MASARYK UNIVERSITY
FACULTY OF SCIENCE
DEPARTMENT OF BOTANY AND ZOOLOGY
ECOLOGY OF (HEMI)PARASITIC PLANTS
Habilitation Thesis
Jakub Těšitel
Brno 2017
Abstrakt
Tato habilitační práce se věnuje ekologii parazitických a poloparazitických
rostlin. V její první části probírám evoluční ekologii rostlinného parazitismu. Druhů
část je zaměřena na ekologii kořenových poloparazitů, které jsou spolu se jmelími
největší funkční skupinou parazitických rostlin. Jejich ekologii představuji z mnoha
pohledů, od ekofyziologických mechanismů interakce mezi hostitelem a
poloparazitem, přes aspekty ekologie společenstev a ekosystémové ekologie, po
využití poloparazitů v ekologických aplikacích. Součástí habilitační práce je 10
vědeckých článků, které přispěly k rozvoji poznání ekologie (polo)parazitických
rostlin.
Abstract
This thesis deals with the ecology of parasitic and hemiparasitic plants. In its
first part, I introduce the evolutionary ecology of plant parasitism. The second part
focuses on ecology of root hemiparasites, together with mistletoes the largest
functional groups of parasitic plants. I adopt a comprehensive view on their ecology
ranging from the ecophysiological mechanisms of the hemiparasite-host interaction
to community and ecosystem ecology, including also applications of roothemiparasites
in ecological restoration. The thesis is supplemented by 10 research
papers which contributed to understanding (hemi)parasitic plant ecology and
evolution.
Acknowledgement
I would like to thank all colleagues who helped with the research presented in
this thesis. In particular, Jan Lepš, Pavel Fibich and Milan Chytrý greatly
contributed to the papers dealing with vegetation ecology of root-hemiparasitic
plants. Jan Mládek and Ondřej Mudrák cooperated with me on the ecological
applications of hemiparasites. Petra Světlíková, my Ph.D. student has been keen on
continuing my ecophysiological research, one piece of which is also presented here.
I am grateful for the friendly and inspiring atmosphere at the Deparment of Botany
in České Budějovice, where most of my research work was done, as well for the
recent warm welcome at the Department of Botany and Zoology of Masaryk
University in Brno, where this thesis was completed.
I would also like to thank my family for their support. My wife Tamara
substantially contributed to the research presented here. As a very organized
person, her contribution to research planning and management was indeed crucial
due to rather messy nature of my attitude to life. She was also very patient with me
during the time of the thesis completion, despite the need to take care of our
daughters, garden work and many other duties. My daughters Dorotka and
Markétka have contributed an infinite amount of fun to my life, which is greatly
acknowledged.
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Content
1. Story of losers or winners? Evolutionary ecology of parasitic plants.................. 2
2. Ecology of root-hemiparasitic plants ................................................................. 12
2.1. Introduction to root hemiparasites...................................................................... 12
2.2. Ecophysiological mechanisms of the hemiparasite-host interaction.................. 13
2.3. Ecology of the hemiparasite-host interaction..................................................... 16
2.4. Community and ecosystem ecology of parasitic plants ..................................... 21
2.5. Applications of root hemiparasites in ecological restoration............................. 25
2.6. Future perspectives............................................................................................. 28
3. References .......................................................................................................... 30
4. List of papers...................................................................................................... 47
2
1. Story of losers or winners? Evolutionary ecology of parasitic plants
Most plants are photoautotrophic organisms. Their vital processes depend on carbon from CO2,
energy from light and also water and mineral nutrients. While availability of CO2 in the air is
rarely limiting and can be considered as a condition for plant life, the other three factors are
resources available in limited supply. Therefore, they are subject of competition between cooccurring
plants. Plants have evolved a number of strategies to facilitate acquisition of these
resources. Some of them involve ecological interactions with other organisms. Of these,
mutualistic mycorrhizal associations with fungi contributing mineral nutrients in exchange for
organic carbon are most common in vascular plants. In fact, most plant species do establish
mycorrhizal association, a symbiosis which is likely to have facilitated land colonization by
plants (Smith & Read, 2008). Several evolutionary lineages of vascular plants (including e.g.
Fabaceae, Cycadales, and a number of Fagales) developed mutualistic symbiosis with
(cyano)bacteria, which have ability to fix nitrogen, one of the principal biogenic elements, from
the atmosphere (Stevens, 2001; Li et al., 2015). While the strategies mentioned above involve
bidirectional exchange of resources, others involve exclusively flows of resources towards plant
recipients, i.e. they are purely heterotrophic. Mycoheterotrophy refers to the cases where the
balance of the originally mutualistic symbiosis shifted towards the benefit of the plant partner
(Merckx, 2013). While most mycoheterotrophs retain photosynthetic ability (partial
mycoheterotrophs), several evolutionary lineages are non-green and their carbon nutrition is
completely dependent on fungal partner (Selosse & Roy, 2009). Another example includes
carnivorous plants which trap and digest animal prey to acquire mineral nutrients, in particular
nitrogen (Givnish, 2015). Plant parasitism defined as direct parasitic interaction between plant
individuals represents one of the heterotrophic resource-acquisition strategies which contributes
not only mineral nutrients but also water and variable amount of organic carbon.
The mechanism of plant parasitism is based on connection between vascular bundles of
two plant species – the parasite and the host. This connection is established by a specialized
organ called the haustorium which is developed as a modification of roots or stems of parasitic
plants. Parasitic plants comprise ca. 4500 species, which accounts for 1% of angiosperms
(Těšitel, 2016). Parasitism has evolved at least 12 times independently in the angiosperm
evolution (Barkman et al., 2007; Naumann et al., 2013). Species diversity is distributed very
unevenly among individual evolutionary lineages of parasitic angiosperms. Two largest groups,
the Orobanchaceae family and the Santalales order comprise ca. 90% of parasitic species while
multiple groups (Hydnoraceae, Mitrastemonaceae, Cynomoriaceae and Lennooidae) contain
3
less than 10 species (Těšitel, 2016). Individual lineages markedly differ also in their estimated
phylogenetic age. Santalales are the oldest lineage of extant parasitic plants, origin of which is
estimated to early Cretaceous ca. 110 Mya (Naumann et al., 2013). By contrast, the youngest
transitions to the parasitic strategy were reconstructed in the family Orobanchaceae and the
parasitic genus Cuscuta of Convolvulaceae. These groups are of late Paleogene age (32 and 35
Mya, respectively) which also indicates the upper boundary of the age of transition to parasitism
(Naumann et al., 2013). The uneven species richness of individual parasitic plant lineages was
recently related with their phylogenetic age to show that there is little correlation between the
two parameters and the non-parasitic sister clades are mostly more species rich than the parasitic
lineages (Hardy & Cook, 2012; Naumann et al., 2013). Such pattern would indicate a strongly
limited evolutionary potential of parasitic plants, a hypothesis suggested by Hardy & Cook
(2012) on the basis of sister-clade comparisons of parasitic and mycoheterotrophic plants.
Notable exceptions to this are however the two largest parasitic lineages of Santalales and
Orobanchaceae, species richness of which is higher than that of their respective non-parasitic
sister clades by several orders of magnitude (Hardy & Cook, 2012). Naumann et al. (2013)
postulated an alternative temporal specialization hypothesis (TSH) explaining the evolution of
parasitic plants through an assumption that efficiency of parasitic pathways increases in time
together with host specificity. This should produce multiple small, specialized and relict groups
of highly specialized parasites together with few relatively young, non-specialized and
diversified groups. This hypothesis generally seems to fit well with the empirical evidence on
phylogenetic age, trophic specialization and species richness of the parasitic angiosperm
lineages (Naumann et al., 2013); however there is one important exception. Santalales are the
oldest and simultaneously most species-rich group of extant parasitic plants. They display a
range of trophic modes ranging from non-parasitic to full heterotrophy (Naumann et al., 2013;
Těšitel, 2016) with predominance of photosynthetic hemiparasites. This was also
acknowledged by Naumann et al. (2013) who however tried to incorporate existence of
Santalales into their hypothesis by pointing on existence of small specialized groups within the
clade. In contrast to these previous studies investigating exclusively the evolutionary patterns,
I am convinced that the complex evolutionary pattern of parasitic angiosperms may only be
understood through examination of the extensive functional diversity relating to their
physiology (dependence on host species, ability to withdraw resources), life forms, ecological
interactions and also geographical distribution.
