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Review
Blackwell Publishing, Ltd.
Tansley review
Impacts of parasitic plants on natural
communities
Author for correspondence:
Malcolm C. Press
Tel: +44 (0)114 222 4111
Fax: +44 (0)114 222 0002
Email: [email protected]
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
Impacts of parasitic plants on the plant community
739
IV.
V.
Impacts of the plant community on parasite
populations
741
Impacts of the parasite on other trophic levels
742
VII. Impacts of the parasite on the abiotic environment
747
VIII. Concluding remarks
748
VI.
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
CO2 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: 737–751
© New Phytologist (2005) doi: 10.1111/j.1469-8137.2005.01358.x
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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 (∼3–
4000) 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 CO2 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
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Tansley review
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:
© New Phytologist (2005) www.newphytologist.org
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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 m2 (Kelly,
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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, Nrich 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
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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.
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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
Tansley review
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
Review
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
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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 CO2 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
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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
Review
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
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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
Tansley review
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
Review
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
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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 CO2 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.
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