Acta Botanica Brasilica - 30(1): 41-46. January-March 2016.
©2016 doi: 10.1590/0102-33062015abb0177
Host preference of the hemiparasite Struthanthus
flexicaulis (Loranthaceae) in ironstone outcrop
plant communities, southeast Brazil
Fabiana Alves Mourão1*, Rafael Barros Pereira Pinheiro1, Claudia Maria Jacobi1 and José Eugênio Côrtes Figueira1
Received: July 8, 2015
Accepted: October 14, 2015
ABSTRACT
Struthanthus flexicaulis is a hemiparasite abundant in ironstone outcrops in southeast Brazil. We evaluated its host preference
among species of the plant community, taking into account the abundance and foliage cover of the hosts. The importance of
each species in the community and the mortality caused by the parasite were assessed based on a quantitative survey in 10 strips
measuring 1m x 50m. The 10,290 individuals belonged to 42 species. Only 15 had a relative abundance in the plant community
greater than 1%, of which 12 showed vestiges of parasitism. More than 80% of deaths in the community were associated with
parasitism. Non-infected individuals had significantly less mortality rates (7%) than those infected (83%) (²= 1102.4, df = 1,
p < 0.001). The observed infestation was different from the expected both regarding relative host abundance (²= 714.2, df = 11,
p<0.001) and foliage cover (²= 209.2, df = 11, p<0.001). Struthanthus flexicaulis preferred Mimosa calodendron, a legume attractive
to avian seed dispersers. The interaction is maintained and intensified not only by the birds, who deposit innumerous seeds on the
hosts branches, but also very likely by the ability of M. calodendron to fix nitrogen, thereby enhancing the mistletoe’s development.
Keywords: canga, Iron Quadrangle, ironstone outcrop, plant-plant interaction, parasitism
Introduction
Parasitic plants depend on their hosts for nutrient and
water supply, and may show different degrees of specificity for their hosts. This preference is related to the local
abundance and degree of constancy of plants in time and
space (Norton & Carpenter 1998; Norton & Lange 1999).
Besides resource availability (plants), the success of infection also depends on anatomic and chemical aspects that
promote host recognition and haustorium formation, a
modified root specialized in nutrient uptake (Rodl & Ward
2002; Press & Phoenix 2005; Arruda et al. 2006).
Specificity may be advantageous in homogeneous environments, where a certain plant species is predominant.
In these cases, specialist parasites could increase their
efficiency in nutrient uptake from their hosts. In New
Zealand, the mistletoes Alepis flavida, Peraxilla colensoi,
and P. tetrapetala specialize in different Nothofagus species
(Norton & Carpenter 1998). However, in heterogeneous environments, specialists would be in disadvantage
because of the high plant diversity (Norton & Carpenter
1998; Arruda et al. 2006), especially when potential
hosts occur in low densities. This would explain the low
specificity of species of Loranthaceae in heterogeneous
plant communities such as tropical rainforests (Norton
& Carpenter 1998) and savannas (Dzerefos et al. 2003;
Arruda et al. 2006).
The impact caused by mistletoe infection on a plant
community may vary as a function of the host plant identity and abundance. Legumes appear to be preferred hosts
of all parasitic plants on account of their nitrogen-fixation
Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Av. Antônio Carlos, 6627, 31270-901, Belo
Horizonte, MG, Brazil
* Corresponding author: fabimourao@gmail.com
1
Fabiana Alves Mourão, Rafael Barros Pereira Pinheiro, Claudia Maria Jacobi and José Eugênio Côrtes Figueira
ability (Radomiljac et al. 1999; Bowie & Ward 2004). The
term ‘preference’ has been used in several works to indicate
the disproportional infection in relation to host availability in the area (Aukema & Río 2002; Dzerefos et al. 2003;
Press & Phoenix 2005; Runyon et al. 2006; Lemaitre et al.
2012). The main factors that lead to this preference are
the host spatio-temporal distribution, behavior of avian
dispersers, and parasite establishment success (Aukema &
Rio 2002; Medel et al. 2002; Roxburgh & Nicolson 2005).