4
The physiological functioning of individual parasitic plant species can be described by
a set of functional traits (Těšitel, 2016). Ability of photosynthesis indicates autonomy in carbon
acquisition and varies from fully functional to completely missing photosynthesis. Closely
associated with photosynthetic ability is the anatomical structure of the host-parasite contact in
the haustoria. Some parasites access host xylem only while others take up resources from both
xylem and phloem (Hibberd & Jeschke, 2001). Non-photosynthetic species mostly access both
types of vascular bundles due to the need of abundant carbon nutrition provided by phloem
(Irving & Cameron, 2009); however, this is not a strict rule due to existence of xylem-only
feeding holoparasitic plants (Těšitel & Tesařová, 2013; Světlíková et al., 2015; Těšitel, 2016).
Other important traits relate to germination, which may be either induced by host presence or
not, and establishment of the initial connection to the host by primary (terminal) haustoria or
secondary (lateral) haustoria. Location of haustoria on roots or stems of the host determine life
forms of parasitic plants, that is root or stem-parasites. The most advanced parasitic species
however form extensive endophytic structures which may extend from root to shoot (HeideJørgensen,
2008). As a result, the distinction between root and stem parasites is not relevant in
their case. Four functional groups of parasitic plants may thus be distinguished in the basis of
the functional traits mentioned above – root-hemiparasites, root-holoparasites, stem parasites
and endophytic parasites (Těšitel, 2016).
These functional groups make sense from morphological, physiological and ontogenetic
points of view. However differences between some of them lack distinctness from the
perspective of ecological interactions, resource acquisition and use. For instance, there is little
difference in the ecological interactions between root-holoparasites and endophytic parasites
since both are (typically) completely dependent on host for carbon and do not compete with the
host for light. Therefore, I introduce here a scheme displaying major adaptive evolutionary steps
which can be traced in the parasitic plants evolution (Fig. 1). Each of the steps involves an
evolutionary innovation addressing a major ecological constraint limiting
occurrence/abundance of its predecessors which did not display such innovation.
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Fig. 1. Scheme of the evolution of parasitism in the angiosperms. Major evolutionary innovations
facilitating parasitic resource acquisition are indicated by arrows. Rectangles encapsulate principal
evolutionary steps which comprise plants differing in their physiological functioning, resource
acquisition strategies and ecological interactions. Major ecological constraints overcome (i.e.
advantages) and associated with respective evolutionary steps are provided together with the number of
species and estimate of predominant host specificity. Illustration of photosynthetic ability refers to the
state of a majority of species; some important exceptions, e.g. non-photosynthetic Lathraea in C are
commented in the text. Note, that phloem continuity in the haustoria may be difficult to demonstrate in
some less-well studied groups (Cynomoriaceae, Mirrastemonaceae, Hydnoraceae); as a result, their
placement in C or D is not resolved to date.
Development of xylem connection to the host represents the first step in the evolution
of plant parasitism (Fig. 1A). This provides access to the xylem-borne resources, namely
mineral nutrients, water and also a limited amount of carbon (Hibberd & Jeschke, 2001; Irving
& Cameron, 2009; Těšitel et al., 2010a; Jiang et al., 2010; Bell & Adams, 2011). This roothemiparasitic
strategy is characteristic of most Orbanchaceae, Krameriaceae and a substantial
part of Santales. Access to host xylem largely facilitates mineral nutrition of the parasitic plants
6
providing a great competitive advantage over non-parasitic species. This competitive advantage
is however realized through own photosynthetic activity, rate of which is strongly increased by
nutrients obtained heterotrophically (Těšitel et al., 2015b). Therefore, the parasitic plants which
display only this initial albeit crucial evolutionary innovation retain photosynthetic activity
mostly in a fully functional state. As a result of this dependency on own photosynthesis, they
are affected by competition for light from both the host species and other co-occurring species
in the community. In fact, competition for light is the principal constraint limiting their
performance (Fig. 1A; Matthies, 1995; Fibich et al. 2010; Těšitel et al., 2011, 2013).
To address this constraint, some of these parasitic plants (hemiparasitic Santalales)
evolved epiphytic mistletoe life form. Others (genus Cassytha of Lauraceae; also Cuscuta of
Convolvulaceae, all extant species of which access host phloem) underwent the transition to
parasitic xylem-feeding strategy from autotrophic epiphytic vine life forms. Either evolutionary
pathway resulted in a photosynthetic xylem-feeding epiphyte (Fig. 1B), which addresses much
of the constraint imposed by competition for light. Occurrence of such parasitic plants is
however dependent on availability of suitable host species which are large and long-living
enough to support the epiphytes. Dispersal is another important issue for mistletoes germinating
on host branches (Mathiasen et al., 2008). By contrast Cassytha germinates on the ground
which however means that competition for light can still affect its establishment.
The effects of competition for light have most detrimental effects on the seedlings of
the root-hemiparasitic plants (Fig. 1A; Těšitel et al. 2011) restricting their regeneration niche
(Grubb, 1977). To address the seedling establishment constraint, multiple species evolved
initiation of seed germination by presence of host root associated with a holoparasitic-seedling
stage (Fig. 1C). Such strategy, intermediate between hemi- and holo- parasitism (Westwood et
al., 2010), is typical for a number of genera of Orobanchaceae, namely Striga, Alectra, Tozzia
and perennial species of Rhynchocorys. The xylem-only connection to the host provides only a
limited amount of carbon, which requires a transition to own photosynthesis either early in the
subsequent ontogeny (Striga, Alectra) or a slow-growing, long-lasting underground non-green
stage (Tozzia, Rhynchocorys). Most of these plants still produce green shoots which allow
transformation of their mineral-nutrition benefits into offspring production by photosynthesis.
The importance of the autotrophic pathway for generative-reproduction organs has indeed been
demonstrated directly in Striga (Santos-Izquierdo et al., 2008) or may be indirectly deduced
from green shoots which are always fertile in Tozzia and Rhynchocorys (Těšitel et al., 2010b).
The evolutionary stability of their photosynthetic activity (albeit frequently lowered; Graves et
7
al., 1992) is thus secured by a reduction of fitness in eventual non-green mutants. Still, xylem
only-feeding species of the genus Lathraea growing in closed-canopy forest lost photosynthesis
probably as a result of minimal contribution of own photosythesis in the shady environment
and lack of necessity to quickly complete its life cycle in a stable environment with plentiful
resources contributed by long-living hosts. Moreover, the long-living xylem only-feeding
holoparasite stage relies for carbon nutrition of xylem sap with low concentration of carbon.
Sufficient carbon can be obtained only together with excessive amount of water, which cannot
be discarded by transpiration. These species therefore feature specialized hydathode trichomes
on scales of leaf origin covering their rhizomes, which actively excrete excess water (Ziegler,
1955; Renaudin & Garrigues, 1967; Weber, 1975; Těšitel & Tesařová, 2013; Světlíková et al.,
2015). This active process requires energy, which further decreases physiological efficiency of
these parasitic plants.
The constraints related to carbon nutrition in xylem-only feeding hemiparasites, i.e.
sensitivity to competition for light or the need for highly specialized and inefficient physiology,
were addressed by the evolution of connection to host phloem in the haustoria (Fig. 1D).
Phloem sap is rich in organic carbon providing sufficient nutrition to support both growth and
reproduction of phloem feeding parasites which become practically independent of light
conditions. None of the phloem-feeding parasitic plants displays functional photosynthesis
which would contribute substantial proportion of its carbon budget. This indicates that
photosynthetic ability is quickly lost after evolution of phloem connection due to genetic drift
acting upon plastid genome devastating functionality of genes involved in synthesis of
photosynthetic apparatus (Wicke et al., 2013). While plastid genome itself is retained in most
phloem feeding non-green species, recent research discovered that it may be eventually lost
(Molina et al., 2014). Most of the phloem-feeding holoparasitic lineages indeed lost the ability
to photosynthesis in its entirety (Balanophoraceae, Cytinaceae, Cytinaceae, Lenooidae, most
holoparasitic Orobanchaceae). By contrast, some species retain rudimentary photosynthetic
ability. This is the case of the genus Cuscuta, where most species retain photosynthesis
contributing to lipid synthesis which is crucial for offspring production as lipids constitute the
seed reserves but their concentration in host phloem sap is low (McNeal et al., 2007). The
photosynthetic activity may also facilitate foraging for the host in the pre-attachment phase of
Cuscuta seedlings (Švubová et al., 2013). Similarly, in dwarf mistletoes (genus Arceuthobium
of Viscaceae, Santalales), rudimentary photosynthesis may play role in seed production (Miller
& Tocher, 1975) and establishment on host branches may be greatly facilitated by energy
8
coming from photosynthesis of green endosperm present in all mistletoes (Heide-Jørgensen,
2008; Nickrent & García, 2009).
The efficient carbon nutrition allowed phloem-feeding parasites to colonize and thrive
in habitats with conditions unfavourable for autotrophic plant life or largely exploitative,
resource-wasting hemiparasitic strategy. These include e.g. dark forest understory or arid
places, where holoparasitic phloem-feeding plants indeed frequently occur (Těšitel, 2016)..
