Tansley review. Malcolm C. Press and Gareth K. Phoenix. New Phytologist (2005) 166:

Transcription

1 Review Blackwell Publishing, Ltd. Impacts of parasitic plants on natural communities Author for correspondence: Malcolm C. Press Tel: +44 (0) Fax: +44 (0) Malcolm C. Press and Gareth K. Phoenix Department of Animal and Plant Sciences, University of Sheffield, Western Bank, Sheffield, S10 2TN, UK Received: 4 October 2004 Accepted: 16 December 2004 Contents Summary 737 I. Introduction 738 II. Parasitism: direct consequences 738 III. Dynamics of parasite host interactions: host range, preference and selection 738 IV. Impacts of parasitic plants on the plant community 739 V. Impacts of the plant community on parasite populations 741 VI. Impacts of the parasite on other trophic levels 742 VII. Impacts of the parasite on the abiotic environment 747 VIII. Concluding remarks 748 References 748 Summary Key words: biodiversity, competition, ecosystem engineers, herbivory, keystone species, mutualism, nutrient cycling, seed dispersal. Parasitic plants have profound effects on the ecosystems in which they occur. They are represented by some 4000 species and can be found in most major biomes. They acquire some or all of their water, carbon and nutrients via the vascular tissue of the host s roots or shoots. Parasitism has major impacts on host growth, allometry and reproduction, which lead to changes in competitive balances between host and nonhost species and therefore affect community structure, vegetation zonation and population dynamics. Impacts on hosts may further affect herbivores, pollinators and seed vectors, and the behaviour and diversity of these is often closely linked to the presence and abundance of parasitic plants. Parasitic plants can therefore be considered as keystone species. Community impacts are mediated by the host range of the parasite (the diversity of species that can potentially act as hosts) and by their preference and selection of particular host species. Parasitic plants can also alter the physical environment around them including soil water and nutrients, atmospheric CO 2 and temperature and so may also be considered as ecosystem engineers. Such impacts can have further consequences in altering the resource supply to and behaviour of other organisms within parasitic plant communities. New Phytologist (2005) 166: New Phytologist (2005) doi: /j x 737

2 738 Review I. Introduction Parasitic plants are a taxonomically diverse group of angiosperms that rely partially or completely on host plants for carbon, nutrients and water, which they acquire by attaching to host roots or shoots using specialist structures known as haustoria and by penetrating host xylem and/or forming close connections with phloem. The site of attachment to the host classifies the parasite as either a root or shoot parasite, whereas the presence or absence of functional chloroplasts defines the parasite further as being either hemiparasitic or holoparasitic, respectively (Musselman & Press, 1995). Parasitic plants are common in many natural and seminatural ecosystems from tropical rain forests to the high Arctic (Press, 1998), accounting for 1% of angiosperm species ( ) within c. 270 genera and more than 20 families (Nickrent et al., 1998; Press et al., 1999). They occur in many life forms, including annual and perennial herbs (e.g. Rhinanthus spp. and Bartsia spp.), vines (e.g. Cuscuta spp. and Cassytha spp.), shrubs (e.g. Olax spp. and mistletoes) and trees (sandlewoods, e.g. Okoubaka aubrevillei, which grows up to 40 m tall; Veenendaal et al., 1996). Parasitism often severely reduces host performance, which leads to changes in competitive interactions between host and nonhost plants and a cascade of effects on community structure, diversity, vegetation cycling and zonation (Pennings & Callaway, 2002). Impacts on the plant community are enhanced further because parasitic plants simultaneously parasitise and compete with co-occurring plants; their own productivity and populations are therefore dependent on both the quality of the hosts that they parasitise and the strength of competition from neighbouring plants. Additionally, the uptake of host solutes can have consequences for organisms of other trophic levels (such as herbivores and pollinators), and co-occurring organisms may also be affected by the impacts of parasitic plants on the abiotic environment, including impacts on nutrient cycling, soil water relations, local temperature and atmospheric CO 2 concentrations. Importantly, such major impacts can occur even when parasitic plants are minor components of the ecosystem. Despite the profound effects that parasitic plants have on the communities in which they occur, they are still often ignored in community theory (highlighted by Pennings & Callaway, 2002). With this in mind, this review examines the numerous interactions that parasitic plants have with host and nonhost plant communities, with other organisms (including herbivores, pollinators, mycorrhizal fungi and other parasites) and discusses parasitic plant impacts on the abiotic environment to highlight the far-reaching consequences of these interactions for community structure and function. Because this review is primarily concerned with community level interactions, we only briefly review the direct impacts of parasitism on individual host plants; more detail of these direct impacts and their physiological basis can be found in, for example, Stewart & Press (1990), Press & Graves (1995), Watling & Press (2001) and Phoenix & Press (2005). II. Parasitism: direct consequences The acquisition of host resources can exert strong effects on host growth, allometry, reproduction and physiology (Press et al., 1999). Generally, parasitism reduces host productivity and/or reproductive effort, as has been extensively documented for both root parasites (Matthies, 1995, 1996, 1997; Seel & Press, 1996; Davies & Graves, 1998; Matthies & Egli, 1999) and shoot parasites ( Jeschke et al., 1994a,b; Silva & Martínez del Rio, 1996; Tennakoon & Pate, 1996; Howell & Mathiasen, 2004). In most cases, reduction in host performance is considerable, and in the most extreme cases, such as heavy mistletoe infestation, parasitism may result in host death (Aukema, 2003). Critically for community level impacts, effects on the host are often disproportionately great in comparison to the size of the parasite. This can result from both inefficient use of the resources by the parasite, such that reduction in host biomass is generally greater than the increase in parasite biomass (Matthies, 1995, 1996, 1997; Marvier, 1998b; Matthies & Egli, 1999), or from impacts on host physiology that further impair host performance (Watling & Press, 2001; Ehleringer et al., 1986). Further impacts can occur through effects on host allometry and architecture, most notable are the large witches brooms induced by mistletoes that impair the host tree s water balance and nutrient balance, and can reduce host photosynthesis and respiration rates (Ehleringer et al., 1986; Wanner & Tinnin, 1986; Parker & Riches, 1993; Sala et al., 2001; Meinzer et al., 2004). III. Dynamics of parasite host interactions: host range, preference and selection Community-level impacts of parasitic plants depend greatly on which species are parasitised. Ultimately, this is dependent on parasite host-range (diversity of hosts rather than geographical range), preference for particular host species, and the degree to which preferred species can be selected or foraged for. 1. Host range: parasitic plants are usually generalists Most parasitic plants can potentially attack a large number of different co-occurring species (i.e. they have a broad host range), often simultaneously (Gibson & Watkinson, 1989; Nilsson & Svensson, 1997; Pennings & Callaway, 2002; Westbury, 2004). In this respect, most parasitic plants can be considered as generalists (although there are notable exceptions). Examples of wide host range are documented for both root and shoot parasites. In the former case, Castilleja spp., for instance, are known to parasitise more than 100 different hosts from a variety of families (Press, 1998), whereas Rhinanthus minor has approximately 50 different host species from 18 New Phytologist (2005) 166: New Phytologist (2005)

