 28 mg g−1 DW for co-occurring species without a major alternative nitrogen source (i.e. excluding nitrogen fixers and insectivorous plants). Importantly, nitrogen resorption efficiency was low in the hemiparasites, so litter also had far greater nitrogen concentration (31 and 19 mg N g−1 for annual and perennial hemiparasites, respectively) than most co-occurring species (8–11 mg N g−1). Only litter of nitrogen fixers and insectivorous plants had comparably high nitrogen concentrations (30 and 18 mg N g−1, respectively). Further, phosphorus concentrations in hemiparasite litter are also generally much greater than in litter of co-occurring species. In an earlier study, Quested et al. (2002) observed that phosphorus concentrations in litter of sub-Arctic Orobanchaceae (1.7–5.4 mg P g−1 DW) were on average 4.3 times greater than in litter of nine other commonly co-occurring species (0.3–1.9 mg P g−1 DW). In fact, this meant that hemiparasite litter was actually more enriched in phosphorus than nitrogen (litter N concentrations being 3.6 times greater in hemiparasite litter compared with co-occurring species).

foliar nutrients: litter input and decomposition consequences

Hemiparasitic Orobanchaceae therefore represent considerable point sources of nutrient-rich litter, the consequence of which is amplified because these species generally occur in nutrient-poor environments. For example, the high litter nitrogen concentration of Bartsia alpina increased annual nitrogen input from litter to soil by 42% in a sub-Arctic community within a 5-cm radius of the plant, despite being only 15% (by weight) of all species litter input (Quested et al. 2003a,b). Further, such litter can be regarded as ‘high quality’ because not only are nutrient concentrations high, but C : N ratios are low and recalcitrant components such as lignin may also be in low concentrations. For instance, litter of the annual hemiparasite, Euphrasia frigida, was found to have a C : N ratio of only 11, compared with 110 for the co-occurring sub-Arctic dwarf shrub Vaccinium uliginosum (Quested et al. 2002), while in a related study V. uliginosum litter was found to contain 25% lignin, compared with 13% lignin in litter of the co-occurring hemiparasite Bartsia alpina (Quested et al. 2003b).

The high quality of hemiparasite litter enhances the impact on nutrient availability because this litter decomposes rapidly and may enhance decomposition of other litter. In a related studies, Bartsia alpina litter decomposed faster than litter of co-occurring species, losing 5.4–10.8 times more nitrogen over a 240-day laboratory incubation (Quested et al. 2002) and 18 times more N during 2 years decomposition in the field (Quested et al. 2005). The addition of nitrogen-rich hemiparasite litter to that of co-occurring species may act to prime the more recalcitrant litter and enhance its decomposition rates, presumably by stimulating fungal and bacterial decomposers that may be nitrogen limited when acting on low quality litter of other species. Mass loss and CO2 release were at least equal to or greater than expected when mixtures of Bartsia litter and litter of co-occurring dwarf shrubs were decomposed in combination (Quested et al. 2002; but see Quested et al. 2005).

foliar nutrients: community consequences

From such studies, it is becoming increasingly apparent that hemiparasitic Orobanchaceae may play an important role in ecosystems through accelerated uptake and subsequent decomposition of nutrients. Where hosts are slow growing and long lived perennials (such as in the sub-Arctic), the hemiparasite can be seen as unlocking tightly held, slowly released, nutrients (Press 1998). Clonal hemiparasites (such as Bartsia alpina) can form rhizomes > 50 cm in length and can live for more than 100 years (Molau 1990; Nilsson & Svensson 1997) and thus may facilitate the redistribution of nutrients, making them potentially available to both host and non-host species. Quested et al. (2003b) observed that growth of Betula nana and Poa alpina seedlings was greater by up to 51% and 41%, respectively (with up to a twofold increase in foliar nitrogen concentration), when grown with a supply of Bartsia alpina litter compared with growth on litter of co-occurring species. This may well enhance seedling recruitment, especially in harsh climates such as the sub-Arctic, where nitrogen status and seedling growth rates are major factors that determine over-winter survival (Weih & Karlsson 1999) (Fig. 3).

image

Figure 3. Potential increase in winter survival of birch seedlings resulting from enhanced relative growth rate (RGR) when grown with litter from the hemiparasite Bartsia alpina. Winter survival/RGR line based on Betula pubescens from Weih & Karlsson (1999). RGR with and without Bartsia litter is of Betula nana taken from Quested et al. (2003b).

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It is likely that inputs of the nutrient-rich litter will affect the soil biota, with hemiparasite litter patches supporting a larger, more active and different diversity of soil organisms. Certainly, the nutrient-rich litter of legumes can support much greater active microbial biomass than non-legume species (Beare et al. 1990) and fungal community composition is highly sensitive to litter quality, as is the balance between bacterial and fungal components of the soil system (Wardle 2002). Nitrogen availability could also be enhanced further if nutrient-rich litter inputs enhance mineralization rates and thus release more of the large stock of previously unavailable (more recalcitrant) bulk soil nutrients.

Conclusion

  1. Top of page
  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References

In this review, we have described how the impacts of hemiparasitic Orobanchaceae on hosts, plant communities and other trophic levels result from their distinctive suite of ecophysiological traits, many of which stem from their dependency on host (xylem) sap and the mechanisms that have evolved to acquire carbon, nutrients and water from this source.

It is clear that this distinctive group of plants has a diversity of impacts on the communities in which they are found, and that impacts are likely to differ according to hosts, vegetation type and community structure. The most apparent (and most studied) impacts on hosts are usually negative, and as such, many of the impacts on plant communities arise from reduced host plant productivity, reproduction and competitive ability. However, it is also clear that the impacts of hemiparasitic Orobanchaceae should not be regarded solely as ‘detrimental’ or ‘negative’. Among the complex interactions of multispecies communities, one plant's loss is another's gain. More obvious ‘positive’ effects can result from the interactions of hemiparasites with their communities; perhaps the most striking (yet currently under-researched) being the increase in co-occurring plant fitness resulting from enhanced nutrient inputs from hemiparasite litter. Intriguingly, hemiparasites may therefore be considered to act in a more mutualistic way at the community level. Further, the potential for this distinctive group of plants to interact with and affect soil microbes and fauna and higher trophic levels is apparent, but also remains poorly understood. Finally, we have also proposed mechanisms for further potential impacts based on observations of other (non-Orobanchaceae) parasitic plants; it is apparent that more work is needed to understand the full impacts of hemiparasitic Orobanchaceae within communities and to understand how these impacts link with their physiological traits.

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  2. Summary
  3. Introduction
  4. Transpiration and water relations
  5. Heterotrophic carbon and nutrient acquisition
  6. Autotrophic nutrition
  7. Uptake of secondary metabolites
  8. Root functioning
  9. Foliar nutrients and retention during senescence
  10. Conclusion
  11. Acknowledgements
  12. References
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