Given the efficiency of carbon nutrition by phloem feeding, an apparent question also arises:
why did not all parasitic plants evolve this nutritional mode to avoid constraints imposed by
competition for light? It seems that establishment of phloem contact is much more complicated
compared to xylem contact – phloem is a living tissue and at least certain level of specific
interaction with the host to facilitate transfer of the resources from host phloem to the parasite
(Irving & Cameron, 2009). The higher specialization of phloem-feeding compared to xylem
only-feeding haustoria implies also greater hosts specificity. This means that most of the
phloem-feeding parasites are limited by host availability, which rarely limits distribution of
xylem-feeding hemiparasites (in particular root-hemiparasites). Exemplified by the case of
Orobanchaceae, horizontal gene transfer between host and parasite (which was documented in
multiple phloem-feeding lineages; (Davis & Xi, 2015) has recently been suggested to play an
important role in the evolution of phloem-feeding ability (Yang et al., 2016). However,
horizontal gene transfers are still rather rare events; obtaining the set of genes necessary for
phloem-contact establishment may thus require substantial amount of time even on the
evolutionary time scale. The evolution towards greater efficiency of heterotrophic carbon
acquisition may moreover be hindered by the contrast between the hemiparasitic and
holoparasitic strategies. Despite variable gain of host-derived carbon in the hemiparasites
(Těšitel et al., 2010a; Bell & Adams, 2011), they capitalize the benefits of their parasitism via
own photosynthesis (Těšitel et al., 2015b). Switching to holoparasitism means that the principal
benefits of hemiparasitism, i.e. low-cost yet abundant mineral nutrition and water supply, are
lost as holoparasites cannot benefit from their elevated availability.
Looking back to the evolutionary pattern of parasitic angiosperms, what can be
concluded about the theories aiming at its explanation by the hypotheses on ecological
limitation of parasitic plant diversification (Hardy & Cook, 2012) or temporal specialization
(Naumann et al., 2013)? Both of these hypotheses have a structure of universal laws of nature,
which are however exercised on the evolutionary history. Such approach has been demonstrated
inadequate from the philosophical perspective (Popper, 1957; Taleb, 2007). Moreover, both of
9
these hypotheses are refuted by data available, most notably by the existence Santalales, a
species-rich group containing mostly relatively non-specialized root- or stem-hemiparasitic
plants (Těšitel, 2016). If the two proposed hypotheses are wrong and universal theory
describing the evolution of plant parasitism is impossible, what can I offer instead? I propose
an interpretation of the evolutionary pathways of individual parasitic plant lineages and their
similarities.
Clearly, we can identify a number of small and functionally homogeneous lineages in
the parasitic plants on the one hand and two highly successful species-rich and a functionally
diverse groups on the other. This contrast will further increase when we consider their
geographic distributions. The small holoparasitic lineages typically have a limited geographic
distribution. The geographic ranges of Cytinaceae, Apodanthaceae and Mitrastemonaceae are
also disjunct (Heide-Jørgensen, 2008), which indeed indicates their relict origin. By contrast,
the two most successful lineages, Santalales and Orobanchaceae, have global distributions,
which also applies for the genus Cuscuta (Heide-Jørgensen, 2008). These three groups represent
an omnipresent component of principal terrestrial ecosystems worldwide. Root-hemiparasitic
Santalales have been successful in both tropical woody and open temperate vegetation (Fig.
2A) , while Loranthaceae and Viscaceae, two independently evolved mistletoe lineages within
the order (Nickrent et al., 2010), colonized predominantly forest, savanna and other woody
vegetation from the tropics to the temperate (Fig. 2B; Heide-Jørgensen, 2008). Root-parasitic
Orobanchaceae have been highly successful in the open vegetation and diversified in both
temperate and tropical grassland biomes (Fig. 2C,D; McNeal et al., 2013). Hemiparasitic
species of both Santalales and Orobanchaceae are moreover recognized as keystone species
with profound effects on the communities and ecosystems, where they occur (Press, 1998;
Watson, 2001, 2009, 2016; Phoenix & Press, 2004). Similarly, the genus Cuscuta has a global
geographic distribution and its species were demonstrated to play a keystone role in structuring
plant communities (Callaway & Pennings, 1996, 1998). Considering the other groups, species
10
of the genus Cassytha are mostly restricted to Australia but C. filiformis has a remarkable
pantropic distribution (Heide-Jørgensen, 2008). In their Australian homeland, the Cassytha
Fig. 2. Parasitic plants as vegetation dominants. A: Santalum acuminatum shrubs in Western
Australian bush; B: Viscum album mistletoes parasitizing Populus nigra in floodplain forests, South
Moravia; C: Rhinanthus major dominating a mesic meadow in Transsilvania; D: Odontites vernus
dominance in a floodplain meadow in the regrowth stand after summer cut; E: Cassytha sp. in
Western Australian bush; F: Cuscuta sp. (presumably C. epithymum) forming a dominance patch
on a lowland meadow in Austrian part of Pannonia, note hyperparasitism on Rhinanthus major.
11
species may attain dominance in the communities (Fig. 2E) and recently have even been
demonstrated to strongly suppress growth of leguminous invasive species (Prider et al., 2009;
Shen et al., 2010). The parasitic-plant strategies which seem successful are thus rather diverse.
Their success may be related to the history of global ecosystem and biota, i.e. the host
environment. For instance, the evolution and radiation of Orobanchaceae coincides with the
expansion of the grassland biome in the late Tertiary (Strömberg, 2011; Naumann et al., 2013).
The evolution and diversification of mistletoe life forms followed expansion of angiospermdominated
forests in the late Cretaceous (Wang et al., 2009). Loranthaceae mistletoes
originated and radiated in the Oligocene following the expansion of savanna, their primary
habitat at present (Vidal-Russell & Nickrent, 2008). The evolutionary success of Cuscuta may
lay in the fact that most of the species of this genus are able to parasitize a wide range of hosts
(Baráth & Csiky, 2012), which is otherwise rare among phloem-feeding parasites. This could
possibly have been facilitated by the Cuscuta vine life form allowing interactions with many
potential host species simultaneously (Fig. 2F) with possible repeated trials to attack also those
hosts which were originally incompatible. Such situation may have triggered the evolution of a
generalist phloem-feeding parasite. In summary, many different parasitic strategies underlie the
success of individual parasitic plants. The lack of a universal hypothesis explaining the
evolutionary pattern should not prevent us from acknowledging the evolutionary success and
ecological roles of these successful groups of parasitic plants as well as extraordinary
morphological and functional variability recognized in the whole functional group of parasitic
plants.
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2. Ecology of root-hemiparasitic plants
2.1. Introduction to root hemiparasites
Root-hemiparasitic plants are green photosynthetic plants which attack roots of other plants to
withdraw resources of their xylem (Section 1; Irving & Cameron, 2009; Těšitel, 2016). To
uptake the host resources they use a specialized organ, the haustorium which, in their case, is a
modified root. Root hemiparasites comprise ca 2400 species (more than 50% of all parasitic
plants, ca 0.5% of angiosperms) of three independent evolutionary lineages: Santalales,
Orobanchaceae and Krameriaceae. Of these, the first two contain most of the diversity while
Krameriaceae consist of a single genus with 18 species.
Extensive morphological diversity exists in root-hemiparasites ranging from tiny annual
Euphrasia species occurring in alpine grasslands to large tropical forest trees with Okoubaka
aubrevillei of Santalales, their largest representative, reaching up to 40 m high (Veenendaal et
al., 1996). Root hemiparasites are a functional group distributed globally on all continents
except the Antarctic and occurring in all major terrestrial habitats (Heide-Jørgensen, 2008).
Most species however occur in open habitats such as temperate grasslands, alpine vegetation
and (semi)arid vegetation (Těšitel, 2016).
Root hemiparasites have been demonstrated to substantially affect structure of plant
communities and ecosystem processes (Press, 1998; Press & Phoenix, 2005; Watson, 2009)
together with other parasitic plant groups, the mistletoes (Watson, 2001) and parasitic vines
(Callaway & Pennings, 1996). Some species (e.g. Rhinanthus spp.) are recognized for their
ecosystem engineering capacity which may increase community diversity (Pywell et al., 2004;
Těšitel et al., 2017) while others (e.g. Striga spp.) are recognized as serious weeds threatening
the production of agriculture (Pennisi, 2010; Parker, 2013).
In this text, I first aim to introduce the physiological and ecological mechanisms of the
root-hemiparasitic interaction. Second, I explain how these fundamentals underlie community
and ecosystem effects recognized in a series of root-hemiparasitic species. And third, I discuss
ecological applications of root-hemparasitic plants, which are based on their effects on plant
communities and ecosystems. I also outline possible future research directions and applications
of root-hemiparasitic plants in ecological restorations and agriculture.