3 Review 739 families within European grasslands, and in a dune system study, single R. minor plants have been found to parasitise up to seven different host species simultaneously (Gibson & Watkinson, 1989). Although shoot parasites tend to have a smaller host range than do root parasites (Norton & Carpenter, 1998), broad host ranges are still apparent, such as with Cuscuta spp. (dodders) with hosts that number in the hundreds (Kelly et al., 1988; Musselman & Press, 1995), whereas the tropical rain forest mistletoe Dendrophthoe falcata has approaching 400 known host species (Narasimha & Rabindranath, 1964; Narayanasamy & Sampathkumar, 1981; Joshi & Kothyari, 1985). Parasitic plants that can only utilise one or few host species are the exception rather than the rule, and perhaps the most notable among the root parasites is Epifagus virginiana (Orobanchaceae) which only parasitises Fagus grandifolia (Musselman & Press, 1995). Among shoot parasites, mistletoes provide some examples of narrow host range, including the dwarf mistletoe Arceuthobium minutissimum (Viscaceae), which only parasitises the pine species Pinus griffithii (syn. wallichiana) (Kuijt, 1969), and epiparasitic mistletoes (e.g. Phoradendron scabberimum), which only grow on other mistletoes (Musselman & Press, 1995). 2. Host preference: when generalists are specialists Intriguingly, despite the large host range of the majority of parasitic plants, many also show high levels of host preference, such that while many different plant species within a community can act as hosts, the majority of hosts are taken from just a subset of those available (e.g. Orobanchaceae: Werth & Riopel, 1979; Gibson & Watkinson, 1989; Santalaceae: Joel et al., 1991; Krameriaceae: Musselman & Dickison, 1975; Olacaceae: Musselman & Mann, 1978). In this way, parasitic plants are not true generalists and can behave more as specialists. Therefore, we can assume that these parasites may behave as discriminate consumers by increasing their parasitism of better hosts (i.e. hosts that most greatly enhance the growth, reproduction and fitness of the parasite population). What makes some hosts better than others is not always clear, although studies to date show that both root and shoot parasites often prefer, or perform better on, hosts with a high nitrogen content, such as legumes (Schulze & Ehleringer, 1984; Kelly, 1992; Seel & Press, 1993; Seel et al., 1993; Matthies, 1996, 1997; Radomiljac et al., 1999), or hosts that have readily accessible vascular systems (Kelly et al., 1988) and/or lower defence capacity (Cameron, 2004; Cameron et al., 2005). Hosts may also be preferred if they are available as a resource for longer (e.g. a preference for woody perennials over herbaceous annuals; Kelly et al., 1988) or if they have ready access to limiting resources (e.g. a preference for deep rooted hosts with access to the water table during drought; Pate et al., 1990a). Further, parasitic plants may use different host species within different parts of their geographic range (e.g. mistletoes: Martínez del Rio et al., 1995; Norton & Carpenter, 1998; Aukema & Martínez del Rio, 2002) or even show differences in host preference between parasites in different parts of the same population (Gibson & Watkinson, 1989). Why parasites may have a different host preference in different locations is not known, although for mistletoes, changes in host susceptibility to infection between different regions has been suggested as one mechanism (Snyder et al., 1996). Host preference may also depend on the diversity of potential hosts available; mistletoes of the Loranthaceae show a low host preference in heterogeneous tropical rain forests and high host preference in less diverse temperate forests. This may occur because preference for a particular (and perhaps better) host is more possible in a less diverse system where the preferred host is therefore a larger component of the community (Norton & Carpenter, 1998). 3. Host selection Selection of or foraging for preferred hosts can operate in a number of ways, both spatially and temporally. A particular host species may appear to be preferred simply as an artefact of its abundance, i.e. an abundant host species is used more because it is more likely to be encountered by the parasite. Even so, true host preference when a host is used disproportionately to its abundance appears to be a common occurrence among both root and shoot parasitic plants. For such preference to operate, the parasite may need chemical cues from suitable hosts to trigger germination (e.g. Bouwmeester et al., 2003) and/or haustorial development (Matvienko et al., 2001; Tomilov et al., 2004). Because rapid attachment following germination is critical for many parasites, many have adapted to follow such chemical cues. Host preference therefore results because the parasite is less likely to germinate and/or produce haustoria away from the triggering host species (Musselman & Press, 1995). Chemical cues may also play a role in the active foraging seen in the stem parasites Cuscuta subinclusa and C. europea. These parasites display nastic movements that allow them to forage for hosts, rejecting (growing away from) or accepting (coiling around) the stem of hosts following contact, but before any penetration of the host shoot is made (Kelly, 1990, 1992). The mechanisms underpinning these responses, however, remain elusive. IV. Impacts of parasitic plants on the plant community Impacts on the community are often considerable and occur because: (i) impacts on the host are great; (ii) major impacts occur even where the parasite is a minor component of the ecosystem; and (iii) a single parasite may impact on a large area of the ecosystem. Over one season, for instance, a single Cuscuta plant may form thousands of connections with many host species and may cover an area greater than 100 m 2 (Kelly, New Phytologist (2005) New Phytologist (2005) 166:

4 740 Review 1990), resulting in considerable impacts on the plant community despite its being perhaps less than 5% of vegetation biomass (Pennings & Callaway, 1996). 1. Plant community biomass Because reductions in host growth are often greater than the increases in parasite growth, reductions in plant community productivity are often observed. Rhinanthus species, for instance, have been shown to reduce total productivity in European grasslands by between 8 and 73% (Davies et al., 1997), whereas dwarf mistletoes (one of the most destructive pathogens of commercially viable trees) can reduce volume growth of Douglas fir, for instance, by up to 65% (Mathiasen et al., 1990). Interestingly, Joshi et al. (2000) have shown that community biomass reductions by Rhinanthus are smaller in grasslands that have greater functional diversity. They proposed that higher plant diversity could buffer the effects of overexploitation of individual host species such that less sensitive species will compensate for loss of biomass of more sensitive species. Further, Matthies and Egli (1999) have shown that host biomass is reduced the most under low nutrient conditions, suggesting that community-level impacts may also be greatest where resources acquired by the parasite (such as nutrients) are limiting. 2. Plant community diversity Impacts on community structure can also be great. Primarily, impacts on host performance shift the competitive balances from host species toward nonhost species and ultimately result in community change. Very often, the most heavily parasitised species are competitive dominants, in which case parasitism facilitates the maintenance of competitively subordinate species (Press, 1998). The preference (by choice or chance) of Rhinanthus spp. for grass hosts, for instance, is well known to reduce grass biomass and facilitate an increase in forb abundance (Davies et al., 1997). Introduction of Rhinanthus is therefore used as an effective management tool to restore high-fertility/low-diversity pastures to high-diversity meadows (Westbury & Dunnett, 2000). In the case of shoot parasites, the salt marsh studies of Pennings & Callaway (Pennings & Callaway, 1996, Callaway & Pennings, 1998) have shown that Cuscuta salina has preference for the host Salicornia virginica. Because this host is the community dominant, its suppression in areas where Cuscuta is abundant facilitates the expansion of the competitively subordinate species Limonium californicum and Frankenia salina. This in turn increases community diversity. Conversely, where preferred hosts are competitively subordinate, parasitism can reduce abundance of subordinate species, allow greater dominance of the most abundant species and hence reduce community diversity. Such a case was observed in sand dune systems, where Gibson & Watkinson (1989) showed that Rhinanthus minor known usually to increase diversity tended to reduce diversity by preferentially parasitising subordinate species. Further, supposed preferred host species may not necessarily decline in abundance where the abundance of other potential hosts is great enough to hide the preferred host from the parasite. For instance, N- rich legume species are well known to be good (preferred) hosts for Rhinanthus spp., but in the study of Davies et al. (1997), Rhinanthus actually increased, rather than reduced, legume abundance in European grasslands. Davies et al. (1997) proposed that the high density of grasses overrides host preference, so that grasses are parasitised more and suppressed more because their roots are far more likely to be encountered than roots of preferred legumes. By facilitating coexistence and diversity through limitation of competitive dominants, parasitic plants can be considered as keystone species (Paine, 1969; Pennings & Callaway, 1996; Smith, 2000). Certainly, parasitic plants fit the keystone species definition of exerting a major influence on community assemblages out of proportion to their own abundance or biomass. Paine (1969) coined the keystone species term from observations of the predatory starfish, Pisaster, which increases the diversity of mussel bed communities by consuming dominant species of mussel and hence facilitates the coexistence of subordinate mussel species. The keystone species term has since been used to describe the central role played by a variety of species within communities, from sea otters and fish (Estes & Palmisano, 1974; Power, 1995) to succulent trees and Sphagnum mosses (Midgley et al., 1997; Mitchell et al., 2002). In many cases, parallels with the action of parasitic plants are clear. In addition to the effects of parasitism, annual parasites may further increase diversity through facilitation of invasion; for example, an increase in bare ground following die-back of Rhinanthus alectorolophus at the end of the season was seen to facilitate weed invasion and led to increased community diversity (Joshi et al., 2000). Interestingly, facilitation of invasion was less in more diverse communities, indicating that a negative feedback mechanism may operate: once the community reaches a certain level of diversity, invasion may no longer be facilitated; should community diversity decline again, invasion will once again increase. 3. Vegetation cycling and zonation The effects of parasitic plants on community structure are often dynamic and will change depending on environmental conditions or the performance of the parasite itself. Parasitic plants can therefore impact and regulate both vegetation cycling and zonation. At the simplest level, an aggressive parasite can drive a preferred host locally extinct; this may, in turn, result in the parasite also becoming locally extinct. The originally suppressed preferred host is then able to return, and following this, the parasite can then re-establish on the new New Phytologist (2005) 166: New Phytologist (2005)