Struthanthus flexicaulis is a common hemiparasite on
plant communities over ironstone outcrops in the Iron
Quadrangle region (southeast Brazil), and is known to
cause a significant reduction on the survival and fitness
of its hosts (Mourão et al. 2009). In these communities it
successfully infects more than 40 plant species (Mourão
et al. 2006), although probably with different degrees of
success among these hosts, based on the preference factors mentioned above. Previous studies suggested that
the shrub Mimosa calodendron (Fabaceae) is its preferred
host (Mourão et al. 2009; Reis et al. 2010). However, since
this species is one of the most abundant on ironstone
outcrops in the Iron Quadrangle, this perception needs
to be validated by a rigorous comparison among hosts. In
this study we evaluated the preference of S. flexicaulis to
hosts in the plant community based on their abundance
and cover, and the effect of parasitism on the mortality rate of each host species. Our hypothesis was that
M. calodendron is a preferred perching species for birds
dispersing S. flexicaulis seeds and, being a legume, a better
host for their survival and also a more resistant host to
parasitism. We predicted that M. calodendron individuals
are significantly more infected than other hosts but less
prone to death by parasitism.
Materials and Methods
We performed our survey in a plant community over
ironstone outcrop (20°03’60”S, 44°02’00”W, 1300 m),
within the limits of the Serra do Rola Moça State Park,
a strictly protected area located in the Iron Quadrangle,
southern Espinhaço Range. The climates is mesothermic,
with mean annual rainfall between 1000 and 1500 mm, a
pronounced dry season between April and September, and
mean annual temperature of 25°C (Rizzini 1997).
The plant communities established on these outcrops
are species-rich and are home to members of 45% of the
native vascular families that occur in Brazil, including until
now 60 endemic species (Carmo & Jacobi 2012). Individuals are subjected to high radiation, poorly developed soils
(litholic neosols) with high heavy metals concentrations,
and low water retention (Porto & Silva 1989; Teixeira &
Lemos-Filho 2002; Jacobi et al. 2007). Given these conditions, vegetation is predominantly composed of herbs and
shrubs, with few tree species. Species-rich dicotyledon
families are Asteraceae, Fabaceae and Myrtaceae; and the
42
main monocotyledons are Poaceae, Cyperaceae and Orchidaceae (Jacobi et al. 2007; Viana & Lombardi 2007). Among
parasitic plants, the genera Tripodanthus and Struthanthus
are very abundant, both belonging to Loranthaceae, the
largest mistletoe family.
To evaluate the importance of each species in the community and mortality rates associated to parasitism, we
performed a quantitative survey along ten parallel strips
(1m x 50 m), distant 10 m between each other, totaling
500 m2. Each strip was divided into 1 m2 plots and individuals within them were counted and identified. Because
of the difficulty of calculating their abundance, Poaceae,
Cyperaceae, and Orchidaceae were excluded from the
analyses. Members of these families are seldom –if ever–
hosts for Loranthaceae, so analyses were not affected by
their exclusion.
In both the analyses of mortality and preference, we
only took into account the twelve species with relative
abundance > 1% in the sampled area and at least one
infected individual. Individuals were separated into four
categories, combining two binary characteristics: alive
or dead, and infected or not. This classification was possible because dry branches and haustoria of S. flexicaulis
remained clearly visible on dead infected individuals. We
used Chi-square tests to test for significant mortality differences between infected and non-infected individuals
of each species.
To quantify the abundance of each plant species in the
sampled area we considered all individuals. Species with
clonal growth, such as Cactaceae and Velloziaceae, were
counted as one individual when distance between ramets
was less than 5 cm. For this reason the exact number of
individuals is probably overestimated in these families.
Plant cover of each individual was estimated based on the
vertical crown projection to the ground. These areas were
calculated by approximating them to regular geometric
figures.