13
2.2. Ecophysiological mechanisms of the hemiparasite-host interaction
The life cycle of a hemiparasite starts by seed germination as in other plants. The germination
may be spontaneous in favourable conditions or may require an external stimulus to break seed
dormancy. In most species, the dormancy-breaking factor is environmental; germination is
triggered by a period of low temperature (Curtis & Cantlon, 1968; ter Borg, 2005; Liebst &
Schneller, 2008), which in temperate species secures that the seedlings appear in spring when
the conditions are favorable for seedling survival. Following germination, the seedling grows
independently of a host. It produces a root system to forage for host roots and uptake water and
mineral nutrients from the soil. The formation of haustoria and establishment of host connection
usually follows after a period lasting few days to few weeks and is facilitated by chemical clues
(haustorial inducing factors) which are excreted from host roots (Yoshida et al., 2016). The
unattached seedlings of most hemiparasites display inefficient physiology with low rates of
photosynthesis and frequently observed imbalance of mineral nutrient concentration. This
results in in poor growth or even premature death if host attachment is not established (Mann
& Musselman, 1981; Seel et al., 1993; Fer et al., 1994; Lechowski, 1996; Matthies, 1997; Jiang
et al., 2007). While, there are some exceptions of hemiparasites that are able to grow decently
without a host, such as Odontites vernus, Euphrasia minima (Matthies, 1998) or Santalum
acuminatum (Radomiljac et al., 1999), there is no empirical evidence reporting unattached
hemiparasites from natural conditions. Some root hemiparasites evolved an advanced strategy
of host-contact establishment. These species require a chemical trigger from the host to initiate
germination (Section 1, Fig. 1). The chemical signals used to trigger germination are called
strigolactones (Cardoso et al., 2011; Yoshida et al., 2016) and were identified to play a crucial
role in plant communication with arbuscular mycorhizal fungi (Akiyama et al., 2005) and later
became recognized as a previously unknown type of plant hormones (Gomez-Roldan et al.,
2008). Typically, these species also have a fully heterotrophic seedling. This means that they
practically avoid the stage of unattached seedling which a critical phase of the life cycle when
most of the mortality occurs caused either by adverse environmental conditions or competitive
pressure from the host community (Ameloot et al., 2006; Ducarme & Wesselingh, 2009; Těšitel
et al., 2011).
Root hemiparasites withdraw resources from xylem vessels in the host roots. This nature of
the anatomical connection determines resources taken up from the host, i.e. water, mineral
nutrients, but only a limited amount of organic carbon. The unidirectional flow of resources
from the host to parasite is underlain by high concentration of sugar alcohols, which are
14
osmotically active and lower the water potential of the hemiparasites (Hodgson, 1973; Press,
1995; Pageau et al., 1998; Jiang et al., 2005). Moreover, the resource flow may be further
facilitated by some types of the xylem-xylem contact in the haustoria. In many hemiparasitic
species (typically those of Santalales and Krameriaceae but also some Orobanchaceae) either
cell wall or parenchyma cells are present on the host-parasite interface (Tennakoon et al., 1997;
Tennakoon & Cameron, 2006; Brokamp et al., 2012). While water and some smaller molecules
can pass through cell walls, the parenchyma cells may actively transport nutrients from host to
the parasite facilitating uptake of greater molecules. A number of root-hemiparasitic species
have however evolved open xylem continuity in the haustoria (Hibberd & Jeschke, 2001). Such
continuity allows mass flow of xylem sap from the host to the parasite and is typical of species
of Orobanchaceae genera Striga (Dörr, 1997) and Rhinanthus (Cameron et al., 2006). These
hemiparasites typically have highly elevated transpiration rates which greatly facilitates
resource uptake from the hosts. Moreover, Orobanchaceae of the Rhinanthoid clade possess
specialized hydathode-trichomes on their leaves which excrete water during night-time when
transpiration does not proceed (Govier et al., 1968; Světlíková et al., 2015).
All water and mineral nutrition of root hemiparasites is typically of the host origin and
may account for a substantial proportion of these resources taken up by the host (Ehleringer &
Marshall, 1995; Jiang et al., 2003, 2004). By contrast, carbon nutrition used to be hypothesized
to be dependent solely or mostly on hemiparasites’ photosynthesis. This was based on their
morphology which in most cases resembles that of non-parasitic plants and in recent decades
also on gas-exchange measurements indicating rates of photosynthesis comparable to those
found in other plants (Fer et al., 1994; Seel & Press, 1994; Lechowski, 1996; Těšitel et al.,
2011). Earlier reports on insufficiency of hemiparasites photosynthesis to secure carbon
nutrition in a series of temperate hemiparasitic Orobanchaceae (Press et al., 1988; Press, 1989)
can nowadays be quite safely considered mistakes attributable to limitations of gas-exchange
measurement instrumentation available at that time. Exceptions of this are however species of
the genus Striga, photosynthesis of which was demonstrated to be generally low (Graves et al.,
1992; Cechin & Press, 1994). Similarly, species of genera Tozzia and Rhynchocorys, which are
holoparasitic in the initial phase of their life (Section 1) may, be presumed to display reduced
photosynthetic ability; however no empirical data are available in this respect.
Still, many root hemiparasites obtain organic carbon from their hosts despite the
efficiency of photosynthesis and the exclusive connection to host xylem. This is because xylem
sap of the hosts contains certain concentration of carbon (usually around 5-10 mmol org. C/l),
15
mainly in the form of amino-acids or organic acids (Govier et al., 1967; Seel & Jeschke, 1999;
Alvarez et al., 2008). The transfer of organic compounds from host to hemiparasite was first
demonstrated by a 14
C-radioisotope labelling study of the model hemiparasitic associations of
Odontites vernus with Hordeum vulgare and Trifolium repens hosts (Govier et al., 1967). While
this approach successfully identified numerous compounds translocated from the host to the
parasite, it was largely qualitative and thus could not provide information on the quantitative
contribution of host-derived carbon to the parasite carbon budget. The first quantitative
assessment followed two decades later and was based on an analysis of carbon-stable isotopic
composition of biomass of two Striga species attached to hosts with C4 photosynthetic pathway
(Press et al., 1987). C4 plants are known to differ in carbon stable-isotopic composition of
assimilates from C3 plants (Boecklen et al., 2011). All hemiparasites use the C3 pathway while
a number of hosts are C4 plants. Comparisons between the actual stable-isotopic composition
of a hemiparasite attached to a C4 host with that of hemiparasite attached to a C3 host or a
prediction based on gas-exchange measurement can thus be used to estimate proportion of hostderived
carbon in hemiparasite biomass. The latter approach was used by Press et al. (1987),
which resulted in an estimate of 28% and 35% of host-derived carbon in hemiparasite biomass
in S. hermonthica and S. asiatica, respectively. Comparable proportions of heterotrophic carbon
in hemiparasite biomass were identified also in a number other root-hemiparasitic species
including temperate species of genera Euphrasia and Rhinanthus (Těšitel et al., 2010a). Recent
research has however identified extensive variability of heterotrophic carbon proportion present
even within a single host-hemiprasite association. The host contribution to carbon budget was
demonstrated to vary during ontogeny and also differ between below- and above- ground parts
of the hemiparasite (Pageau et al., 1998; Santos-Izquierdo et al., 2008). Increased proportions
of host-derived carbon were found in hemiparasites which were shaded, i.e. their photoassimilation
was limited by an external factor (Těšitel et al., 2011). Most recently, a glasshouse
experiment with Rhinanthus alectorolophus (Těšitel et al., 2015b) has demonstrated that
contributions of heterotrophic and autotrophic pathways to the carbon budget of hemiparasites
largely depend on the availability of other resources and physiological balance between the host
and parasite. Highest proportion of host-derived carbon was found in hemiparasites that were
stressed by simultaneous low availability of water and mineral nutrients, which had a strong
negative impact on their photosynthetic ability. Hemiparasite biomass also contained elevated
proportions of host derived carbon when the balance of the hemiparasitic assotiation was shifted
towards the hosts’ side due to the simultaneous abundance of both abiotic resources,. This
indicates that host-derived carbon is used as a back-up resource when hemiparasite’s own
16
photoassimilation is limited. It is also notable that the amount of carbon transferred from the
host to the hemiparasite accounted for approximately 5% of total carbon in host above ground
biomass (Těšitel et al., 2015b) irrespective of experimental treatment. This indicates that carbon
loss is not responsible for a major part of harm inflicted to the host by hemiparasitism.
2.3. Ecology of the hemiparasite-host interaction
The hemiparasitic interaction between a root hemiparasite and its host has an ambiguous nature.
It is a clear case of parasitism below ground, where the parasite benefits from resources taken
up from the host. Hemiparasites are mostly strong parasites which generally cover their needs
for abiotic resources by parasitism. They also benefit from the fact that they do not need to
invest into extensive root systems. Above-ground, however, a host and a hemiparasite are just
two green plants that compete for light (Matthies, 1995; Fibich et al., 2010), an interaction
which is further strengthened by the spatial proximity of their shoots (Keith et al., 2004). Root
hemiparasites are mostly considered or assumed poor competitors (Hellström et al., 2004;
Cameron et al., 2009; Fibich et al., 2010; Borowicz & Armstrong, 2012). The effect of
competition for light suppresses hemiparasite growth (Matthies, 1995; Těšitel et al., 2011;
Mardoian & Borowicz, 2016) but also increases seedling mortality (Těšitel et al., 2011;
Mardoian & Borowicz, 2016). The latter should have even stronger consequences for the
population dynamics in particular considering the annual life history typical of many roothemiparasitic
species especially in Orobanchaceae (Tank & Olmstead, 2008; Těšitel et al.,
2010b). Elevated competitive pressure from the host (community) can largely be expected in
ecosystems with favorable climate and with abundant below-ground resources (water and
mineral nutrients), i.e. sites with high above-ground primary productivity (Hautier et al., 2009).
Hemiparasite populations have repeatedly been demonstrated to decrease in density at sites of
elevated productivity; however the individuals having survived the critical seedling stage
produced more biomass and/or more seeds (van Hulst et al., 1987; Mudrák & Lepš, 2010;
Těšitel et al., 2013). It is likely that the surviving individuals were exceptionally well attached
to their hosts (Keith et al., 2004); their survival may hence be facilitated by heterotrophic carbon
acquisition (Těšitel et al., 2011). The elevated growth can then be attributed to elevated soil
resources on which the hemiparasites response by an increase of photosynthesis similarly to
non-parasitic plants (Simier et al., 2006; Těšitel et al., 2015b) and subsequent elevated
individual fitness (Mudrák & Lepš, 2010; Hejcman et al. 2011; Těšitel et al. 2013). Still, the
population may become exterminated since the elevated fecundity of the hemiparasites does
not compensate for the decrease of population density under productivity level above certain
17
threshold. For instance, Rhinanthus minor population persistence was largely dependent on
import of seeds from the surrounding in a field fertilizer experimental setup if productivity of
the meadow was higher than 5t dry mass per hectare (Hejcman et al., 2011).
Both parasitic and competitive components of the root-hemiprasitic interaction were
included in a model of hemiparasite population dynamics (Fibich et al., 2010). This model
identified equilibria of stable coexistence between a parasite and a host under low to moderate
productivity. By contrast, parasite population was predicted to perish under very low and high
productivity values, caused by insufficient host resources and competitive pressure from the
host, respectively. Such model is largely in line with empirical evidence from field experiments
described in the previous paragraph. However, there are two effects that may counter-act the
effect of competition on root-hemiparasites. First, parasitism may contribute significant amount
of heterotrophic carbon, which may support parasite vertical growth and facilitate escape from
competition (Těšitel et al., 2011). Some species with holoparasitic-seedling stage (Tozzia
alpina, Rhynchocorys elephas, Striga asiatica) were even observed to be able to flower and
reproduce under heavy light deficiency (Fig. 3A,B; Dörr, 1997). Second, infection by a root
hemiparasite may inflict substantial harm to the host which may decrease its competitive ability.
The suppression of host growth by hemiparasitism mostly impacts shoots more than roots
(Těšitel et al., 2015b; Matthies, 2017), which makes this effect a crucial determinant of aboveground
competition. Hemiparasitism was recently suggested to have a disproportionally great
impact on clonal hosts (Demey et al., 2015; Mudrák et al., 2016), which are typically strong
competitors in temperate grasslands (Gough et al. 2012; Herben et al., 2014). This strategy may
strongly decrease the intensity of above-ground competition and create gaps for seed
regeneration, which may facilitate persistence of hemiparasite populations (Lepš & Těšitel,
2015). An extreme case of hemiparasite causing harm to its hosts to decrease competitive
pressure was reported for Okoubaka aubrevillei. This species of Santalales is a tree growing in
tropical rainforests, a habitat characteristic by extreme intensity of competition for light (Grace
& Tilman, 1990). To facilitate regeneration from seeds, O. aubrevillei saplings inflict extreme
harm to its hosts, some of which may even be killed (Veenendaal et al., 1996).
Disproportionally greater negative effects are exerted upon fast-growing hosts, which has clear
benefit for the parasite in terms of avoiding competition. The population dynamics model of
Fibich et al. (2010) thus needs further generalization to account for these cases which
apparently contradict its prediction.
18
Root hemiparasites are mostly recognized as generalist parasites though the host range
may be narrower in those species requiring host induction for germination, e.g. the Striga
species (Parker, 2013). However, individual hosts markedly differ in their quality, i.e. how
much they support hemiparasite growth. Some species may be even resistant to hemiparasitic
infection. This may be based either on pre-attachment mechanism related to chemical signaling
before the haustorial initiation or on post-attachment mechanisms when the host blocks resource
Fig. 3. Hemiparasitic strategy in environment of heavy light deficiency. A,B: Rhynchocorys elephas
and Tozzia alpina growing under the canopy of Petasistes spp.; both species have long-lasting
underground heterotrophic stage. Shoots are only produced for the purpose of generative
reproduction. C: Dense stand of Melampyrum sylvaticum in a shady spruce-forest understory.
19
transfer from its vascular bundles (Cameron et al., 2006; Yoder & Scholes, 2010). The postattachment
resistance mechanism may be recognized by inspection of haustorial anatomy as
was exemplified on the interaction between Rhinanthus minor and Plantago lanceolata
resistant to Rhinanthus infection (Cameron et al., 2006; Rümer et al., 2007). Interestingly, P.
lanceolata had earlier been demonstrated as a very good host of several hemiparasitic
Euphrasia species (Yeo, 1964). This indicates that the root-hemiparasitic interaction depends
on species identity of the host and the hemiparasite and there are no universal good or bad hosts.
Nitrogen-fixing legumes and grasses have been repeatedly suggested as better hosts than ‘forbs’
at least for a majority of hemiparasitic Orobanchaceae, which was also supported by certain
empirical evidence (Seel & Press, 1993, 1994; Svensson et al., 2001; Cameron et al., 2006).
However, recent studies investigating multiple host associations of Rhinanthus minor
(Rowntree et al., 2014) and Melampyrum arvense (Schädler et al., 2005; Matthies, 2017) did
not support such hypothesis. Similarly, host quality of hemiparasitic Santalales is not
determined by any simple difference between functional groups. Instead, there seems to be a
continuous pattern high quality hosts to hosts of very poor quality (Radomiljac et al., 1999;
Calladine et al., 2000; Guo & Luo, 2010), presence of which may even suppress hemiparasite
growth compared to unattached individuals (Radomiljac et al., 1999). Below the species level,
an interplay between host and hemiparasite genotypes was identified to significantly affect the
outcome of the interaction (Rowntree et al., 2011). Similarly, genotypes resistant to
hemiparasitic infection are known from many field crops attacked by Striga species (Yoder &
Scholes, 2010), which highlights the importance of genetic variability for hemiparasitism.
Field trials generally identified a large number of species to which root-hemiparasitic
plants attach. In addition, certain selectivity for some taxonomic groups (and avoidance of
others) is also frequently observed. For instance, Suetsugu et al. (2008) reported Thesium
chinense attached to 22 species of 11 families with grasses to be positively selected while the
haustoria formed on legumes were of larger size. By contrast, Dostálek & Münzbergová (2010)
reported frequency of Thesium linophyllon attachments to host species largely proportional
their root abundance. Gibson & Watkinson (1989) reported a number of significantly avoided
hosts of Rhinanthus minor while a few were selected positively. Interestingly, Plantago
lanceolata, known to be a resistant host (Cameron et al., 2006), was shown to be positively
selected in this study (though the haustoria can be assumed to be non-functional). Most recently,
(Holá et al., 2017) used a DNA-barcoding approach to identify host associations of three roothemiparasitic
Orobanchaceae (Rhinanthus minor, R. major and Melampyrum nemorosum),
20
which co-occurred at one site. The three species notably differed in selectivity for hosts at the
family taxonomic level. Interestingly, many haustorial connections were identified between
hemiparasitic species themselves both between and within species. Detailed field surveys are
however rare due to methodological difficulties of associated with root-system inspection. In
this respect, the DNA-barcoding approach may facilitate the workflow though there is still a lot
of space for improvement and refinement of this method (Holá et al., 2017). Deficiency of
direct data on host identity is a critical issue of almost all studies aiming at community ecology
of root hemiparasites. There are only few studies where above ground patterns of vegetation or
results of manipulative experiments are compared with parasitic associations below-ground. An
example of such a study is represented by a removal experiment with Pedicularis kansuensis in
which positively selected hosts, grasses and legumes, significantly increased after weeding of
the hemiparasite (Bao et al., 2015).
The hosts’ side of the interaction is characterized by harm inflicted by hemiparasitism,
which is mostly measured as a reduction of its biomass production (or crop reduction in the
case of hosts important for agriculture). The negative effects of hemiparasites on the hosts are
very variable, ranging from negligible to lethal. Besides the extreme host damage inflicted by
Okoubaka aubrevillei described above, hemiparasitic species with open xylem contacts in their
haustoria, such as Striga or Rhinanthus, tend also to be highly host-damaging (Parker, 2013;
Těšitel et al., 2015b). Multiple physiological mechanisms are involved in the harmful effect of
the hemiparasites on their hosts. Loss of abiotic resources is certainly the principal factor in
most cases while loss of organic carbon seems of minor importance (Těšitel et al., 2015b).
Recent experiment with manipulated availability of water and mineral nutrients identified
strong interactive effects of these two resources on harm inflicted to maize and wheat hosts of
Rhinanthus alectorolophus (Těšitel et al., 2015b). This indicates that loss of either resource due
to parasitism may underlie the host damage. In this experiment, the largest harm was inflicted
when either of the resources was provided in abundance while the other was deficient. Even
damage to host photosynthesis (maximum quantum yield) was identified under dry and nutrient
rich conditions. Simultaneous abundance of both resources largely alleviated the effect of
parasitism on the host, while simultaneous deficiency was stressful for the parasites which
consequently limited the harmful effect on the hosts (Těšitel et al., 2015b). While individual
hemiparasitic species differ in their intrinsic harmfulness the damage inflicted to the hosts
depends also on host species. Obviously, resistant hosts are harmed less than susceptible ones
(Cameron et al., 2006). Several studies actually reported a tight correlation between host quality
21
and damage inflicted by hemiparasitism (Matthies, 1996; Marvier, 1998). However, a recent
extensive study with Melampyrum arvense (Matthies, 2017) testing 27 different hosts identified
a group of hosts which supported vigorous growth of the hemiparasites but suffered relatively
little harm. The growth of two legumes, Trifolium pratense and Lotus corniculatus, was actually
negligibly reduced while supporting a decent growth of the parasite. Such pattern was also
reported for some legume hosts also in studies with Rhinanthus spp. (Davies et al., 1997; Joshi
et al., 2000; Cameron et al., 2006). These results are mostly based on simple cultivation trials
comparing host performance between infected and uninfected individuals. Largely ignored in
such experimental setups, the litter input from hemiparasitic plants may however positively
affect productivity of host community (see the next section for details). A recent study has
found that high quality hosts of a hemiparasite may obtain disproportional benefit, which may
partly compensate for the negative effect of parasitism (Fisher et al., 2013). In real
communities, competitive interactions between host and non-host plants and with other trophic
levels are also involved together with the effect of the environment, all of which may have
strong modifying effects on hemiparasitic interactions.
2.4. Community and ecosystem ecology of parasitic plants
Root-hemiaprasitic plants are a generally omnipresent component of terrestrial vegetation, in
particular open (i.e. non-forest) plant communities (Heide-Jørgensen, 2008; Těšitel et al.
2015a). Due to their unique ecophysiology, trophic status and interactions with the hosts they
have been recognized for their ability to influence structure of plant communities (Phoenix &
Press, 2004). The community and ecosystem effects of some root-hemiparasitic species are so
pronounced that they are even considered keystone species or ecosystem engineers (Phoenix &
Press, 2004; Cameron et al., 2005; Press & Phoenix, 2005; Watson, 2009; Decleer et al., 2013;
Těšitel et al., 2017).
Root-hemiparasites may be expected to occur mostly in low-productiveand nutrient
poor environments. Under such conditions, they would benefit most from the parasitism,
providing low cost access to mineral nutrients (Phoenix & Press, 2004, 2005; Fibich et al.,
2010; Borowicz & Armstrong, 2012). In addition, corresponding plant communities tend to be
of relatively low sward or stem density which implies good light availability. As a result, the
effects of above-ground competition, a crucial factor limiting occurrence of root-hemiparasites
(see section 2.3), are rather low. Most Krameriaceae and many of root-hemiparasitic Santalales
largely conform to this scheme occurring in low-productive (semi-)arid habitats (Giannini et
al., 2011; Heide-Jørgensen, 2013). Still, a number of Santalales are tropical-rainforest trees
22
detailed ecology of which has yet to be described. In temperate regions, a recent analysis of
ecological niches of root-hemiparasites in the Czech Republic (Central Europe) identified a
relatively wide range of habitats suitable for at least some root-hemiparasitic species (Těšitel et
al., 2015a). While some species were indeed found to occur at sites of low-productivity limited
by nutrient availability, water deficiency, short vegetation season or a combination of these
(e.g. Euphrasia stricta, Thesium linophyllonm, Odontites luteus, Pedicularis sylvatica,
Rhinanthus riphaeus), some others grow at sites with relatively high productivity. Euphrasia
officinalis Melampyrum arvense, M. pratense, Rhinanthus alectorolophus, R. major, R. minor
can be found over most of the range of the soil fertility gradient but only if such sites are
relatively dry as indicated by Ellenberg indicator values. Some of these species may also be
found on moist sites but their niche is restricted to oligotrophic places at this end of moisture
gradient. Such pattern corresponds well to the experimental study manipulating water and
mineral nutrients, which demonstrated loss of advantage of parasitism and alleviation of its
effect on the host when both resources were provided in abundance (Těšitel et al., 2015b). Two
root-hemiparasitic species, Odontites vernus and Pedicularis palustris, may however grow
even in these conditions, which is underlain either by disturbance, which limits competition and
creates regeneration gaps in the sward or by the selectivity of the hemiparasite for dominant
competitors which are extremely harmed by parasitism (Decleer et al., 2013), respectively.
Three species of Melampyrum (M. nemorosum, M. pratense, M. sylvaticum) grow in understory
of closed-canopy forests (Fig. 3C), where they are also unique by their annual life history
(Těšitel et al., 2015a). A recent model of M. pratense carbon budget based on gas-exchange
data and light-condition monitoring throughout the growth season however suggests
insufficiency of their autotrophic carbon assimilation pathway (Světlíková et al. unpublished).
In particular, the predicted carbon balance was close to zero in summer, when energy- and
carbon-demanding seed production is in progress. This points to possible importance of
heterotrophic carbon acquisition in these species, which is however difficult to demonstrate
directly.
Presence of root-hemiparasites usually results in possibly strong negative effects on host
community productivity (Davies et al., 1997; Joshi et al., 2000; Ameloot et al., 2005; Bardgett
et al., 2006; Stein et al., 2009; Mudrák & Lepš, 2010; Borowicz & Armstrong, 2012; Demey
et al., 2013a; Bao et al., 2015)., which is underlain by suppression of host growth (Phoenix &
Press, 2004; Press & Phoenix, 2005). Moreover, in many cases, a decrease of total productivity
(i.e. host + hemiparasite biomass) was observed (Davies et al., 1997; Ameloot et al., 2005;
23
Stein et al., 2009; Mudrák & Lepš, 2010; Demey et al., 2013a; Bao et al., 2015), which means
that parasite biomass did not compensate for the loss on the hosts’ side. This effect is usually
attributed to lower photosynthetic resource-use efficiency in hemiparasites (Seel & Press, 1994;
Westbury, 2004). However, this effect on total community productivity is far from universal.
In some cases, higher community productivity was observed, e.g. in case of species-poor
assemblages in a biodiversity experiment (Joshi et al., 2000). In an observation-based study,
hemiparasitic Castilleja occidentalis was found to be associated with high-productivity patches
in alpine tundra (Spasojevic & Suding, 2011). The positive influence of root-hemiparasites may
largely be attributed to the effect of their litter on the community. Due to their ability to
withdraw mineral nutrients from the hosts and relatively low photosynthetic resource-use
efficiency (Seel & Press, 1994; Press & Phoenix, 2005), litter of hemiparasites displays high
mineral nutrient concentration, often higher than that of co-occurring species (Quested et al.,
2002, 2003a,b, 2005). This implies higher rates of litter decomposition and consequent release
of nutrients (Quested et al., 2003b; Demey et al., 2013b). The nutrients are also frequently
released from litter during the growth season, when the demand for them is high (Quested et
al., 2005; Demey et al., 2013b). These positive effects of the litter pathway on community
productivity may at least partly compensate for the negative effect of parasitism. Recent
experiments have moreover demonstrated that the largest benefits from the litter pathway are
acquired by host plants species (Fisher et al., 2013) or plants with fast-growth strategy (Demey
et al., 2013b), which may either compensate for the losses to parasitism or even further increase
biomass production, respectively. In addition, hemiparasites have been demonstrated to
increase average nutrient concentration in biomass (Ameloot et al., 2008; Fisher et al., 2013),
which may have additional impacts on nutrient cycling. It is notable that many accounts on
reduction of productivity by hemiparasites are based on peak biomass production in early to
mid-summer. In annual hemiparasites, such as Rhinanthus spp., this captures predominantly the
effects of parasitism, while the effect of nutrient release from litter should affect the community
predominantly in the second half of the season (late summer, autumn), which is usually not
monitored.
Root hemiparasites do not influence only the productivity but exert complex direct and
indirect effects on the community structure. Suppression of host species may result in altered
competitive hierarchy in the communities (Gibson & Watkinson, 1991; Marvier, 1998; Mudrák
& Lepš, 2010; Borowicz & Armstrong, 2012; Bao et al., 2015; Demey et al., 2015). If host
species are competitive dominants and a large reduction of their growth is inflicted,
24
hemiparasites may open space for subordinate species and consequently increase community
diversity (Davies et al., 1997; Pywell et al., 2004; Decleer et al., 2013; Těšitel et al., 2017).
This is further supported by creation of gaps following annual hemiparasite die back in mid- to
late summer, which may facilitate their and other species establishment (Joshi et al., 2000; Lepš
& Těšitel, 2015). However, if a subordinate species is parasitized or the suppressed dominant
is replaced by another one, biodiversity may remain unchanged or may be even lower at plots
with the parasites (Gibson & Watkinson, 1992; Mudrák & Lepš, 2010). Nonetheless, a recent
analysis based on extensive vegetation plot database demonstrated that most root hemiparasites
occur in significantly more species-rich vegetation than expected by chance and some of the
hemiparasitic species are among the species most tightly associated with high community
diversity (Fibich et al., 2017). While this pattern is probably not caused solely by the positive
effect of hemiparasites on diversity and other mechanisms are involved (namely the preference
of hemiparasites to grow in low-competitive habitats which are frequently species rich), this
results represent an upscale of the hemiparasite-diversity relationship from the local level of
single site experiments. Taken together with their effect on productivity, it seems that
hemiparasites may decrease productivity in rather productive environments via the parasitic
pathway and harm inflicted to the fast-growing dominants, while in low productive
environments, the positive effect of the litter pathway could prevail. Such hypothesis was
introduced by Watson (2009) suggesting that root-hemiparasites create environment of
intermediate productivity and open opportunities for generative reproduction, which is largely
beneficial for them in terms of host resource availability and limited effect of above-ground
competition. Eventually, communities of intermediate productivity are also those which display
highest biodiversity worldwide (Fraser et al., 2015).
The ecological interactions of root hemiparasites are not limited to the plant component
of the ecosystems. Strong interactions with organisms of other trophic levels were observed and
described in the literature. Root hemiparasites are mostly non-mycorrhizal. In recently
described notable exceptions to this, two species of Pedicularis were demonstrated to have lowcolonization
level of arbuscular mycorrhiza in their roots, which may contribute up to few
percent of their phosphorus nutrition while the rest is provided by the host (Li et al., 2013).
However, strong indirect interactions with arbuscular mycorrhiza were reported. In a
glasshouse experiment, a strong benefit was observed for Rhinanthus minor if attached to a
mycorrhizal host, which was also more suppressed by hemiparasitism (Davies & Graves, 1998).
In another experiment, interactive effects of mycorrhizal fungi and parasitism on community
25
structure were observed, with the effect of parasitism only apparent in mycorrhiza-infected
communities (Stein et al., 2009). Apart from mycorrhiza, presence of hemiparasite was
demonstrated to influence fungal-to-bacterial ratio in soil, a major pattern of soil microbial
communities (Bardgett et al., 2006). A complicated four-member interaction was described
between Rhinanthus major, its grass host (Festuca pratensis), alkaloid-producing endophyte
present in grass roots and an aphid herbivore (Lehtonen et al., 2005). The hemiparasite took up
alkaloids of the host, which are produced by the symbiotic endophyte and protect the host
against herbivory if it is not parasitized. If parasitized, the hemiparasite benefited from the
herbivory protection while the grass host did not. Thus, the hemiparasite changed the originally
mutualistic interaction between the grass and the endophyte to parasitic. Alkaloids, but this time
of intrinsic host origin, also played an important role in another complex interaction. Two
Castilleja species were found to benefit from lupin hosts (Lupinus albus, L. argenteus) and an
uptake of alkaloids from them due to improved pollination and reduced herbivory (Adler, 2000,
2002). Hemiparasites may also mediate herbivory of hosts plants. In a glasshouse experiment,
Rhinanthus major was demonstrated to decrease herbivory of acyanogenic Trifolium repens
hosts while no such effect was observed in the case of cyanogenic plants (Puustinen &
Mutikainen, 2001). In a multi-host experiment. Palatability of Melampyrum arvense biomass
was found to strongly differ if attached to different host species but unrelated to host species
palatability, which indicates a complicated underlying mechanism based on the interaction of
hemiparasitism and host anti-herbivory defense (Schädler et al., 2005). Concerning roothemiparasitic
Santalales, vegetation containing shrubby hemiparasite Exocarpos strictus was
demonstrated to host more species of birds and a higher abundance of arthropods compared to
vegetation without the hemiparasite (Watson et al., 2011).
To sum up, a number of root-hemiparasitic species were demonstrated to affect the
community structure, productivity and diversity via either parasitic or facilitative interaction.
These effects may reach beyond the plant community to the scale of the whole ecosystem. Some
of them may also offer opportunities for ecological applications. More on that in the next
section.
2.5. Applications of root hemiparasites in ecological restoration
The idea on application of root-hemiparasitic plants in ecological restoration and nature
conservation stems from the experimental work of Davies et al. (1997) who demonstrated that
presence of Rhinanthus species is associated with lower grassland productivity. This study
comprised also an experiment manipulating Rhinanthus density by weeding, which
26
demonstrated suppression of grasses by the hemiparasites and reduction of sward density.
Following this pioneering study, a number of further trials were done to test the applicability of
Rhinanthus spp. (mostly Rhinanthus minor) in grassland restoration in Western Europe. The
typical situations included either grassland sites which had been used for intensive agriculture
and managed accordingly or former field used in agriculture. Either of these had been fertilized
and the meadows also mown several times (>2) a year. Such high land-use intensity is known
to greatly decrease diversity of the grassland ecosystem (Allan et al., 2014, 2015; Lepš, 2014).
Cease of fertilizer application combined with a decrease of mowing intensity may help restoring
community diversity of meadows; however, this is largely impeded by high amount of residual
soil nutrients and dominance of fast-growing clonal competitive grasses (Gough et al., 2012;
Lepš, 2014), which prevent establishment of other species. Similarly, in abandoned fields,
competitive species may dominate after several years of succession even if the fields are seeded
by dedicated seed mixtures of regional provenance (Prach et al., 2014). Drastic measures such
as topsoil removal or gramicide chemicals may be used to decrease dominant grass abundance
and/or remove residual nutrients but these are costly and questionable from the environmental
impact perspective. Therefore, the use of Rhinanthus sowing was tested as an alternative
biological option. Application of Rhinanthus minor was demonstrated more beneficial to
community diversity compared to the selective gramicide chemicals (Westbury & Dunnett,
2008) and supported establishment of significantly more target species sown at the beginning
of the experiment. Another experiment identified a positive effect of supplementary soil surface
scarification measure on establishment of R. minor on an abandoned field where a mixture of
target grassland species was sown (Westbury et al., 2006). In the same time, Rhinanthus itself
was demonstrated to decrease grass dominance in the community and to increase community
diversity. A similar experiment on a newly established meadow on ex-arable field demonstrated
that R. minor can decrease grass dominance even at sites with high soil nitrogen concentration
but only at high sowing density (1000 seeds -2
;Westbury & Dunnett, 2007). The most detailed
experiment among these was conducted on a meadow of moderate productivity, which had been
fertilized in the past and was dominated by a few grasses and forbs at the start of the experiment
(Pywell et al., 2007). The experimental treatments included sowing of Rhinanthus minor in
different densities and sowing of a mixture of target species combined in a factorial design.
Rhinanthus established at the plots where sown and later invaded also the unsown plots. A
strong negative effect of Rhinanthus was found on sward height, which decreased by 50% at
plots with a high hemiparasite density. By contrast, the effect on overall diversity as well as
diversity of sown species was significantly positive. Analysis of species composition changes
27
identified a positive effect of Rhinanthus on a number of forb species, such as Leucanthemum
vulgare, Leontodon autumnalis, Plantago lanceolata, Prunella vulgaris. The utility of
Rhinanthus minor on grassland restoration was also tested in a multi-site experiment scaling up
the findings of the other studies to the landscape scale (Hellström et al., 2011). The success of
these experiments with Rhinanthus minor resulted in its regular application in grassland
restoration in Western European countries, in particular the UK (Blakesley & Buckley, 2016).
In addition to high land use intensity, grassland biodiversity is also threatened by
abandonment, i.e. cessation of mowing. This process leads to a similar community structure
with a few competitive dominants as in the case of high land-use intensity. However, species
identity is usually different. Abandonment and associated expansion of dominants is a particular
problem in species-rich meadow grasslands occurring in Central and Eastern Europe, some of
which represent the most species-rich grassland from the global perspective (Wilson et al.,
2012; Dengler et al., 2014; Chytrý et al., 2015). Particular issue there is the expansion of
Calamagrostis epigejos, a dominant clonal grass, which spreads not only to abandoned sites
but also to vegetation managed by low-intensity mowing, i.e. the management type
recommended to maintain biodiversity (Dengler et al., 2014). The competitive strategy of this
clonal species involves spread by rhizomes and resource storage in the roots, which make it
robust against targeted measures applied above ground. However, a recent multi-site study
(Těšitel et al., 2017) demonstrated that the grass may be infected by hemiparasites of the genus
Rhinanthus, namely R. alectorolophus. R. alectorolophus exerts a drastic effect on the grass
and may even exclude it from the community within two years, in particular if its application
is coupled with a moderate increase of mowing intensity. In addition, species diversity may be
restored in a rather short term. Such effect was only identified at one site out of three; however
this represented a typical case of abandoned intermittently wet meadow, which expands the
potential of this finding. Based on these results and also other similar experiments waiting for
publication, nature conservation in the Czech Republic has started to use the hemiparasites as
a restoration measure at sites infested by Calamagrostis epigejos. Another example of a root
hemiparasite suppressing a particular competitive dominant is a report of Pediculartis palustris
which drastically reduced tall sedges (mainly Carex acuta) and transformed a tall-sedge
vegetation into a fen meadow, a highly valuable community from the nature conservation
perspective (Decleer et al., 2013).
All these studies indicate a great potential of the use of root-hemiparasitic plants in
ecological restoration and biodiversity conservation, which is further facilitated by detailed
28
application guidelines (Mudrák et al., 2014; Těšitel, 2015; Blakesley & Buckley, 2016)
However, there are always controversies connected with introduction of seeds of species on
sites from which they were previously absent. Therefore, the hemiparasites should be used with
caution. Preferably local seed sources should be used where possible. Ideal situation includes
seeds transfers within a single site, which complies with the most strict requirements of nature
conservation to preserve genetic resources and thus can be used even in nature reserves.
2.6. Future perspectives
The ecological interactions of root hemiparasites with their hosts are well understood
particularly in grassland habitats and in the case of agricultural weeds. This knowledge is based
on observations and experiments conducted in situ, which provides a good basis for
understanding the ecology in the context of real communities and ecosystems as well as on
glasshouse experiments which aim at identification of the nderlying physiological mechanisms.
However, we still know very little about the ecology and ecophysiology of root hemiparasites
growing in the forest vegetation. This includes e.g. Melampyrum species of Orobanchaceae and
many woody species of Santalales. More information on their ecology, resource acquisition
from the host and especially strategies of carbon acquisition in the shady environment may
reveal new and possibly surprising ecological stories such as that of Okoubaka aubrevillei and
its extreme effect on the hosts (see section 2.3).
The contemporary literature summarized here also contains a number of accounts on
complicated ecological interactions where root hemiparasites play a central role. Most of these
reports are however based on experiments in glasshouse conditions. The extent to which, these
effects may be present in the context of real ecosystems remains questionable. Certainly some
effects may be quite strong and frequent as demonstrated e.g. by field studies on stem-parasitic
mistletoes which have a profound effects on nutrient cycling, productivity and community
composition of several trophic levels (Watson, 2016). More studies aiming e.g. at direct and
indirect interactions with mycorrhizal fungi, pollinators, invertebrate and vertebrate herbivores
in the field conditions are thus needed to develop this topic.
One of the appealing question is the true nature of the interaction between root
hemiparasites and Fabaceae. Both groups display specialized strategies of nutrient acquisition
and Fabaceae frequently serve as hosts of the hemiparasites. While mostly high quality hosts,
harm inflicted to them seems rather restricted at least in some species. A number of field
experiments also did identify none or only moderately negative effect of hemiparasites on
29
legume abundance in the community. Therefore, they may be rather tolerant hosts. In such case,
they may actually establish an alliance with the hemiparasites to suppress competitively
superior grasses. Such hypothesis may be supported by existence of vegetation patches, where
these groups co-occur in abundance (Fig. 4A) and both look rather vigorous while grasses seem
strongly suppressed (Fig. 4B). Although such patches may be transient, repeated informal
observations of the same site suggest that they persist for at least several years. If such
community could be established on a large scale, there may be a number of applications in agriand
horticulture, such as designing low-intervention high-benefit grassland communities for
orchard understory (Fig. 4C).
The role of hemiparasitic plants in ecological restoration and nature conservation is
generally established due to recent strong development of the topic. However, practical
experience indicates success at some sites, mixed effects at others and complete failure
elsewhere. Scaling the research up to the large landscape scale is therefore needed to assess
suitability of sites for hemiparasite application and identify underlying biotic and abiotic
factors. This would greatly facilitate further use of hemiparasites by nature conservation and
possibly also stakeholders.
Fig. 4. Illustrations of possible alliances between root hemiparasites and legumes (A,B). A: Patch
of Rhinanthus alectorolophus and Onobrychys viciifolia on a restored meadow near Suchov, Bílé
Karpaty Mts.; B: Intraction of Rhinanthus minor, Trifolium pratense and the grass Festuca rubra.
Trifolium seems to support vigorous growth of Rhinanthus, while Festuca looks strongly supressed.
C: pilot application of the hemiparasites (R. minor, R, minor) in apricot orchard understory.
30
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4. List of papers
1. Těšitel J. 2016. Functional biology of parasitic plants: a review. Plant Ecology and
Evolution 149: 5–20.
2. Těšitel J, Těšitelová T, Fisher JP, Lepš J, Cameron DD. 2015. Integrating ecology
and physiology of root-hemiparasitic interaction: interactive effects of abiotic resources
shape the interplay between parasitism and autotrophy. New Phytologist 205: 350–360.
3. Světlíková P, Hájek T, Těšitel J. 2015. Hydathode trichomes actively secreting water
from leaves play a key role in the physiology and evolution of root-parasitic rhinanthoid
Orobanchaceae. Annals of Botany 116: 61–68.
4. Těšitel J, Hejcman M, Lepš J, Cameron DD. 2013. How does elevated grassland
productivity influence populations of root hemiparasites? Commentary on Borowicz
and Armstrong (Oecologia 2012). Oecologia 172: 933–936.
5. Těšitel J, Fibich P, de Bello F, Chytrý M, Lepš J. 2015. Habitats and ecological niches
of root-hemiparasitic plants: an assessment based on a large database of vegetation
plots. Preslia 87: 87–108.
6. Fibich P, Lepš J, Chytrý M, Těšitel J. 2017. Root he miparasitic plants are
associated with high diversity in temperate grasslands. Journal of Vegetation Science
28: 184–191.
7. Lepš J, Těšitel J. 2015. Root hemiparasites in productive communities should attack
competitive host, and harm them to make regeneration gaps. Journal of Vegetation
Science 26: 407–408.
8. Těšitel J, Mládek J, Horník J, Těšitelová T, Adamec V, Tichý L. 2017. Suppressing
competitive dominants and community restoration with native parasitic plants using the
hemiparasitic Rhinanthus alectorolophus and the dominant grass Calamagrostis
epigejos. Journal of Applied Ecology. doi: 10.1111/1365-2664.12889.
9. Holá E, Kocková J, Těšitel J. 2017. DNA barcoding as a tool for identification of host
association of root-hemiparasitic plants. Folia Geobotanica. doi:10.1007/s12224-017-
9286-z.
10. Mudrák O, Mládek J, Blažek P, Lepš J, Doležal J, Nekvapilová E, Těšitel J. 2014.
Establishment of hemiparasitic Rhinanthus spp. in grassland restoration: lessons learned
from sowing experiments. Applied Vegetation Science 17: 274–287.