5 Review 741 Fig. 1 Change in abundance of two competing pickleweeds, Arthrocnemum subterminale and Salicornia virginica, at their ecotone following parasitism by the shoot parasite Cuscuta salina in a Californian salt marsh. Where Cuscuta is absent (open bars), Arthrocnemum may decline under competition from the expanding Salicornia. Because Cuscuta, however, preferentially parasitises Salicornia over Arthrocnemum, the presence of Cuscuta (closed bars) results in a decline in Salicornia and hence allows Arthrocnemum to expand. This action effectively stops Salicornia from invading into the Arthrocnemum zone (reproduced with permission from Callaway & Pennings, 1998). host plants. Such population cycling has similarities with some predator prey cycles (see e.g. Krebs et al., 1995). Perhaps the best example of such cycling in parasitic plants is provided by Cuscuta salina described previously (Pennings & Callaway, 1996). Not only does Cuscuta facilitate invasion of subordinate species, but this process also initiates vegetation cycling because Cuscuta populations decline following Salicornia suppression, which in turn reduces the facilitation of Limonium and Frankenia invasion and allows Salicornia to return. Such cycling interactions may also explain why some parasites, such as Rhinanthus minor, appear to move through vegetation. Patches heavily infested with Rhinanthus will quickly decline in grass (preferred host) abundance, leaving neighbouring uninfected patches with higher grass abundance more suitable for establishment of the next generation of Rhinanthus seedlings, and the Rhinanthus patch will appear to move over time. The vegetation left behind will recover rapidly (Gibson & Watkinson, 1992) and will once again become suitable for Rhinanthus. Such interactions between hosts and parasites are often constrained by environmental factors that can influence the virulence of the parasite and the competitiveness of hosts and nonhosts. Through this, parasitic plants can regulate the zonation of vegetation. Again, Cuscuta salina provides and excellent example of this. Whereas Salicornia dominates in the lower part of the salt marsh, Arthrocnemum subterminale dominates at higher elevations (Callaway & Pennings, 1998) and the two compete strongly at their abrupt ecotone (Pennings & Callaway, 1992). Cuscuta preferentially parasitises Salicornia, conferring a competitive advantage to Arthrocnemum, and effectively stops Salicornia from invading into the Arthrocnemum zone (Fig. 1). Because Cuscuta patches are dynamic, this probably makes the Salicornia Arthrocnemum ecotone less abrupt. Further, the competitive advantage provided to Arthrocnemum by Cuscuta is seen to be much greater at lower elevations within the marsh. Here, Arthrocnemum is much less competitive in these more saline areas, so the benefit of being released from Salicornia competition by Cuscuta is much greater. This suggests that the advantage of parasitism to a subordinate species should be greatest where it is most at a competitive disadvantage (i.e. where competition is most asymmetrical) (Callaway & Pennings, 1998). V. Impacts of the plant community on parasite populations At a simple level, greater abundance and/or performance of preferred or good hosts will enhance the performance (growth and reproduction) of the parasite. Root hemiparasites, for instance, are particularly common in grassland systems because grasses are often preferred hosts, having abundant root systems (i.e. easy to locate) and fine roots that are easy to penetrate. Similarly, Cuscuta shows greater biomass and reproduction within patches of preferred/good hosts (Kelly et al., 1988; Kelly, 1990). The age of the hosts selected by the parasite may also impact on its own population dynamics. Seel and Press (1996), for instance, observed that Rhinanthus minor produced significantly less biomass when parasitising 6-month-old Poa alpina hosts than when parasitising mature plants. Further, Rhinanthus attached to Poa that had been previously parasitised grew better than Rhinanthus attached to Poa not previously parasitised. It was suggested that the parasite benefited from previous parasitism of the host because this reduced host flowering that would otherwise represent a loss of resources. Impacts of hosts on parasite communities clearly not only depend on what is parasitised but also when parasitism occurs. New Phytologist (2005) New Phytologist (2005) 166:

6 742 Review Because parasites compete with hosts for resources, competition from the host can also affect parasite populations. With some hemiparasites, competition with hosts for light is believed to restrict the parasites to low-productivity environments (Matthies, 1995). In high-productivity environments, increased shading of these partially autotrophic plants may reduce their competitiveness. This theory is supported by the work of Matthies (1995), who showed that shading from host plants reduced biomass of the root hemiparasites Rhinanthus seratonis and Odonites rubra by 30%, and also by the work of Joshi et al. (2000), in which survival of Rhinanthus alectorolophus in grassland communities was inversely correlated with community leaf-area index. It has been suggested therefore that parasiteinduced reductions in host and community biomass represent an advantage to some hemiparasites because this also reduces competition for light. In extreme cases, where resource limitation results in parasite death, host access to limiting resources can almost completely control parasite distribution. Summer drought in southwest Australian heaths restricts Olax phyllanthi to patches of deep-rooted hosts that have access to the water table (Pate et al., 1990a). Further, where environmental conditions vary within a community, the parasite may prefer hosts in areas where the hosts experience less environmental stress. For instance, Miller et al. (2003) suggest that in a semiarid flood plain in southern Australia, eucalyptus (E. largiflorens) are poor hosts for the mistletoe Amyema miquelii in areas of greater water and/or salinity stress. Beyond this, parasite performance may depend on the diversity of its host community. Joshi et al. (2000) found that both growth and reproductive effort of Rhinanthus alectoroluphus was greatest when growing in plant communities of high functional diversity (Fig. 2). This may occur because: (i) high functional diversity facilitates a mixed diet believed to be beneficial to some parasitic plants (Marvier, 1998a); (ii) high diversity enhances the chance of the parasite finding a good host; and/or (iii) the parasite benefits form greater host biomass (resource size) where higher diversity leads to greater community productivity ( Joshi et al., 2000). Host preference can result in aggregation of the parasites around preferred hosts; such aggregation can occur at the level of the host, patch or community. The majority of mistletoes within a population, for example, may be found on just a few host individuals a conseqeuence of the mistletoe seed dispersal mechanisms (see Section VI.3) with most other hosts of the same species harbouring no or few parasites (Aukema, 2003). Mistletoes also aggregate at the community and landscape scale. Isolated trees are unlikely to become infected, and migration of the parasite through the landscape may be slow until a new site eventually reaches some threshold of mistletoe density and then readily attracts its avian seed dispersers (Aukema, 2003). Finally, parasites can directly impact on their own populations through parasitism of members of their own population Fig. 2 The influence of grassland community functional diversity on the performance of the root hemiparasite Rhinanthus alectorolophus. Grassland communities with greater plant functional diversity support greater growth and reproductive effort of Rhinanthus (reproduced with permission from Joshi et al., 2000). (self-parasitism). This is seen in the case of Olax phyllanthi, where physiologically superior individuals acquire resources from inferior Olax plants and which may therefore explain the rapid self-thinning which takes place in Olax populations during early postfire succession (Pate et al., 1990b). VI. Impacts of the parasite on other trophic levels It is not only plants within communities that can be heavily affected by parasitic plants. Many other organisms, including birds and insect herbivores, other parasites and mycorrhizal fungi can be affected, either directly or indirectly. This wide range of impacts occurs because many parasitic plants can have both top-down effects (e.g. as a natural enemy of the host) and bottom-up effects (e.g. as a keystone resource). For instance, herbivorous insects and mammals consume parasitic plant foliage; frugivorous birds consume mistletoe berries; fungi and insects can take advantage of host plants weakened New Phytologist (2005) 166: New Phytologist (2005)

7 Review 743 by parasitic plants (Parker & Riches, 1993; Aukema, 2003); and parasitic plants can compete with other consumers where the host is a shared (and potentially limiting) resource (Pennings & Callaway, 2002). 1. Interactions with herbivores In the case of indirect effects, hosts weakened by a parasitic plant may be more susceptible to insect attack. In the case of dwarf mistletoes (Arceuthobium spp.), the increased susceptibility of host trees may result from their increased water stress because the parasite transpires readily despite its relatively small surface area even under water-limited conditions (Fisher, 1983). A resulting reduction in host resin exudation may be one mechanism for increased host susceptibility (Parker & Riches, 1993; Aukema, 2003). Conversely, herbivores may feed less on parasitised hosts, possibly because of competition between herbivore and parasite for the host resource. Puustinen & Mutikainen (2001), for example, observed that parasitism by Rhinanthus serotinus reduced feeding of the snail Arianta arbustorum on Trifolium repens hosts (this being an indicator of the competition for resources between snail and parasitic plant). However, when feeding on cyanogenic and acyanogenic Trifolium hosts was compared, the saving in leaf area consumed of cyanogenic Trifolium over acyanogenic individuals was lower in parasitised hosts, i.e. parasitism appeared to reduce the benefits of cyanogenisis in alleviating herbivory. In natural ecosystems, this could prove particularly costly for the acyanogenic plants because cyanogenesis is energetically expensive. Further, where parasites and herbivores compete for the same host resource, the performance of the parasite may be reduced where hosts experience heavy herbivory. Salonen and Puustinen (1996) observed that partial defoliation of the host Agrostis capillaris could reduce flowering of the parasite Rhinanthus serotinus. Parasitic plants themselves can be attractive food sources for herbivores. In the case of mistletoes, their fruit is often available year round, their flowers provide abundant nectar and their foliage is often rich in nutrients (Watson, 2001). Indeed, fruit, flowers and foliage of mistletoes are known to be food for some 66 families of birds, 30 families of mammals and even one fish species (Watson, 2001), in addition to an unknown diversity of insect herbivores. The quality of the parasite as a resource to these herbivores can be greatly affected by host nutrient status. Although nutrient-rich hosts benefit both holo- and hemiparasites, enhanced nutrition of the parasite can also cause it to be more attractive to insect herbivores and to increase the population growth of those herbivores further. Survival of the aphid, Nearctaphis kachena, for instance, when feeding on the root-hemiparasite Castilleja wightii, was positively correlated with the N concentration of the host plant (Marvier, 1996). Castilleja performance was therefore poorer on N-rich hosts because of resource competition with the larger aphid population. In this case, hosts with high N content were poorer hosts for Castilleja in the presence of herbivores. Further, N-rich hosts were therefore better as indirect host for aphids than they were as direct host for Castilleja because N-rich hosts increase Castilleja aphid populations at the expense of Castilleja performance. The host plant may not only affect parasite herbivore interactions through uptake of nutrients, but also through uptake of host secondary metabolites that may have antiherbivory properties. The uptake of host alkaloids by root-hemiparasitic Orobanchaceae has been well documented (e.g. Stermitz et al., 1989; Schneider & Stermitz, 1990; Mead & Stermitz, 1993; Marko & Stermitz, 1997) and reductions in herbivory or herbivore performance when feeding on the alkaloidacquiring parasites have been observed (Marko & Stermitz, 1997; Mead et al., 1992). Loveys et al. (2001) observed that fruit of the root hemiparasite Santalum acuminatum (the quandong) contained a natural insecticidal compound acquired from neighbouring Melia azadarach hosts. The uptake of such compounds from the host was proposed to be beneficial because a bioassay using the apple moth (Epiphyas postvittana) showed that its larvae suffered higher mortality when feeding on fruit of Santalum growing near Melia hosts. This may also explain the observation of commercial growers that Santalum growing near Melia have fruit that suffer less insect attack. In addition to such direct benefits, the parasite may also gain indirect benefits from uptake of secondary metabolites. In the case of Castilleja indivisa, Adler (2000) observed that this root hemiparasite not only gained from reduced herbivory by insect larvae when acquiring alkaloids from bitter lupine hosts (compared with alkaloid-free sweet lupine hosts), but the reduced herbivory of floral parts increased the visitation by hummingbird pollinators (Fig. 3). In turn, the Castilleja parasite showed greater seed production and hence gained increased fitness from both reduced herbivory and increased pollination. The proposed benefits of the mixed diet mentioned previously (see Section IV) may also extend to host mediated impacts on herbivory. Marvier (1998a) observed that a mixed diet of legume and nonlegume hosts not only enhanced the growth of Castilleja wightii (compared with double legume or double nonlegume hosts) but also resulted in slower growth of aphid colonies feeding on the Castilleja. Such benefits may provide one reason for the maintenance of a broad host range by many parasitic plants growing in natural communities (i.e. in the presence of herbivores) despite certain hosts appearing to be far more beneficial to parasite performance in pot studies (i.e. in the absence of herbivores). Parasitic plants may also mimic or use their host s foliage to avoid herbivory. Protective cryptic mimicry in mistletoes (Barlow & Wiens, 1977) where the mistletoe foliage appears similar to its host s may protect the mistletoe against vertebrate herbivores that use visual cues for feeding selection. Such mimicry may be important (and indeed appears more New Phytologist (2005) New Phytologist (2005) 166:

8 744 Review Fig. 3 Uptake of host alkaloids can benefit parasitic plants. (a) Herbivore damage (mainly from moth larvae) on the root hemiparasite Castilleja indivisa when parasitic on either bitter (high alkaloid content) or sweet (low alkaloid content) lupine hosts. Uptake of lupine alkaloids clearly reduces herbivory of the parasite. (b) Pollinator visits to the Castilleja when parasitic on either bitter or sweet lupines. Uptake of alkaloids from bitter lupines increases pollinator visits (mainly by hummingbirds) to the Castilleja possibly because the less herbivore-damaged Castilleja provide greater nectar rewards (redrawn with permission from Adler, 2000). frequently) in mistletoes that are nutritionally better food sources than their hosts, i.e. those with higher nitrogen and protein concentrations than their hosts (Ehleringer et al., 1986). Conversely, mistletoes with lower tissue nutritional quality than their hosts may benefit from advertising this fact by not mimicking host foliage (Ehleringer et al., 1986). Certainly, mistletoes with lower tissue quality than their hosts are more likely to lack mimicry (Ehleringer et al., 1986; Bannister, 1989). However, the relationship between mistletoe foliar quality and mimicry for herbivore defence is open to debate because the relationship between foliar N and mimicry is apparent in populations of mistletoes (in New Zealand) which probably evolved in the absence of and therefore without selection pressure from herbivorous mammals (Bannister, 1989). Further debate arises because levels of herbivory may not necessarily be lower in mimic compared with nonmimic mistletoe species (Canyon & Hill, 1997), and because mistletoe leaf N may be directly related to host N (Glatzel, 1987; Canyon & Hill, 1997). A simple direct relationship between mistletoe nutritional quality and mimicry cannot be assumed. 2. Interactions with pollinators Two groups of parasitic plants show particularly close interactions with pollinators and seed dispersers: the mistletoes and the Rafflesiaceae. The latter, particularly species of the genera Rafflesia and Rhizanthes, consist almost entirely of endothermic flowers and lack stems and leaves. High respiration rates and endothermy combine to create flowers that are up to 9 K warmer than surrounding ambient air and have considerably elevated local CO 2 concentrations. These factors, in combination with the release of volatiles, which give the flowers the odour of faeces or carrion, result in the attraction of blowflies that pollinate these parasitic flowers (Patiño et al., 2000, 2002). The endothermy and high respiration rates are metabolically costly, but these costs are ultimately passed to the hosts that provide substrates for respiration (Patiño et al., 2002). In the case of Rhizanthes, the effective mimicry of faeces and carrion further enhances pollination by the blowflies because oviposition can be stimulated, which increases the time the blowflies spend inside the flower while searching for somewhere to lay. Mistletoes show close interactions with pollinators and their seed vectors, associations that can be considered truly mutualistic. Mistletoes therefore may act simultaneously as parasites and mutualists in natural communities. Many mistletoes in the Loranthaceae are dependent on birds to open flower buds and act as pollinators, and therefore often have large, odourless flowers of bright colour to attract these pollinators (Watson, 2001). The explosive action on flower opening insures transfer of pollen to the bird and in return allows the bird access to a previously untapped nectar supply which is often available in large quantities and particularly rich in sugars (Stiles & Freeman, 1993; Baker et al., 1998). Such luxurious provision of carbohydrate-rich nectar may be made possible because the substrates are provided by two sources: the host and the partially autotrophic mistletoe. It appears that for both mistletoes and the Rafflesiaceae, the parasitic habit allows energetically expensive mechanisms for the attraction of pollinators. 3. Interactions with seed dispersers For most mistletoes, birds act as seed dispersers, and in some instances the same species may act as both pollinator and seed disperser (Kuijt, 1969; Robertson et al., 1999). Indeed, many of the bird species are highly specialised to consume mistletoe berries (Restrepo et al., 2002), and even in those mistletoes where initial seed dispersal is by hydrostatic explosion, birds can play a subsequent role in transporting seeds further (Watson, 2001). Fruits are often adapted for bird dispersal: they are usually large; conspicuously coloured; and are often high in soluble carbohydrate, minerals, lipids and fats, and can have an abundance of amino acids (Chiarlo & Cajelli, 1965; Godschalk, 1983; Lamont, 1983). As with nectar rewards, the provision of such energetically expensive fruit New Phytologist (2005) 166: New Phytologist (2005)

9 Review 745 may be facilitated by the parasitic habit, which will confer much of the production cost to the host. The close association of avian frugivores with mistletoes may be further enhanced because these fruit dispersers may find the fruit reward available all year round. This is achieved through discontinuous ripening of a single mistletoe (prolonging duration of fruit provision) and asynchrony in peak fruiting time between individual mistletoes of the same population or between mistletoes of separate population (Watson, 2001). A key feature of the frugivore mistletoe association is that the behaviour of the seed disperser is modified by the mistletoe to enhance successful seed dispersal (cf. blowfly oviposition stimulation to enhance pollination of Rhizanthes). To aid seed dispersal, a sticky viscin coats the mistletoe seed, allowing it to adhere to host branches following defecation or regurgitation by the avian vector (Reid et al., 1995; Aukema, 2003). Indeed, this effect is the origin of the name mistletoe, which approximates to dung-stick, a name based on the early observations that mistletoes appear where bird droppings are deposited on trees. Further, because defecated or regurgitated seed may stick to the bird s bill or abdomen, the birds will engage in bill or abdomen wiping to dislodge the seed, and because such behaviour often takes place on suitable host branches, the seed is effectively stuck to the host by the bird. The chance of seed being deposited on suitable hosts is enhanced further because a suitable host already parasitised by mistletoes will carry the mistletoes fruit reward and attract further avian mistletoe dispersers. Mistletoes therefore are among the few examples of plants with directed dispersal, ensuring that seed is often moved to suitable hosts (Aukema, 2003). Perhaps this explains why mistletoe seeds germinate readily in most situations without the need for a specific chemical germination cue (Norton & Carpenter, 1998). Beyond this, where the same frugivore species disperse seeds of both mistletoe and host, novel tripartite mutualistic associations can develop. Such a case occurs with Townsend s solitaires (Myadestes townsendi) that forage for seed of the mistletoe Phoradendron juniperinum and its juniper host, Juniperus monosperma (van Ommeren & Whitham, 2002). The mistletoe provides a stable and prolonged resource of fruit, whereas the juniper fruit supply is much more variable: mistletoe berry production therefore most strongly regulates the abundance of the avian frugivores, and far more of these birds are attracted to juniper stands infected with mistletoe than to uninfected juniper stands. The junipers ultimately benefit, because the mistletoes attracts greater populations of the juniper/ mistletoe shared seed dispersal agent (the Townsend s solitaires), the end result being that mistletoe-infected juniper stands have higher juniper seedling densities (van Ommeren & Whitham, 2002). However, there are trade-offs because at very high mistletoe densities, the negative physiological impacts of the mistletoe on juniper hosts will outweigh any positive effect of attraction the Townsend s solitaires and, further, at such high Fig. 4 Effects of increasing mistletoe density on co-occurring juniper and avian frugivores. (a) As mistletoe densities increase, infected (solid line) and uninfected (dashed line) juniper benefit because the mistletoes attract avian frugivores which disperse seed of both mistletoe and juniper. At very high mistletoe densities, in infected juniper, the benefits of frugivore attraction are outweighed by the negative physiological impacts of parasitism; conversely, uninfected junipers continue to benefit from the increasing attraction of avian frugivores. (b) The effects of avian frugivores on the juniper is positive at low and intermediate mistletoe densities due to the attraction of avian frugivores which disperse the juniper seeds. However, at very high mistletoe densities, the avian seed dispersers have an overall negative effect through their dispersal and spread of the parasitic mistletoes (redrawn with permission from van Ommeren & Whitham, 2002). mistletoe densities, the attraction of Townsend s solitaires may be detrimental to the juniper because this will serve to enhance the mistletoe population further (Fig. 4). The close host parasite vector association means that parasite seed vectors may have patchy distributions determined by the parasite and its host. The abundance of Chilean mockingbirds (Mimus thenca), for instance, is strongly associated with the prevalence of Tristerix aphyllus, a mistletoe parasitic New Phytologist (2005) New Phytologist (2005) 166:

10 746 Review on columnar cacti (Martínez del Rio et al., 1996), which in turn is restricted to north-facing slopes populated by its cacti hosts. This association also provides an example of where the behaviour of seed dispersal agents can be used by hosts to reduce the chance of mistletoe infection (rather than being used by the parasite to increase infection). In this case, the Tristerix mistletoe reduces the reproductive effort in the cacti hosts, but the resulting selection pressure appears to select for cacti with longer spines that deter the mistletoes avian seed vectors (Martínez del Rio et al., 1995; Medel, 2000; Medel et al., 2004). As highlighted by Medel et al. (2004), the aggregation of parasites within a community is therefore not only dependent upon the attraction of seed vectors to already infected hosts, but also on host resistance traits. 4. Interactions with other (nonplant) parasites of the host Where two parasites share the same host, either one parasite may facilitate the establishment of the other (e.g. by weakening the host), or there may be direct competition between the two parasites for host resources (Petney & Andrews, 1998). Interactions between parasitic plants and other parasitic organisms have been little studied, but it can be predicted from theory that attack by multiple parasites will be more detrimental to the host and that the most aggressive of the two parasites will benefit to the detriment of the other. These predictions are supported by Puustinen et al. (2001), who studied dual parasitism of Trifolium pratense by the root hemiparasite Rhinanthus serotinus and the cyst nematode Heterodera trifolii. Simultaneous parasitism by both parasites reduced Trifolium biomass more than parasitism by either parasite alone. Further, Heterodera appeared to be a more aggressive parasite than Rhinanthus because the reduction in Trifolium biomass was greater under parasitism by the cyst nematode than under parasitism by the root hemiparasite. The competitive advantage of Heterodera over Rhinanthus was confirmed under dual parasitism conditions where attachment to the Trifolium host did not enhance Rhinanthus growth if the host was also parasitised by Heterodera, while conversely, parasitism by Rhinanthus did not reduce the number or size of cysts produced by Heterodera. 5. Interactions with soil microbes Parasitic plants can have considerable impacts on soil organisms, even though their direct contact with the soil system through roots may be minimal or nonexistent. Both root and shoot parasites, for instance, can reduce the mycorrhizal associations of host plants. Gehring and Whitham (1992) found that colonisation of arbuscular mycorrhizal (AM) fungi on Juniper monosperma tree roots was negatively associated with mistletoe (Phoradendron jumiperum) density. This may be driven by two mechanims: either AM fungi increase resistance of the juniper host to mistletoe infection and/or (because mistletoes and mycorrhizas compete for host photosynthate) mycorrhizal infection rates will be lower where mistletoes are stronger competitors for plant carbon. The latter seems more likely because it was also observed that reductions in mycorrhizal associations caused by mistletoe infection were greater in female trees than in males, presumable because female trees invest more photosynthate in reproductive structures, therefore increasing the competition for photosynthate between mistletoes and AM fungi (Gehring & Whitham, 1992). Similar parasite mycorrhiza interactions have been observed for root hemiparasitic plants. Rhinanthus minor has been shown to reduce AM colonisation of Lolium perenne by about 30% (Davies & Graves, 1998). Again, this reduction in colonisation may be explained if the AM fungi are weaker competitors than the hemiparasite for host carbon. This was further supported by the observation that Rhinanthus appeared to benefit from AM colonisation of the host, showing greater growth and reproductive output on AM colonised Lolium. Clearly, the AM fungi did not significantly reduce the acquisition of host carbon by Rhinanthus while Rhinanthus may have benefited from enhance nutrition of AM colonised hosts. Indeed, because mycorrhizal stimulation of plant productivity was much greater for Rhinanthus than for Lolium, the indirect benefits of AM fungi to Rhinanthus were greater than their direct benefits to Lolium. Similarly, Salonen et al. (2000) observed that the hemiparasite Melampyrum had greater growth and produced more flowers when parasitising Pinus sylvestris colonised by ecto-mycorrhizal (EM) fungi than when parasitising nonmycorrhizal Pinus. Because EM symbiosis increased the growth of Pinus, it was proposed that greater photosynthate could be made available to the Melampyrum (despite competition with EM fungi) because of the greater photosynthetic leaf area of the larger mycorrhizal host (Salonen et al., 2000). A further way in which parasitic plants may impact on soil microbes is through inputs of their particularly nutrient-rich litters. Although such impacts are yet to be directly measured, parasite litter is known to impact on nutrient cycling (discussed in Section VII) (Quested et al., 2002, 2003a,b) so we should also expect considerable impacts on soil organisms. Because nutrient-rich litter can support greater, more active microbial populations (Beare et al., 1990), and because litter quality is known to affect fungal community composition and the balance between bacterial and fungal components of the soil system (Wardle, 2002), nutrient-rich parasite litter may have similarly large effects on the soil biota. 6. Effects on the diversity of other (nonplant) organisms Given the role of parasitic plants as a keystone resource within communities and their considerable impact on the diversity of co-occurring plants, it is perhaps unsurprising that they also have profound effects on the diversity of other organisms. In addition to their importance as a food resource for birds and New Phytologist (2005) 166: New Phytologist (2005)