To calculate the expected number of infected individuals based on their relative abundance we used the equation:
n
Pexp = n i x Ptot
tot
where Pexp = number of expected individuals of each host
species, ni = abundance of each host species, ntot = total
number of sampled individuals, and Ptot = total number of
infected individuals.
Similarly, the following equation was used for the
expected number of infected individuals based on plant
cover, substituting variables as follows:
cov
Pexp = cov i x Ptot
tot
where covi = plant cover of each host species and covtot =
total plant cover of infected individuals.
Acta Botanica Brasilica - 30(1): 41-46. January-March 2016
Host preference of the hemiparasite Struthanthus flexicaulis (Loranthaceae)
in ironstone outcrop plant communities, southeast Brazil
In both cases, we performed Chi-square tests to check
if the observed distribution differed from the expected
distribution, whereby a small departure from the expected
indicates lack of preference.
other hosts, and this was strongly associated with infection by S. flexicaulis.
The observed frequency of infected hosts was different from the expected, both using abundance (²= 714.2,
df = 11, p < 0.001) and plant cover (²= 209.2, df = 11,
p < 0.001). Not all hosts contributed equally to this outcome. Regarding relative abundance, most of the observed
infected proportions were close to the expected values,
with notable exceptions: M. calodendron was infected
249% more than expected, whereas M. daphnoides and T.
heteromalla were, respectively, 64% and 68% less infected
than expected (Fig. 1). These ‘preference’ results differed
from those of relative cover, due to the size of individual
plants, even within a single species. Consequently, when
host cover was used, the number of infected M. daphnoides
and T. heteromalla was very close to the expected, M. calodendron was 89% more infected, and L. pinaster was 55%
less parasitized than expected (Fig. 2).
Results
The 10,290 individuals in the sampled area belonged
to 24 families and 42 species (Tab. S1 in supplementary
material). The more frequent families were Asteraceae
(eight spp.), Melastomataceae (five spp.), and Velloziaceae
and Orchidaceae (four spp. each). The four more abundant
species were Cattleya caulescens (Orchidaceae, 1491 ind.),
Microstachys daphnoides (Euphorbiaceae, 1130 ind.),
M. calodendron (Fabaceae, 858 ind.) and Lychnophora
pinaster (Asteraceae, 806 ind.).
Fifteen species had a relative abundance > 1% in the
community, of which 12 had signs of parasitism (Tab. 1).
The most infected species were the shrubby eudicots
M. calodendron and L. pinaster. The monocots Cattleya
caulescens, Acianthera teres and Vellozia graminea had no
infected individuals. The proportion of non-infected
dead plants (7%) was significantly lower than that of infected individuals (83%) (²= 1102. 4, df = 1, p < 0.001).
Overall, more than 80% of deaths among individuals of
the 12 host species analysed were related to parasitism.
However, the number of dead infected individuals varied
considerably among hosts. For instance, of 164 dead plants
of M. calodendron, 139 showed mistletoe vestiges, while
M. daphnoides, one of the most abundant species, had only
one dead infected individual (Tab. 1). Mimosa calodendron
had a much larger proportion of dead individuals than the
Discussion
The preference of S. flexicaulis for M. calodendron was
evident. The fact that M. calodendron was among the
most abundant and also occupied the largest cover in the
community indicates dominance over the other species.
Being a legume growing in a nutrient-poor environment,
this species has advantage as a competitor. It was therefore expected that, if only by its relative abundance, a
large number of M. calodendron plants would be infected.
Comparison with other hosts, however, showed that the
association between both species goes beyond how well
represented the legume is in the community.
Table 1. Species with relative abundance above 1% and parasitized. Columns represent the number of individuals in each category: not parasitized (NP) or
parasitized (P), dead or alive. Species were ranked according to decreasing abundance values. Cattleya caulescens, Acianthera teres (Orchidaceae), and Vellozia
graminea (Velloziaceae) had relative abundance > 1% in the plant community but were excluded from this list because they did not have parasitized individuals.
Live
Dead
Species
NP
P
NP
P
Microstachys daphnoides
1106
26
3
1
Mimosa calodendron
542
164
13
139
Lychnophora pinaster
696
97
7
6
Tibouchina heteromalla
726
24
0
0
Stachytarpheta glabra
357
24
0
1
Symphyopappus brasiliensis
363
4
1
0
Vellozia compacta
282
14
0
1
Eriope macrostachya
185
16
0
1
Borreria capitata
195
5
0
0
Baccharis reticularia
132
26
5
4
Croton serratoideus
133
1
1
0
Chromolaena multiflosculosa
89
1
0
0
4806
402
30
153
Total
Acta Botanica Brasilica - 30(1): 41-46. January-March 2016
43
Fabiana Alves Mourão, Rafael Barros Pereira Pinheiro, Claudia Maria Jacobi and José Eugênio Côrtes Figueira
Figure 1. Expected and observed parasitism based on the relative abundance of each species. Bars are the 95% CI. Bca = Borreria capitata; Bre = Baccharis reticularia; Cmu = Chromolaena multiflosculosa; Cse = Croton serratoideus; Ema = Eriope macrostachya; Lpi = Lychnophora pinaster; Mca = Mimosa calodendron; Mda =
Microstachys daphnoides; Sbr = Symphyopappus brasiliensis; Sgl = Stachytarpheta glabra; The = Tibouchina heteromalla; Vco = Vellozia compacta.
Figure 2. Expected and observed parasitism based on the relative cover of each species. Bars are the 95% CI. Bca = Borreria capitata; Bre = Baccharis reticularia;
Cmu = Chromolaena multiflosculosa; Cse = Croton serratoideus; Ema = Eriope macrostachya; Lpi = Lychnophora pinaster; Mca = Mimosa calodendron; Mda = Microstachys daphnoides; Sbr = Symphyopappus brasiliensis; Sgl = Stachytarpheta glabra; The = Tibouchina heteromalla; Vco = Vellozia compacta.
Other factors that may increase the strength of this
interaction are related to the two types of dispersal that
the mistletoe shows: vegetative and by birds. In the study
area M. calodendron is one of the tallest shrubs and can get
as high as 1.60 m. Its hemispherical, branched crown is
make this species one of the few suitable perching options
for the birds that disperse the mistletoe seeds. In addition,
because of its high density, the probability increases of
receiving branches of the parasite coming from neighbor
infected plants where they resume xylem-tapping (Mourão
2012). The vegetative dispersal is more successful when
hosts are close and have a similar height (Aukema 2003;
Mourão 2012).
44
Compared to the other 11 hosts, M calodendron was
much more parasitized than expected, whether estimating
the infection by its abundance or cover. Lychnophora pinaster represented the only example of less infection than
expected by its relative cover. This species has very flexible
branches that spread across the substrate and individuals
were rarely taller than 1 m, so its architecture is not suitable for bird perching or shelter. Because birds prefer to
perch on plants that rise above the others (Robinson &
Holmes 1984), only a handful of species would be more
frequently visited, among which M. calodendron.
Mortality of the plants in the community, particularly
in M. calodendron, was directly caused or enhanced when in
Acta Botanica Brasilica - 30(1): 41-46. January-March 2016
Host preference of the hemiparasite Struthanthus flexicaulis (Loranthaceae)
in ironstone outcrop plant communities, southeast Brazil
association with S. flexicaulis. Contrary to our predictions,
the mortality rate of infected M. calodendron was the highest among hosts. This suggests that besides being infected
more frequently it is likely that individuals are parasitized
with more intensity. A feasible explanation is that more
seeds are deposited on account of more frequent bird visits. Additionally, because it is a high-quality resource, it
favours the parasite’s growth, as suggested by Kelly (1990).
High levels of infestation allied to edapho-climatic conditions in canga outcrops may impose a severe stress on the
host, and even death (Mourão et al. 2009). Parasitic plants
may inflict several types of damages to their hosts, notably
leaf biomass reduction (Press & Graves 1995; Cameron et
al. 2008), usually leading to decreased photosynthetic rates
(Graves et al. 1992), which may result in less flower output
(Mugabe 1983). When intensely infected, M. calodendron
loses from 75% to 95% of its foliage, followed by a steep
reduction in the number of all reproductive structures
(Mourão et al. 2009). Hence, mistletoe infection would
act as a population control mechanism of M. calodendron,
a nitrogen-fixing species with competitive advantage in
environments with serious nutritional restrictions.
The evolution of host specificity in plant communities
is highly correlated with the development of ecological
dominance (Barlow & Wiens 1977). Although M. calodendron is not the most abundant species in the area, it does
have the largest foliage cover in the community, granting
the necessary proximity for the branches of the mistletoe
to reach new hosts. The marked preference of S. flexicaulis
for this host is the result of a combination of factors of
both species that increase infestation opportunities and
reinforce their interaction.
Acknowledgements
Research funding was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)
and Fundação de Amparo à Pesquisa do estado de Minas
Gerais (FAPEMIG). We thank IEF for the research and
collection license, and the staff of Rola Moça State Park
for logistic support. FAM thanks CNPq for her doctorate
scholarship; CMJ holds a CNPq research productivity
scholarship. We are also grateful for the valuable comments
of two anonymous reviewers.
References
Arruda R, Carvalho LN, Del-Claro K. 2006. Host specificity of a Brazilian
mistletoe, Struthanthus aff. polyanthus (Loranthaceae), in cerrado
tropical savanna. Flora 201: 127-134.
Aukema JE. 2003. Vectors, viscin, and Viscaceae: mistletoes as parasites,
mutualists and resources. Frontiers in Ecology and the Environment
1: 212-219.
Aukema JE, Rio CMM. 2002. Where does a fruit-eating bird deposit
mistletoe seeds? Seed deposition patterns and an experiment.
Ecology 83: 3489-3496.
Barlow BA, Wiens D. 1977. Host-parasite resemblance in Australian
mistletoes: the case for cryptic mimicry. Evolution 31: 69-84.
Bowie M, Ward D. 2004. Water and nutrient status of the mistletoe
Plicosepalus acaciae parasitic on isolated Negev Desert populations
of Acacia raddiana differing in level of mortality. Journal of Arid
Environments 56: 487-508.
Cameron DD, Geniez JM, Seel WE, Irving LJ. 2008. Suppression of host
photosynthesis by the parasitic plant Rhinanthus minor. Annals of
Botany 101: 573-578.
Carmo FF, Jacobi CM. 2012. Vascular plants on cangas. In: Jacobi CM,
Carmo FF. (eds.) Diversidade florística nas cangas do Quadrilátero
Ferrífero. Belo horizonte, IDM Ltda. p. 43-50.
Dzerefos CM, Witkowski ETF, Shackleton CM. 2003. Host-preference and
density of woodrose-forming mistletoes (Loranthaceae) on savanna
vegetation, South Africa. Plant Ecology 167: 163-177.
Graves JD, Press MC, Smith S, Stewart GR. 1992. The carbon economy of
the association between cowpea and the parasitic angiosperm Striga
gesnerioides. Plant, Cell and Environment 15: 283-288.
Jacobi CM, Carmo FF, Vincent RC, Stehmann JR. 2007. Plant communities on ironstones outcrops: a diverse and endangered Brazilian
ecosystem. Biodiversity and Conservation 16: 2185-2200.
Kelly KC. 1990. Plant foraging: a marginal value model and coiling response in Cuscuta subinclusa. Ecology 71: 1916-1925.
Lemaitre A, Troncoso A, Niemeyer H. 2012. Host preference of a temperate mistletoe: Disproportional infection on three co-occurring
host species influenced by differential success. Austral Ecology 37:
339-345.
Medel R, Botto-Mahan C, Smith-Ramírez C, et al. 2002. Historia natural
cuantitativa de una relación parásito-hospedero: el sistema Tristerix-cactáceas en Chile semiárido. Revista Chilena de Historia Natural
75: 127-140.
Mourão FA. 2012. Dinâmica do forrageamento da hemiparasita Struthanthus flexicaulis Mart. (Loranthaceae) e sua influência na estrutura da
comunidade vegetal de campos rupestres ferruginosos – MG. PhD
Thesis, Universidade Federal de Minas Gerais, Brazil.
Mourão FA, Carmo FF, Ratton P, Jacobi CM. 2006. Hospedeiras da hemiparasita Struthanthus flexicaulis Mart. (Loranthaceae) em campos rupestres ferruginosos, Quadrilátero Ferrífero, MG. Lundiana 7: 103-110.
Mourão FA, Jacobi CM, Figueira JEC, Batista EKL. 2009. Effects of the
parasitism of Struthanthus flexicaulis (Mart.) Mart. (Loranthaceae)
on the fitness of Mimosa calodendron Mart. (Fabaceae), an endemic
shrub from rupestrian fields over ironstone outcrops, Minas Gerais
State, Brazil. Acta Botanica Brasilica 23: 820-825.
Mugabe NR. 1983. Effects of Alectra vogelli Benth on cowpea (Vigna
unguiculata (L.) Walp). Some aspects on reproduction of cowpea.
Zimbabwe Journal of Agricultural Research 21: 135-147.
Norton DA, Carpenter MA. 1998. Mistletoes as parasites: host specificity and speciation. Trends in Ecology and Evolution 13: 101-105.
Norton DA, Lange PJ. 1999. Host specificity in parasitic mistletoes
(Loranthaceae) in New Zealand. Functional Ecology 13: 552-559.
Porto ML, Silva MFF. 1989. Tipos de vegetação metalófila em áreas da
Serra de Carajás e de Minas Gerais. Acta Botanica Brasilica 3: 13-21.
Press MC, Graves JD. 1995. Parasitic plants. London, Chapman & Hall.
Press MC, Phoenix GK. 2005. Impacts of parasitic plants on natural
communities. New Phytologist 166: 737-751.
Radomiljac AM, McComb JA, Pate JS. 1999. Gas exchange and water
relations of the root hemiparasite Santalum album L. in association
with legume and non-legume hosts. Annals of Botany 83: 215-224.
Reis Jr FB, Simon MF, Gross E, et al. 2010. Nodulation and nitrogen fixation by Mimosa spp. in the Cerrado and Caatinga biomes of Brazil.
New Phytologist 186: 934-946.
Rizzini CT. 1997. Tratado de Fitogeografia do Brasil: Aspectos Ecológicos,
Sociológicos e Florísticos. 2nd. edn. Rio de Janeiro, Âmbito Cultural
Edições Ltda.
Robinson SK, Holmes RT. 1984. Effects of plant species and foliage structure on foraging behavior of forest birds. The Auk 101: 672 - 684.
Rodl T, Ward D. 2002. Host recognition in a desert mistletoe: early
stages of development are influenced by substrate and host origin.
Functional Ecology 16: 128-134.
Acta Botanica Brasilica - 30(1): 41-46. January-March 2016
45
Fabiana Alves Mourão, Rafael Barros Pereira Pinheiro, Claudia Maria Jacobi and José Eugênio Côrtes Figueira
Roxburgh L, Nicolson SW. 2005. Patterns of host use in two African
mistletoes: the importance of mistletoe-host compatibility and avian
disperser behaviour. Functional Ecology 19: 865-873.
Runyon JB, Mescher MC, Moraes CM. 2006. Volatile chemical cues
guide host location and host selection by parasitic plants. Science
313: 1964-1967.
46
Teixeira WA, Lemos-Filho JP. 2002. Fatores edáficos e a colonização de
espécies lenhosas em uma cava de mineração de ferro em Itabirito,
Minas Gerais. Revista Árvore 26: 25-33
Viana PL, Lombardi JA. 2007. Florística e caracterização dos campos
rupestres sobre a canga na Serra da Calçada, Minas Gerais, Brasil.
Rodriguésia 58: 159-177.
Acta Botanica Brasilica - 30(1): 41-46. January-March 2016