11 Review 747 invertebrates, mistletoes can alter the structure of the habitat for many organisms that live on or within the host. Witches brooms and mistletoe clumps are used extensively as nesting or roosting sites for birds, either as structural support for nests or to aid in concealment and may provide hibernation sites or shelter in hot weather for mammal species such as pine martens, porcupines and squirrels (reviewed by Watson, 2001). The silviculture practise of sanitising forest stands by removing infected trees (and therefore also removing witches brooms) can therefore be to the detriment of wildlife using these structures (Bull et al., 2004). Also, mistletoe foliage may be used in nest lining, perhaps intriguingly because the foliage of some species may have antibacterial properties and may stimulate the immune function of fledglings (Watson, 2001). Further, through increasing the chance of host mortality, mistletoes can create a more heterogeneous mosaic of habitat structure (Bennetts et al., 1996). Given these numerous roles, it is perhaps unsurprising that mistletoes have been shown to increase the diversity of forest insects and birds, the former also potentially increasing the abundance and diversity of the later. Such mechanisms are apparent in, for instance, Colorado Ponderosa pine forests, where bird number and diversity are positively correlated with the level of dwarf mistletoe (Arceuthobium vaginatum) infestation despite this species of mistletoe rarely being used as a food source by birds (Bennetts et al., 1996). In this case, the number of cavity nesting birds is also greater in heavily mistletoe-infested sites, probably because more tree snags are available as a result of greater tree mortality in heavily infested stands. Similar impacts for root parasites have yet to be reported. However, because root parasites often alter the diversity of co-occurring plants and can increase habitat heterogeneity through their own patchy distribution, impacts on the diversity of other organisms such as invertebrate herbivores seem likely. VII. Impacts of the parasite on the abiotic environment In addition to being considered as keystone species, parasitic plants can also be seen as ecosystem engineers (organisms that modulate the availability of resources by causing physical state changes in biotic and abiotic materials) ( Jones et al., 1994). Within this definition, their role as autogenic engineers (which change the environment through their own physical structure) has been discussed above, for instance, where mistletoes are used as nesting sites for birds, or where the die-back of Rhinanthus opens gaps in grassland communities, thus facilitating the invasion of weeds ( Joshi et al., 2000). However, parasitic plants can also play a major role as allogenic engineers, which change the environment by transforming materials from one physical state to another. This role is perhaps best exemplified by their impacts on nutrient cycling, particularly by root hemiparasites. These plants often occur in nutrient-poor communities, and it is becoming increasingly apparent that their effects on nutrient cycling within these systems can be considerable. The transformation of materials that occurs in this allogenic engineering process is the unlocking of nutrients from more recalcitrant or less available forms into more labile, available forms. Parasitic plants typically have much higher concentrations of foliar nutrients than their hosts (reviewed by Lamont, 1983; Pate, 1995), typically being two- to fourfold greater for N and P in root hemiparasite foliage (Quested et al., 2002, 2003a,b) and up to 20-fold greater for K in mistletoes (Lamont, 1983). Further, because nutrient resorption efficiency is low, litter may have similar concentrations of nutrient as living foliage (Quested, 2002, 2003a,b). In a study of seven annual and perennial species of sub-arctic root hemiparasitic Orobanchaceae, of 64 co-occurring species, only plants with an alternative N source (N-fixers and carnivorous plants) had equivalently high concentrations of N in litter (Quested et al., 2003b). It was apparent therefore that these hemiparasites could represent a considerable point source of nutrients. This was confirmed with litter-fall studies using Bartsia alpina, which was seen to increase annual litter-n input to soil by 42% within a 5-cm radius of its stem. These litter inputs are considered to be of heightened importance because they decompose faster and release nutrients more rapidly than litter of co-occurring species, and, further, may stimulate the decomposition of more recalcitrant litters of co-occurring species when mixed (Quested et al., 2002; Quested et al., 2005). In the nutrient-limited environments where such parasites often occur, the potential for impacts on the nutrition of cooccurring plants is clear. Indeed, a bioassay study showed that, compared with litter inputs of other co-occurring species, Bartsia alpina litter could considerably increase foliar N concentration (twofold increase) and growth ( 50% increase) of two commonly co-occurring species, Betula nana and Poa alpina (Quested et al., 2003a). Clearly, such impacts on growth are likely to affect the competitive balance between species, with those plants most able to access parasite litter nutrients benefiting the most. The importance of this release of nutrients may be further heightened because host species are often slow-growing, longlived and are often evergreen with nutrient-poor, slowly decomposing litter. As such, the acquisition of nutrients from such hosts and its release in more labile form as parasite litter represents the unlocking of tightly and long-held nutrients (Press, 1998). Also, this process may act to concentrate nutrients in the vicinity of the parasite, but because many hemiparasites are clonal (such as Bartsia alpina, which can form rhizomes > 50 cm in length; Nilsson & Svensson, 1997), there may also be a significant redistribution of nutrients unlocked from host species, possibly making them more available to more host and nonhost plants. Such redistribution will be further enhanced where reciprocal parasitism occurs (parasites attached to each other). In such cases, resources acquired by one parasite can become shared between parasites (Prati et al., 1997) that will New Phytologist (2005) New Phytologist (2005) 166:

12 748 Review then become redistributed through the senescent leaves of both individuals. In the case of shoot parasites such as mistletoes, there will be little redistribution of nutrients spatially because parasite litter will fall below the host tree; however, this parasitism will still unlock host tree nutrients and redistribute it to understorey plants. As yet, however, we know of no study that has determined whether understorey vegetation below mistletoe-infected trees differs from the understorey vegetation of uninfected trees. Finally, given that some parasitic plants may be long-lived (e.g. for more than 100 yr; Molau, 1990), the impacts of this continuous enhancement of nutrient inputs may build up to have considerable impacts on local biogeochemical cycling. In addition to their impacts on biogeochemical cycling and nutrient availability, parasitic plants may also impact on water availability as result of their very high rates of transpiration (Ehleringer & Marshall, 1995) and further impact on host water relations. By increasing the whole-tree water use, for instance, mistletoes may reduce soil water potentials, and so reduce the availability of this resource to host and nonhost species alike (Sala et al., 2001). Further, Marvier (1998b) suggested a similar mechanisms to explain why the root hemiparasite Triphysaria pussilus does not release subordinate dicots from competitive exclusion when vigorously parasitising dominant prairie grasses. In this case, it was proposed that where Triphysaria grows particularly well on its preferred grass hosts, its high transpiration rates result in reduced soil water potentials, and hence effectively outcompetes dicots for this limited resource. Marvier (1998b) highlighted that in such circumstances, the successful exploitation of preferred dominant host species is counterintuitively not good for subordinate nonhost species. Impacts on nutrients and soil water may help to maintain a heterogenous patchy distribution of these key resources. This, in turn, may enhance biodiversity of co-occurring species at the ecosystem scale because the point-to-point differences in resource supply will allow coexistence of different plant species, each most suited to (or a superior competitor within) each patch with a particular composition of resources (Tilman, 1997). Other abiotic factors which can be influenced by parasites include atmospheric CO 2 concentrations and floral temperatures, which, in the case of the Rafflesiaceae, may aid in attraction of pollinating insects (see description of Rafflesia and Rhizanthes in Section VI.2). However, whereas the endothermic flowers of the Rafflesiaceae can be considerably warmer than ambient air temperatures, the high transpiration rates of some other parasitic plants may make parasite foliage considerably cooler. This has yet to be studied in parasites of natural ecosystems, but certainly the considerable transpiration of the crop parasite Striga hermonthica can cool its canopy temperature by 7 C below that of its host (sorghum) and ambient air (Press et al., 1989). Although 7 C represents a considerable cooling, to date, the significance of this for other organisms, such as insect herbivores, is unknown. VIII. Concluding remarks Parasitic plants are a diverse group of organisms with regard to their taxonomy, morphology and biogeography. In this review, we have demonstrated that they can play key roles in determining community structure and function and should be considered as both keystone species and allogenic and autogenic ecosystem engineers. The combination of both topdown and bottom-up effects means that they can have considerable impact on multiple trophic levels within communities, affecting population dynamics, diversity and distributions of co-occurring host and nonhost plants, invertebrates, birds and mammals. Further, despite their minimal contact with the soil system, they may also impact greatly on the soil biota and soil resources: this can have further consequences for cooccurring organisms. Parasitic plants are clearly major and key components of many ecosystems, given the considerable extent of their impacts (even when minor components of ecosystems), the diversity of ecosystems in which they occur, and the diversity of organisms with which these parasites interact. Parasitic plants should not be ignored in community study or theory. References Adler LS Alkaloid uptake increases fitness in a hemiparasitic plant via reduced herbivory and increased pollination. American Naturalist 156: Aukema JE Vectors, viscin, and Viscaceae: mistletoes as parasites, mutualists, and resources. Frontiers in Ecology and Environment 1: Aukema JE, Martínez del Rio C Variation in mistletoe seed deposition: effects of intra- and interspecific host characteristics. Ecography 25: Baker HG, Baker I, Hodges SA Sugar composition of nectar and fruits consumed by birds and bats in the tropics and subtropics. Biotropica 30: Bannister P Nitrogen concentration and mimicry in some New-Zealand mistletoes. Oecologia 79: Barlow BA, Wiens D Host-parasite resemblance in Australian mistletoe: the case for cryptic mimicry. Evolution 31: Beare MH, Neely CL, Coleman DC, Hargrove WL A substrate induced respiration (SIR) method for measurement of fungal and bacterial biomass on plant residues. Soil Biology and Biochemistry 22: Bennetts RE, White GC, Hawksworth FG, Severs SE The influence of dwarf mistletoe on bird communities in Colorado ponderosa pine forests. Ecological Applications 6: Bouwmeester HJ, Matusova R, Zhongkui Beale MH Secondary metabolite signalling in host parasitic plant interactions. Current Opinion in Plant Biology 6: Bull EL, Heater TW, Youngblood A Arboreal squirrel response to silvicultural treatments for dwarf mistletoe control in northeastern Oregon. Western Journal of. Applied Forestry 19: Callaway RM, Pennings SC Impact of a parasitic plant on the zonation of two salt marsh perennials. Oecologia 114: Cameron DD Role for differential host resistance to the hemiparasitic angiosperm, Rhinanthusminor (L.) in determining the structure of host plant communities. PhD Thesis, University of Aberdeen, UK. Cameron DD, Hwangbo J-K, Keith AM, Geniez J-M, Kraushaar D, Rowntree J, Seel W Interactions between the hemi-parasitic New Phytologist (2005) 166: New Phytologist (2005)

13 Review 749 angiosperm Rhinanthus Minor L. & its. hosts: from the cell to the ecosystem. Folia Geobotanica. (in press.) Canyon DV, Hill CJ Mistletoe host-resemblance: a study of herbivory, nitrogen and moisture in two Australian mistletoes and their host trees. Australian Journal of Ecology 22: Chiarlo B, Cajelli E Fatty acids and amino acids in the berries of Loranthus europaeus. Bollettino Chimico Farmaceutico 104: Davies DM, Graves JD Interactions between arbuscular mycorrhizal fungi and the hemiparasitic angiosperm Rhinanthus minor during coinfection of a host. New Phytologist 139: Davies DM, Graves JD, Elias CO, Williams PJ The impact of Rhinanthus spp. on sward productivity and composition: implications for the restoration of species-rich grasslands. Biological Conservation 82: Ehleringer JR, Marshall JD Water relations. In: Press, MC, Graves, JD, eds. Parasitic Plants. London, UK: Chapman & Hall. Ehleringer JR, Ullmann J, Lange OL, Farquhar GD, Cowan IR, Schulze ED, Ziegler H Mistletoes a hypothesis concerning morphological and chemical avoidance of herbivory. Oecologia 70: Estes JA, Palmisano JF Sea otters: their role in structuring nearshore communities. Science 185: Fisher JT Water relations of mistletoes and their hosts. In: Calder, M, Bernhardt, P, eds. The Biology of Mistletoes. Sydney, Australia: Academic Press, Gehring CA, Whitham TG Reduced mycorrhizae on Juniperus monosperma with mistletoe the influence of environmental stress and tree gender on a plant parasite and a plant-fungal mutualism. Oecologia 89: Gibson CC, Watkinson AR The host range and selectivity of a parasitic plant: Rhinanthus minor L. Oecologia 78: Gibson CC, Watkinson AR The role of the hemiparasitic annual Rhinanthus minor in determining grassland community structure. Oecologia 89: Glatzel G Haustorial resistance, foliage development and mineral nutrition in the hemiparasitic mistletoe Loranthus europaeus Jacq. (Loranthaceae). In: Weber, HC, Forstreuter, eds. Parasitic Flowering Plants. Proceedings of the 4th International Symposium on Parasitic Flowering Plants. Marburg, Germany: Phillips Universität, Godschalk SKB A biochemical analysis of the fruit of Tapinanthus leedertziae. South African Journal of Botany 2: Howell BE, Mathiasen RL Growth impacts of Psittacanthus angustifolius Kuijt on Pinus oocarpa Schiede in Honduras. Forest Ecology and Management 198: Jeschke WD, Baumel P, Rath N, Czygan FC, Proksch P. 1994b. Modeling of the flows and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa roxb and its host Lupinus albus L.2. Flows between host and parasite and within the parasitized host. Journal of Experimental Botany 45: Jeschke WD, Rath N, Baumel P, Czygan FC, Proksch P. 1994a. Modeling the flow and partitioning of carbon and nitrogen in the holoparasite Cuscuta reflexa roxb and its host Lupinus albus L.1. Methods for estimating net flows. Journal of Experimental Botany 45: Joel DD, Kleifeld Y, Bucsbaum H Osyris alba causing damage in orchards. In: Ransom, JK, Musselman, LJ, Worsham, AD, Parker, C, eds. Proceedingd of the 5th International Symposium of Parasitic Plants. Nairobi, Kenya: CIMMYT, Jones CG, Lawton JH, Shachak M Organisms As Ecosystem Engineers. Oikos 69: Joshi GCPCP, Kothyari BP New host of Dendrophthoe falcata (Linn. f.) Etting. Indian Journal of Forestry 8: 235. Joshi J, Matthies D, Schmid B Root hemiparasites and plant diversity in experimental grassland communities. Journal of Ecology 88: Kelly CK Plant foraging: a marginal value model and coiling response in Cuscuta subinclusa. Ecology 71: Kelly CK Resource choice in Cuscuta europaea. Proceedings of the National Academy of Sciences of the USA 89: Kelly CK, Venable DL, Zimmerer K Host specialization in Cuscuta costaricensis: An assessment of host use relative to host availability. Oikos 53: Krebs CJ, Boutin S, Boonstra R, Sinclair ARE, Smith JNM, Dale MRT, Martin K, Turkington R Impact of food and predation on the snowshoe hare cycle. Science 269: Kuijt J The Biology of Parasitic Flowering Plants. Berkeley, CA, USA: University of California Press. Lamont B Mineral nutrition of mistletoes. In: Calder, M, Bernhardt, P, eds. The Biology of Mistletoes. New York, USA: Academic Press, Loveys BR, Tyerman SD, Loveys BR Transfer of photosynthate and naturally occurring insecticidal compounds from host plants to the root hemiparasite Santalum acuminatum (Santalaceae). Australian Journal of Botany 49: Marko MD, Stermitz FR Transfer of alkaloids from Delphinium to Castilleja via root parasitism. Norditerpenoid alkaloid analysis by electrospray mass spectrometry. Biochemical Systematics and Ecology 25: Martínez del Rio C, Hourdequin M, Silva A, Medel R The influence of cactus size and previous infection on bird deposition of mistletoe seeds. Australian Journal of Ecology 20: Martínez del Rio C, Silva A, Medel R, Hourdequin M Seed dispersers as disease vectors: Bird transmission of mistletoe seeds to plant hosts. Ecology 77: Marvier MA Parasitic plant host interactions: Plant performance and indirect effects on parasite-feeding herbivores. Ecology 77: Marvier MA. 1998a. A mixed diet improves performance and herbivore resistance of a parasitic plant. Ecology 79: Marvier MA. 1998b. Parasite impacts on host communities: Plant parasitism in a California coastal prairie. Ecology 79: Mathiasen RL, Hawksworth FG, Edminster CB Effects of dwarf mistletoe on growth and mortality of douglas-fir in the southwest. Great Basin Newsletter 50: Matthies D Parasitic and competitive interactions between the hemiparasites Rhinanthus serotinus and Odontites rubra and their host Medicago sativa. Journal of Ecology 83: Matthies D Interactions between the root hemiparasite Melampyrum arvense and mixtures of host plants: Heterotrophic benefit and parasitemediated competition. Oikos 75: Matthies D Parasite host interaction in Castilleja and Orthocarpus. Canadian Journal of Botany 75: Matthies D, Egli P Response of a root hemiparasite to elevated CO 2 depends on host type and soil nutrients. Oecologia 120: Matvienko M, Torres MJ, Yoder JI Transcriptional responses in the hemiparasitic plant Triphysaria versicolor to host plant signals. Plant Physiology 127: Mead EW, Looker M, Gardner DR, Stermitz FR Pyrrolizidine alkaloids of Liatris punctata and its root parasite, Castilleja intergra. Phytochemistry 31: Mead EW, Stermitz FR Content of iridoid glycosides in different parts of. Castilleja Integra Phytochemistry 32: Medel R Assessment of parasite-mediated selection in a host-parasite system in plants. Ecology 81: Medel R, Vergara E, Silva A, Kalin-Arroya M Effects of vector behavior and host resistance on mistletoe aggregation. Ecology 85: Meinzer FC, Woodruff DR, Shaw DC Integrated responses of hydraulic architecture, water and carbon relations of western hemlock to dwarf mistletoe infection. Plant, Cell and Environment 27: Midgley JJ, Cowling RM, Hendricks H, Desmet PG, Esler K, Rundel P Population ecology of tree succulents (Aloe and Pachypodium) in the New Phytologist (2005) New Phytologist (2005) 166:

14 750 Review arid western Cape: Decline of keystone species. Biodiversity and Conservation 6: Miller AC, Watling JR, Overton IC, Sinclair R Does water status of Eucalyptus largiflorens (Myrtaceae) affect infection by the mistletoe Amyema miquelii (Loranthaceae)? Functional Plant Biology 30: Mitchell EAD, Buttler A, Grosvernier P, Rydin H, Siegenthaler A, Gobat JM Contrasted effects of increased N and CO 2 supply on two keystone species in peatland restoration and implications for global change. Journal of Ecology 90: Molau U The genus Bartsia (Scrophulariaceae, Rhinanthoideae). Opera Botanica 102: Musselman LJ, Dickison WC The structure and development of haustorium in parasitic Scorphulariaceae. Botanical Journal of the Linnean Society 70: Musselman LJ, Mann WF, Jr Root Parasites of Southern Forests. USDA Forest Service, general technical report, SO-20. New Orleans, USA: USDA. Musselman LJ, Press MC Introduction to parasitic plants. In: Press, MC, Graves, JD, eds. Parasitic Plants. London, UK: Chapman & Hall, Narasimha VL, Rabindranath V A further contribution to the host range of Dendrophthoe falcate (L.f.) Ettingsh. Bulletin of the Botanical Survey of India 6: 103. Narayanasamy C, Sampathkumar R Host parasite relationships of Dendrophthoe falcata (Linn. f.) Bettingh. (Loranthus longiflorus Desr.). Journal of the Bombay Natural History Society 78: Nickrent DL, Duff RJ, Colwell AE et al Molecular phylogenetic and evolutionary studies of parasitic plants. In: Soltis, DE, Soltis, PS, Doyle, JJ, eds. Molecular Systematics of Plants II DNA Sequencing. Boston, USA: Kluwer Academic, Nilsson CH, Svensson BM Host affiliation in two subarctic hemiparasitic plants: Bartsia alpine and Pedicularis lapponica. Ecoscience 4: Norton DA, Carpenter MA Mistletoes as parasites: host specificity and speciation. Trends in Ecology and Evolution 13: van Ommeren RJ, Whitham TG Changes in the interactions between juniper and mistletoe mediated by shared avian frugivores: parasitism to potential mutualism. Oecologia 130: Paine RT A note on trophic complexity and community stability. American Naturalist 103: Parker C, Riches CR Parasitic Weeds of the World: Biology and Control. Wallingford, UK: CAB International. Pate JS Mineral relationships of parasites and their hosts. In: Press, MC, Graves, JD, eds. Parasitic Plants. London, UK: Chapman & Hall, Pate JS, Davidson NJ, Kuo J, Milburn JA. 1990a. Water relations of the root hemiparasite Olax phyllanthi (Labill) R.Br. (Olacaceae) and its multiple hosts. Oecologia 84: Pate JS, Pate SR, Kuo J, Davidson NJ. 1990b. Growth, Resource Allocation and Haustorial Biology of the Root Hemiparasite Olax phyllanthi (Olacaceae). Annals of Botany 65: Patiño S, Aalto T, Edwards AA, Grace J Is Rafflesia an endothermic flower? New Phytologist 154: Patiño S, Grace J, Banziger H Endothermy by flowers of Rhizanthes lowii (Rafflesiaceae). Oecologia 124: Pennings SC, Callaway RM Salt-marsh plant zonation the relative importance of competition and physical factors. Ecology 73: Pennings SC, Callaway RM Impact of a parasitic plant on the structure and dynamics of salt marsh vegetation. Ecology 77: Pennings SC, Callaway RM Parasitic plants: Parallels and contrasts with herbivores. Oecologia 131: Petney TN, Andrews RH Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28: Phoenix GK, Press MC Linking physiological traits to impacts on community structure and function: the role of root hemiparasitic Orobanchaceae (ex-scrophulariaceae). Journal of Ecology 93: Power ME Floods, food chains, and ecosystem processes in rivers. In: Jones, CG, Lawton, JH, eds. Linking Species and Ecosystems. New York, USA: Chapman & Hall, Prati D, Matthies D, Schmid B Reciprocal parasitization in Rhinanthus serotinus: a model system of physiological integration in clonal plants. Oikos 78: Press MC Dracula or Robin Hood? A functional role for root hemiparasites in nutrient poor ecosystems. Oikos 82: Press MC, Graves J, eds Parasitic Plants. London, UK: Chapman & Hall. Press MC, Nour JJ, Bebawi FF, Stewart GR Antitranspirant induced heat stress in the parasitic plant Striga hermonthica a novel method of control. Journal of Experimental Botany 40: Press MC, Scholes JD, Watling JR Parasitic plants: physiological and ecological interactions with their hosts. In: Press, MC, Scholes, JD, Barker, MG, eds. Physiological Plant Ecology. Oxford, UK: Blackwell Science, Puustinen S, Jarvinen O, Tiilikkala K Asymmetric competition between a hemiparasitic plant and a cyst nematode on a shared host plant. Ecoscience 8: Puustinen S, Mutikainen P Host parasite herbivore interactions: Implications of host cyanogenesis. Ecology 82: Quested HM, Press MC, Callaghan TV, Cornelissen JHC The hemiparasitic angiosperm Bartsia alpina has the potential to accelerate decomposition in sub-arctic communities. Oecologia 130: Quested HM, Cornelissen JHC, Press MC, Callaghan TV, Aerts R, Trosien F, Riemann P, Gwynn-Jones D, Kondratchuk A, Jonasson SE. 2003a. Decomposition of sub-arctic plants with differing nitrogen economies: a functional role for hemiparasites. Ecology 84: Quested HM, Press MC, Callaghan TV. 2003b. Litter of the hemiparasite Bartsia alpina enhances plant growth: evidence for a functional role in nutrient cycling. Oecologia 135: Quested HM, Callaghan TV, Cornelissen JHC, Press MC The impact of hemiparasitic plant litter on decomposition: direct, seasonal and litter mixing effects. Journal of Ecology 93: Radomiljac AM, McComb JA, Pate JS Gas exchange and water relations of the root hemi-parasite Santalum album L. in association with legume and non-legume hosts. Annals of Botany 83: Reid N, Smith NM, Yan Z Ecology and population biology of mistletoes. In: Lowman, MD, Nadkarni, NM, eds. Forest Canopies. San Diego, USA: Academic Press, Restrepo C, Sargent S, Levey DJ, Watson DM The role of vertebrates in the diversification of New World mistletoes. In: Levey, DJ, Silva, WR, Galetti, M, eds. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. Oxford, UK: CAB International, Robertson AW, Kelly D, Ladley JJ, Sparrow AD Effects of pollinator loss on endemic New Zealand mistletoes (Loranthaceae). Conservation Biology 13: Sala A, Carey EV, Callaway RM Dwarf mistletoe affects whole-tree water relations of Douglas fir and western larch primarily through changes in leaf to sapwood ratios. Oecologia 126: Salonen V, Puustinen S Success of a root hemiparasitic plant is influenced by soil quality and by defoliation of its host. Ecology 77: Salonen V, Setala H, Puustinen S The interplay between Pinus sylvestris, its root hemiparasite, Melampyrum pratense, and ectomycorrhizal fungi: Influences on plant growth and reproduction. Ecoscience 7: Schneider MJ, Stermitz FR Uptake of host plant alkaloids by root parasitic Pedicularis species. Phytochemistry 29: Schulze ED, Ehleringer JR The effect of nitrogen supply on growth New Phytologist (2005) 166: New Phytologist (2005)

15 Review 751 and water-use efficiency of xylem-tapping mistletoes. Planta 162: Seel WE, Parsons AN, Press MC Do inorganic solutes limit growth of the facultative hemiparasitic Rhinanthus minor L. in the absence of a host? New Phytologist 124: Seel WE, Press MC Influence of the host on three sub-arctic annual facultative root hemiparasites. New Phytologist 125: Seel WE, Press MC Effects of repeated parasitism by Rhinanthus minor on the growth and photosynthesis of a perennial grass, Poa alpina. New Phytologist 134: Silva A, Martínez del Rio C Effects of the mistletoe Tristerix aphyllus (Loranthaceae) on the reproduction of its cactus host Echinopsis chilensis. Oikos 75: Smith D The population dynamics and community ecology of root hemiparasitic plants. American Naturalist 155: Snyder MA, Fineschi B, Linhart YB, Smith RH Multivariate discrimination of host use by dwarf mistletoe Arceuthobium vaginatum subsp cryptopodum: Inter- and intraspecific comparisons. Journal of Chemical Ecology 22: Stermitz FR, Belofsky GN, Ng D, Singer MC Quinolizidine alkaloids obtained by Pedicularis semibarbata (Scrophulariaceae) from Lupinus fulcratus (Leguminosae) fail to influence the specialist herbivore Euphydryas editha (Lepidoptera). Journal of Chemical Ecology 15: Stewart GR, Press MC The physiology and biochemistry of parasitic angiosperms. Annual Review of Plant Physiology and Plant Molecular Biology 41: Stiles FG, Freeman CE Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25: Tennakoon KU, Pate JS Effects of parasitism by a mistletoe on the structure and functioning of branches of its host. Plant, Cell & Environment 19: Tilman D Mechanisms of plant competition. In: Crawley, MJ, ed. Plant Ecology, 2nd edn. Oxford, UK: Blackwell Science Ltd Tomilov A, Tomilova N, Yoder JI In vitro haustorium development in roots and root cultures of the hemiparasitic plant Triphysaria versicolor. Plant Cell Tissue and Organ Culture 77: Veenendaal EM, Abebrese IK, Walsh MF, Swaine MD Root hemiparasitism in a West African rainforest tree Okoubaka aubrevillei (Santalaceae). New Phytologist 134: Wanner J, Tinnin RO Respiration in lodgepole pine parasitized by American dwarf mistletoe. Canadian Journal of Forest Research 16: Wardle DA Communities and Ecosystems Linking the Aboveground and Belowground Components. Princeton, NJ, USA: Princeton University Press. Watling JR, Press MC Impacts of infection by parasitic angiosperms on host photosynthesis. Plant Biology 3: Watson DM Mistletoe A keystone resource in forests and woodlands worldwide. Annual Review of Ecology and Systematics 32: Werth CR, Riopel JL A study of the host range of Aureolaria pedicularia (L.) Raf. (Scrophulariaceae). American Midland Naturalist 102: Westbury DB Biological Flora of the British Isles. Rhinanthus minor L. Journal of Ecology 92: Westbury DB, Dunnett NP The effects of the presence of Rhinanthus minor on the composition and productivity of created swards on ex-arable land. Aspects of Applied Biology 58: About New Phytologist New Phytologist is owned by a non-profit-making charitable trust dedicated to the promotion of plant science, facilitating projects from symposia to open access for our s. Complete information is available at Regular papers, Letters, Research reviews, Rapid reports and Methods papers are encouraged. We are committed to rapid processing, from online submission through to publication as-ready via OnlineEarly the 2003 average submission to decision time was just 35 days. Online-only colour is free, and essential print colour costs will be met if necessary. We also provide 25 offprints as well as a PDF for each article. For online summaries and ToC alerts, go to the website and click on Journal online. You can take out a personal subscription to the journal for a fraction of the institutional price. Rates start at 109 in Europe/$202 in the USA & Canada for the online edition (click on Subscribe at the website). If you have any questions, do get in touch with Central Office (newphytol@lancaster.ac.uk; tel ) or, for a local contact in North America, the USA Office (newphytol@ornl.gov; tel ). New Phytologist (2005) New Phytologist (2005) 166: