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ڽڼہڼڼڼڿڽۀۀڿۀڿڿھڼۑ
ۙۦۙۜڷ۟ۗ۠Өڷۃڷۣۧۢۧۧۡۦۙێڷۨۧۙ۩ۥۙې
ۀڽڼھڷۤۙۑڷڽڽڷۣۢڷہڽғڽڿғھڿھҢҢғڽڷۃۧۧۙۦۘۘٷڷێٲڷۃۍېےۛҖۦۣۘۛۙғۦۖۡٷۗ۠ۧғٷۢۦ۩ۣ۞ҖҖۃۤۨۨۜڷۣۡۦۚڷۘۙۘٷۣۣ۠ۢ۫ө
Journal of Tropical Ecology (2014) 30:153–163. © Cambridge University Press 2013
doi:10.1017/S0266467413000801
Reciprocal transplant experiment suggests host specificity of the mistletoe
Agelanthus natalitius in South Africa
Desale Y. Okubamichael1 , Megan E. Griffiths and David Ward
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville 3209, Pietermaritzburg, South Africa
(Received 9 September 2013; revised 11 November 2013; accepted 11 November 2013; first published online 13 December 2013)
Abstract: We surveyed the community composition of trees that host the mistletoe Agelanthus natalitius (Loranthaceae)
at two sites (Highover and Mtontwane) in South Africa. We recorded a total of 1464 trees (Acacia karroo and A. caffra)
hosting 1202 mistletoes in the 64 surveyed plots (20 × 50 m). There were almost four times as many A. karroo as A.
caffra at Highover and three times as many A. karroo as A. caffra at Mtontwane. There was no significant difference
in prevalence (percentage of infected trees) at Highover (A. karroo = 22% and A. caffra = 26%), but a significantly
greater percentage of A. caffra trees were parasitized at Mtontwane (A. karroo = 25% and A. caffra = 34%). Intensity
of infection (number of mistletoe infections per tree) was higher for A. karroo (0.73 ± 0.04 and 1.03 ± 0.64) than
for A. caffra (0.66 ± 0.01 and 0.89 ± 0.035) at Highover and Mtontwane, respectively. Prevalence and intensity
of infection showed a significant positive relationship with tree size for both host species at both sites. We tested the
genotype-by-environment interaction effects in this mistletoe by conducting reciprocal transplant experiments (64
individual trees each received 20 seeds). Initial germination was not site-, substrate- or host-sensitive. However, a
general pattern was found that hypocotyls of the germinated seeds grew longer when seeds were placed on the same
host species as the parent plant within their own source locality. Consistent with this observation, mistletoes placed
on their source host species generally had higher survival than those transferred to non-source host species after 6
mo. Overall, mistletoe seeds from parent plants on A. karroo and mistletoe seeds placed on A. karroo had the highest
survival. This could be the result of an adaptation of the mistletoe to the most frequently encountered host species.
Key Words: Adaptive phenotypic plasticity, Acacia caffra, Acacia karroo, Agelanthus natalitius, coevolution, G × E
interactions, prevalence, intensity, host specificity, reaction norms
INTRODUCTION
Mistletoes comprise a diverse group of hemiparasitic
flowering plants that have become specialized to access
nutrients and water from host trees via a haustorium
(Stewart & Press 1990). Mistletoes vary widely in their
degree of host specificity, ranging from extreme specialists
that parasitize a single host species to generalists that use
many different host species with no apparent infection
difference among host species (Dean et al. 1994, Norton
& Carpenter 1998, Norton & de Lange 1999). In some
mistletoe species, host infection varies geographically
such that at a given location a mistletoe species may
infect only part of its potential host set (Okubamichael
et al. 2011a, Rödl & Ward 2002, Thorogood et al. 2009).
It could be argued that mistletoes use the most abundant
1
Corresponding author. Email: dessu81@gmail.com
trees in the community simply because there are few
alternatives (neutral interactions governed by species
abundance) but a mechanism of host adaptation is still
required. The factors that explain why mistletoe species
only infect a subset of the available host species in a given
locality are not clear.
Host specificity in mistletoes is a composite measure of
relative abundance of mistletoes on the parasitized host
species (Mathiasen et al. 2008). Differential parasitism of
mistletoes of the available host species is often expressed
as host preference (i.e. only a subset of host trees are
infected). Host compatibility at the genetic, mechanical,
physiological and biochemical level are most likely to
affect the growth and survival of mistletoes on host trees,
subsequently determining host preference in mistletoes
(Fadini 2011, Okubamichael et al. 2011a, Yan 1993a,
Yan & Reid 1995). Host preference may not be necessarily
driven by traits of host trees that directly affect the
growth and survival of mistletoes. For example, birds
154
DESALE Y. OKUBAMICHAEL, MEGAN E. GRIFFITHS AND DAVID WARD
may influence seed dispersal patterns and thus affect host
preference in mistletoes. It is therefore crucial to quantify
the differential parasitism of mistletoes in the field and to
test host compatibility.
Genotype performance across environments can be
reflected in reaction norms tested by an interaction effect
in analysis of variance (Lynch & Walsh 1998). If the
genotypic responses to environmental changes of two
or more reaction norms are non-parallel, it indicates a
genotype by environment (G × E) interaction (Japhet
et al. 2009). In this particular study, we tested the
contribution of G × E interactions to local adaptation
of mistletoes on host species at a specific site by means of
reciprocal transplant experiments in two combinations of
mistletoe–host populations, using hypocotyl length and
survival as indices of growth performance. The growth
of the hypocotyl – the structure that eventually forms
the haustorium – is hypothesized to be an essential trait
determining the establishment success of parasitic plants
(Yoder 1999).
The aims of this study were to quantify the degree of
host specificity and to evaluate the factors that determine
the local distribution and specialization of the mistletoe
Agelanthus natalitius (Loranthaceae) in two populations
in South Africa. We predicted that host recognition and
preference occurs during the early developmental stages
of germination and haustorium formation in mistletoes
and would be reflected in differential survival of mistletoes.
parasite’s range suggests that A. natalitius may be locally
specialized on particular host species.
Field survey
Host composition was assessed by quantifying the
tree community in the two study sites (Highover and
Mtontwane). We randomly selected and surveyed 64 plots
(32 plots in each site) (20 × 50 m). We identified all
tree species in each plot; any species that had at least
one infected tree in the study site was recorded as a
host species. We counted the number of mistletoes on
each tree and measured tree size (height and diameter)
because it may be an important parameter in determining
the infection pattern of mistletoes among host trees
(Overton 1994, Roxburgh & Nicolson 2007, Ward et al.
2006). Tree height was measured with a measuring
pole; if the tree was inclined or growing on a slope,
trigonometric calculations were applied to determine
tree height from the ground. Diameter at breast height
(dbh) of the trunk was measured approximately 1.5 m
above the base of the stem; in the case of multi-stemmed
trees the following calculation was used: (dbh = SQRT
[sum (stem diameter2 )]). Trees below 2 m in height and
< 3 cm in diameter were excluded, because these were
never parasitized by a mistletoe (pers. obs.).
Reciprocal transplant germination experiment
METHODS
Study sites and species
We surveyed the tree community and the population
distribution of the mistletoe Agelanthus natalitius in
two sites approximately 110 km apart in KwaZuluNatal, South Africa: Highover (29°54′ S, 30°05′ E) and
Mtontwane (28°48′ S, 29°56′ E). Highover is a privately
owned nature reserve 25 km south-west of Richmond and
Mtontwane is a game ranch adjacent to Weenen Game
Reserve. The vegetation of Mtontwane is characterized by
Acacia caffra, A. karroo, A. tortilis and A. nilotica woodlands
and thickets. The vegetation of Highover is characterized
by A. karroo, A. caffra and A. ataxacantha woodlands and
thickets, with a denser vegetation and steeper terrain than
at Mtontwane.
Agelanthus natalitius is widely distributed throughout
southern Africa (Polhill & Wiens 1998, Visser 1981).
This mistletoe species parasitizes at least 11 tree genera,
including Acacia, Carya, Citrus, Combretum, Dichrostachys,
Dombeya, Grewia, Pterocarpus, Punica, Sclerocarya and
Terminalia (Visser 1981, Wiens & Tölken 1979). However,
geographic variation in the infection patterns over the
We carried out field reciprocal transplant germination
experiments using seeds of mistletoes parasitizing the two
main host species, A. karroo and A. caffra, in our two
field sites. First, we bagged unripe mature fruits using
nylon mesh bags to protect fruits from bird consumption
1 mo prior to collection. To avoid pseudoreplication, we
randomly selected 20 individual mistletoes in different
host trees from each of the two main host species in both
sites. We collected fully ripe and undamaged fruits by
hand picking. For each seed used for the experiment,
we manually removed the exocarp (pulp cover) and
endocarp (the skin covering the seed). This is essential
because the layers covering the seed can act as barriers
to germination in mistletoes (Ladley & Kelly 1996,
Okubamichael et al. 2011b). Furthermore, this enables
the sticky viscin surrounding the seed to be exposed,
which facilitates the temporary attachment of mistletoe
seeds to host branches. We worked the viscin by hand to
increase its stickiness (for a similar method, see Ladley &
Kelly 1996, Sargent 1995).
We used non-parasitized individual trees in our
experiment to avoid any effects of previous infection and
susceptibility. Trees ranged in height from 2–6 m and
were all located in open areas to avoid shade effects
Host specificity of the mistletoe Agelanthus natalitius
(Okubamichael et al. 2011b). We monitored a total of
64 individual trees that were marked at Mtontwane and
Highover. For each host species in each site we had two
groups: one group received seeds of mistletoes obtained
from A. caffra and the other group from A. karroo. Each
group consisted of eight trees. For each experimental tree,
we selected two healthy branches at the same position
within the canopy and of similar size (8–12 cm girth,
although mistletoes are capable of growing on much
smaller twigs). Twig size was based on the optimal size
for seedling establishment based on previous studies in
this particular mistletoe species. In addition, this host twig
size enabled us to inoculate many seeds on a single twig.
Most importantly, if many seeds had established during
the experiment, this branch size would maintain many
seeds better than smaller twigs that would not withstand
high infection of mistletoes (Sargent 1995). Each branch
received 10 seeds linearly orientated and placed 3 cm
apart; of these, five seeds were from Highover and five
seeds from Mtontwane. Each seed was marked with a
distinctly coloured pin. We applied a paired design (one
local and one non-local seed) for each pair to experience
identical environmental conditions including the current
host species, bark surface and branch diameter (Rödl &
Ward 2002).
We monitored the seed germination, hypocotyl growth
and survival after 1 wk, after 1 mo and after 6 mo
at both sites. At each time period we recorded the
condition of each seed as germinated (indicated by
protrusion of the fresh green seed embryo), dead (where
colour had changed to black and the seed had become
dried and shrivelled) or lost in situ. Where germination
occurred we measured hypocotyl length from the base
of the viscin layer to the distal end of the protruded
hypocotyl. Hypocotyls that curved towards the substrate
and attached to the host substrate were considered to have
successfully established because the haustorium will form
in this position. However, if the hypocotyls grow away
from the host bark they do not attach to the host and do
not become successfully established. The experiment was
designed to test the G × E interactions in response to site,
source and current substrate while other abiotic factors
were equivalently experienced by mistletoe seeds.
Statistical analysis
Host species and germination (expressed as the
percentage of seeds that germinated) were analysed
for differences in frequency using χ 2 tests (SPSS 18.0
for Windows). The difference in prevalence (i.e. the
percentage of individual trees carrying at least a single
mistletoe infection) between host species and correlations
of prevalence with tree height and dbh were tested using
binary logistic regression. We also tested prevalence
155
of grouped host trees with height (1-m class width)
and with dbh (10-cm class width) after prevalence
was arcsine-square root-transformed. The relationship
between intensity of infection and tree height and trunk
dbh was further analysed with GLIM, as the frequency
distribution of parasitism among the two host species
followed a negative binomial distribution (Krebs 1989)
(variance/mean = 6.30/0.79 and k = 0.16, N = 1464,
χ 2 for goodness of fit = 9.17, df = 3, P = 0.027). We
used ANOVA to test the differences among host species
in mean height and dbh, as well as among infected and
uninfected trees in mean height and dbh. We used ANOVA
to test the effect of site, source, current substrate and
time on hypocotyl length in the mistletoe seedlings (SPSS
18.0 for Windows). Significant interactions in an ANOVA
indicate that the reaction norms are not parallel (i.e. that
there is a G × E interaction). We performed Kaplan–Meier
survival analysis (Kaplan & Meier 1958, SPSS 18.0 for
Windows) for the 6-mo period. When overall significance
was confirmed we did a pairwise comparison and a new
alpha value was computed to account for the Bonferroni
correction. We fitted a sigmoid curve to determine the
effect of hypocotyl length within 6 mo on survival of the
mistletoe seedlings.
RESULTS
Field survey
At the two study sites, five host species were recorded as
being parasitized by the mistletoe Agelanthus natalitius,
namely Acacia caffra, Acacia karroo, Acacia tortilis,
Acacia nilotica and Leucaena leucocephala (all Fabaceae;
nomenclature after Van Wyk & Van Wyk 1997). Acacia
tortilis, A. nilotica and L. leucocephala were excluded from
further analyses because these species were either rare
in the study sites or had few infected individuals. Acacia
tortilis was absent in Highover and only one A. nilotica was
recorded in the survey plots at that site. Similarly, only two
individuals of L. leucocephala were recorded in a single plot
at Highover, both of which were infected. At Mtontwane,
only a few individuals of A. nilotica (N = 3) and A. tortilis
(N = 9) were infected, each supporting a single Agelanthus
natalitius individual. Thus, all statistical analyses were
applied to the two most common host species, A. karroo
and A. caffra, which grow abundantly at both sites and
were recorded with many trees infected by Agelanthus
natalitius.
We recorded a total of 1464 trees (Acacia karroo and
A. caffra) hosting 1202 Agelanthus natalitius mistletoes
in the 64 surveyed plots at the two sites (Highover
and Mtontwane). Acacia karroo was significantly more
abundant than A. caffra at both sites; there were almost
four times as many A. karroo as A. caffra at Highover
156
DESALE Y. OKUBAMICHAEL, MEGAN E. GRIFFITHS AND DAVID WARD
Table 1. Chi-square test on the frequency of two tree species (Acacia
karroo and A. caffra) that are hosts of the mistletoe Agelanthus natalitius
at two sites (Highover and Mtontwane). Acacia karroo was significantly
higher in abundance than A. caffra in both sites (N = 1464).
Source of variation
df
χ2
P
Site
Species
Species in Highover
Species in Mtontwane
1
1
1
1
4.8
421
278
150
0.029
<0.001
<0.001
<0.001
Table 2. Generalized linear model test results for the
prevalence of infection (% of trees with a mistletoe infection)
of two host species (Acacia karroo and A. caffra) in two sites
(Highover and Mtontwane) (N = 1464).
Source of variation
df
Wald χ 2
P
Site
Species
Site × species
1
1
1
3.6
5.5
0.6
0.06
0.02
0.43
Table 3. Generalized linear model test results for the intensity of
mistletoe infection (mean number of parasites per tree) for two host
species at two sites. Intensity of infection was significantly higher
on A. karroo than on A. caffra (N = 1464 trees parasitized by 1202
mistletoes).
Source of variation
df
Wald χ 2
P
Species
Site
Species × site
1
1
1
11.2
0.047
1.88
0.024
0.829
0.171
and three times as many A. karroo as A. caffra at
Mtontwane (Table 1). There was no significant difference
in prevalence of mistletoe infection on the two host species
at Highover (prevalence of A. karroo = 22% and A. caffra
= 26%), but a significantly greater percentage of A. caffra
trees were parasitized at Mtontwane (A. karroo = 25% and
A. caffra = 34%) (Table 2). Infection intensity (number
of mistletoes per tree) was higher for A. karroo (0.73 ±
0.04 and 1.03 ± 0.64 mistletoes per tree) than for A.
caffra (0.66 ± 0.01 and 0.89 ± 0.035 mistletoes per tree)
at Highover and Mtontwane, respectively (Table 3). At
Highover, infected trees of A. karroo had an average of
3 mistletoes per infected tree as compared with 2.5 per
infected tree for A. caffra. At Mtontwane, infected trees of
A. karroo had an average of 4 mistletoes per infected tree as
compared with 2.5 per infected tree of A. caffra. If we had
excluded the two highly infected trees at Highover and
one at Mtontwane that many mistletoe-dispersing birds
used for nesting (pers. obs.), the number of mistletoes per
infected tree of A. caffra would drop to 1.
There was no significant difference (species, site and
species × site) in tree height (range in Wald χ 2 = 0.001–
0.074, range in P = 0.786–0.927, N = 1464) and
trunk dbh (range in Wald χ 2 = 2.8–6.3, range in P =
Table 4. GLIM of test for the height and diameter at breast height (dbh)
of infected and uninfected trees (status) of two host species (Acacia karroo
and A. caffra) at two sites (Highover or Mtontwane).
Height
Source of variation
df
Species
1
Site
1
Status
1
Species × site
1
Species × status
1
Site × status
1
Site × species × status
1
Error degrees of freedom 1464
dbh
Wald χ 2
P
Wald χ 2
P
0.2
107
63.7
5.0
0.3
10.4
0.2
0.697
<0.001
<0.001
0.025
0.584
0.001
0.656
0.2
14.8
68.6
1.8
2.6
5.6
0.1
0.642
<0.001
<0.001
0.176
0.109
0.018
0.706
0.227–0.435, N = 1464) between A. karroo and A. caffra
trees at either site. However, the mean height and trunk
dbh of infected trees were significantly greater than for
uninfected trees for both species in both sites (Table 4,
Figure 1). The logistic regression analysis indicated that
both height and dbh had a significant positive effect on the
probability of infection (slopes for prevalence and height
ranged from 0.38–0.85, range in Wald χ 2 = 12–40,
P < 0.001, range in N = 157–622). A similar result
was obtained for dbh, although there was a lower slope
(slopes for prevalence and dbh ranged from 0.050–0.096,
range in Wald χ 2 = 5–41, P < 0.001, range in N = 157–
622). Prevalence of grouped trees was the proportion of
infected trees in the given class. Prevalence was positively
correlated with height (1-m class width) and with dbh
(10-cm class width) (results after prevalence was arcsinesquare root-transformed, height, range in r = 0.90–0.95,
range in F = 17–40, P < 0.05, range in N = 157–622;
and dbh, range in r = 0.90–0.97, range in F = 12–50, P <
0.05, N = 157–622). However, the dbh class of A. caffra at
Highover was not significantly positively correlated with
prevalence (r = 0.50, F = 1.00, P = 0.39, N = 157)
(Figure 2).
The distribution of Agelanthus natalitius among host
trees was strongly aggregated, meaning that most
potential hosts were not infected, while a few individual
host trees were highly infected and supported most of
the parasites (e.g. we observed a single host tree with
56 mistletoes in our study). The GLIM analysis showed
that the number of mistletoes per host tree (infection
intensity) had a positive significant relationship with tree
height (range in slopes = 0.30–0.70, P < 0.001, range
in N = 157–622). A similar result was obtained for dbh,
although with a lower slope (range in slopes = 0.024–
0.032, P < 0.001, range in N = 157–622).
Reciprocal transplant germination experiment
Germination of Agelanthus natalitius seeds started within
1 d in both sites and reached 100% after 1 wk, independent
Host specificity of the mistletoe Agelanthus natalitius
(a) Height
7
N = 1464
Tree height (m)
6
Infected
Uninfected
5
4
3
2
1
0
A. karroo A. caffra
Highover
A. karroo A. caffra
Mtontwane
(b) Diameter at breast height
157
Table 5. GLIM of the reciprocal transplant experiment of Agelanthus
natalitius. Site = Highover or Mtontwane; Source = source (original)
host species; Current substrate = host that the mistletoe was transferred
to manually.
Source of variation
df
Current substrate
1
Site
1
Source
1
Time
1
Current substrate × site
1
Current substrate × source
1
Current substrate × time
1
Site × source
1
Site × time
1
Source × time
1
Current substrate × site × source
1
Current substrate × site × time
1
Current substrate × source × time
1
Site × source × time
1
Current substrate × site × source × time
1
Error degrees of freedom
1206
Wald χ 2
P
102
23.9
77.3
17.2
3.9
19.6
0.6
75.4
0.1
0.3
53.6
0.1
1.0
1.7
0.6
<0.001
<0.001
<0.001
<0.001
0.049
<0.001
0.451
<0.001
0.722
0.559
<0.001
0.796
0.339
0.195
0.446
Tree diameter at breast height (cm)
80
N = 1464
Infected
Uninfected
60
40
20
0
A. karroo
A. caffra
Highover
A. karroo
A. caffra
Mtontwane
Figure 1. Height (a) and diameter at breast height (b) (mean ± SE) of
host trees Acacia karroo and Acacia caffra infected and uninfected by the
mistletoe Agelanthus natalitius at Highover and Mtontwane.
of host substrate and site. Within the first mo, 7% of
the germinated seeds of A. natalitius were unsuccessful
(either they died or were lost in situ) and there was
no significant difference in germination success whether
they were placed on a source or non-source host species
and whether they had been translocated to a different
site or were germinated within their locality (χ 2 = 5,
P = 0.78, N = 1280). In this case, we compared eight
combinations at each site. In contrast to germination
success, hypocotyl length was significantly influenced
by the three-way interactions (site × source × current
substrate). This is important to note because it reflects the
presence of genotype × environment (G × E) interactions
(Table 5).
At Highover, mistletoe seeds placed on the same current
substrate as their source host within their site grew
significantly longer hypocotyls than those transferred
to non-source hosts, except for mistletoes on Acacia
karroo (Figure 3a). There was an unidentified pathogen
on mistletoe seeds placed on A. karroo in Highover and we
suspect that this resulted in very short hypocotyl growth
of these mistletoes (Figure 3a). As a result, mistletoes from
A. karroo at Highover that were placed on A. karroo at
Highover grew much shorter hypocotyls than mistletoes
from A. karroo at Mtontwane that were placed on A. karroo
at Highover (Figure 3a).
In Mtontwane, mistletoe seeds placed on the same
current substrate as their source host within the same
site grew the longest hypocotyls (Figure 3b). Mistletoe
seeds obtained from Acacia caffra and placed on A. karroo
within the same site had longer hypocotyls than those
obtained from A. karroo at Highover (Figure 3b). Similarly,
mistletoes obtained from A. karroo hosts but placed on A.
caffra within the same site grew longer hypocotyls than
those obtained from Highover.
Overall, if substrate only was compared, mistletoe seeds
placed on A. karroo had longer hypocotyls than mistletoe
seeds placed on A. caffra at Highover and Mtontwane
(Figures 3). For mistletoes that were transferred within a
site, mistletoes from A. karroo grew less on A. caffra while
mistletoes from A. caffra placed on A. karroo grew much
longer hypocotyls in both sites.
The number of hypocotyls that curved towards and
contacted the host substrate was also higher when
mistletoe seeds were placed on the source host species
(χ 2 = 97, P < 0.01, N = 309). In this case, we also
compared the eight combinations at each site. Even when
we excluded source and site effects by considering current
host substrate only we found that the hypocotyls of
mistletoe seedlings attached to the host substrate more
frequently on A. karroo (χ 2 = 28, P < 0.01, N = 309).
158
DESALE Y. OKUBAMICHAEL, MEGAN E. GRIFFITHS AND DAVID WARD
(b) Mtontwane
(a) Highover
1.0
1.0
N = 781
N = 585
0.8
Prevalence
Prevalence
0.8
0.6
0.4
0.2
0.6
0.4
0.2
0.0
0.0
2-3
3-4
4-5
5-6
6-7
7-8
2-3
3-4
Height class (m)
(c) Highover
5-6
6-7
7-8
(d) Mtontwane
1.0
1.0
N = 781
N = 585
0.8
0.8
Prevalence
Prevalence
4-5
Height class (m)
0.6
0.4
0.2
0.6
0.4
0.2
0.0
0.0
3 - 13
13 - 23
23 - 33
33 - 43
43 - 53
dbh (cm)
3 - 13
13 - 23
23 - 33
33 - 43
43 - 53
dbh (cm)
Figure 2. Prevalence of the mistletoe Agelanthus natalitius against tree height and dbh of the two host species, Acacia karroo (solid circles with solid
regression line) and Acacia caffra (hollow circles and dashed regression line). (a) Prevalence against tree height at Highover, (b) prevalence against
tree height at Mtontwane, (c) prevalence against dbh at Highover and (d) prevalence against dbh at Mtontwane. All were significantly positively
correlated with the exception of prevalence of A. caffra, which was not significantly correlated with tree dbh at Highover.
Hypocotyl length over 6 mo was positively correlated with
the probability of survival of mistletoe seedlings (r = 0.95,
F1, 8 = 57.5, P < 0.001) (Figure 4).
Survival
A log-rank test showed that overall survival curves
showed significant differences across all 16 combinations
over 6 mo (χ 2 = 51.3, P < 0.001, df = 15). Three groups
(mistletoes on A. karroo at Highover and mistletoes on
both host species at Mtontwane) showed a significant
difference in survival (range in χ 2 = 8.61–10.60, range
in P < 0.001–0.035, df = 3), but mistletoes on A. caffra
at Highover did not show any significant difference in
survival (χ 2 = 3.57, P = 0.31, df = 3) (Figure 5). Overall,
survival was higher for mistletoe seeds on Acacia karroo
than on A. caffra (Figure 5).
At Highover, mistletoes placed on Acacia karroo did not
show any significant differences in survival regardless of
the site or host species from which they were obtained
(Figure 5a). However, mistletoes placed on A. caffra
at Highover showed significant differences in survival
(Figure 5a). Survival of mistletoes from A. karroo at
Mtontwane placed on A. caffra at Highover (mkM ×
kH) was significantly lower than for the other three
combinations at Highover.
At Mtontwane, mistletoes obtained from Acacia karroo
at the same site had the highest survival on A. karroo
(mkM × kM), which was followed by mistletoes obtained
from A. caffra and placed on A. karroo at Mtontwane (mcM
× kM) (Figure 5b). Mistletoes from A. karroo at Highover
placed on A. karroo at Mtontwane had intermediate
survival, while mistletoes obtained from A. caffra at
Highover placed on A. karroo at Mtontwane had the
lowest survival of all seeds inoculated on A. karroo.
Host specificity of the mistletoe Agelanthus natalitius
159
Figure 3. The hypocotyl length after 1 mo (white bar) and 6 mo (black bar) (mean ± SE) of the germinated mistletoe seedlings of Agelanthus natalitius
in the reciprocal transplant experiments of all combinations of source host species × current substrate at both sites, Highover (a) and Mtontwane
(b). Abbreviations: source host species, mk = mistletoe seedlings obtained from mistletoes that grew originally (source) on Acacia karroo and mc =
mistletoe seedlings obtained from mistletoes that grew on Acacia caffra and current substrate; k = A. karroo and c = A. caffra; source host species
with their respective site; mkH = mistletoes from A. karroo at Highover, mkM = mistletoes from A. karroo at Mtontwane, mcH = mistletoes from A.
caffra at Highover, mcM = mistletoes from A. caffra at Mtontwane.
160
DESALE Y. OKUBAMICHAEL, MEGAN E. GRIFFITHS AND DAVID WARD
(a) Highover
0.8
Per cent survival
Probability of survival after 6 mo
1.0
0.6
0.4
mkH × kH
mkM × kH
mcH × kH
mcM × kH
A.NS
karroo
95
NS
70
45
20
0.2
0
1
2
3
4
5
6
7
Time (mo)
2
4
6
8
Hypocotyl length (mm)
Figure 4. Relationship between hypocotyl length of mistletoe seedlings
of Agelanthus natalitius and their survival.
Mistletoes from A. karroo at Mtontwane placed on A. caffra
at Mtontwane (mkM × cM) had the highest survival,
followed by mistletoes of A. caffra from Mtontwane placed
on A. caffra in Mtontwane (mcM × cM) (Figure 5b).
Mistletoes of A. karroo from Highover placed on A. caffra at
Mtontwane (mkH × cM) and mistletoes of A. caffra from
Highover placed on A. caffra at Mtontwane (mcH x cM)
had the lowest survival of seeds inoculated on A. caffra
(Figure 5b). This demonstrates that mistletoe seedlings
perform better on the same host species as the parent plant
and in the same site from which they were obtained.
a
b
a
a
A. caffra
95
70
mkH × cH
mkM × cH
mcH × cH
mcM × cH
45
20
0
1
2
3
4
5
6
7
Time (mo)
(b) Mtontwane
Per cent survival
0
Per cent survival
0.0
A. karroo
95
a
b
c
b
mkH × kM
mkM × kM
mcH × kM
mcM × kM
4
5
70
45
20
0
1
2
DISCUSSION
Agelanthus natalitius parasitizes several host species and
its local distribution can be patchy. Our study found
Acacia karroo to be the most compatible host species for
Agelanthus natalitius in two field sites in KwaZulu-Natal,
South Africa, based on the fact that higher infection
intensity (number of mistletoes per tree) was recorded
on A. karroo. The reciprocal transplant germination
experiment in the field also showed that overall the
hypocotyls of Agelanthus natalitius seedlings grew better
on A. karroo than A. caffra. This demonstrates a general
preference by the mistletoe for the most abundant host
species, A. karroo. These results were consistent with those
of other studies demonstrating that host specificity can be
influenced by host abundance, given that abundant host
species are encountered most frequently and are more
reliable hosts through space and time (López de Buen &
Ornelas 2002, Norton & de Lange 1999, Zuber & Widmer
2000). In contrast, Roxburgh & Nicolson (2005) found
no relationship between observed prevalence among host
Per cent survival
Host abundance
3
6
7
Time (mo)
a
b
a
c
A. caffra
95
70
mkH × cM
mkM × cM
mcH × cM
mcM × cM
45
20
0
1
2
3
4
5
6
7
Time (mo)
Figure 5. Percentage survival over 6 mo of Agelanthus natalitius mistletoe
seedlings. Two groups of mistletoes received from two different host
species placed on two host species at two sites ( = 16 combinations in
total). (a) Highover survival curves of mistletoes placed on Acacia karroo
and Acacia caffra, (b) Mtontwane survival curves of mistletoes placed
on Acacia karroo and Acacia caffra. Abbreviations for mistletoe sources:
mkH = mistletoes from A. karroo at Highover, mkM = mistletoes from
A. karroo at Mtontwane, mcH = mistletoes from A. caffra at Highover,
mcM = mistletoes from A. caffra at Mtontwane. Abbreviations for hosts:
kH = A. karroo from Highover, kM = A. karroo from Mtontwane, cH =
A. caffra from Highover and cM = A. caffra from Mtontwane. NS = not
significant. The lowercase letters denote significant differences between
groups of mistletoe seeds.
Host specificity of the mistletoe Agelanthus natalitius
species and compatibility of the mistletoe Plicosepalus
kalachariensis in Zambia.
Many bird species disperse Agelanthus natalitius seeds
to the same tree as the maternal plant or to nearby trees
(Green et al. 2009, Okubamichael et al. 2011a, Roxburgh
2007). This may reduce colonization of new sites, but
might improve chances of landing in a safe site (Norton &
Carpenter 1998, Norton & de Lange 1999, Okubamichael
et al. 2011a). Thus adaptation of a mistletoe to the most
abundant host species would facilitate dispersal efficiency.
Rare host species are less likely to receive mistletoe seeds
by chance, except when birds differentially perch on those
host species due to the presence of fleshy fruits or some
other trait that would make them attractive to birds.
Host tree traits
Birds differentially disperse mistletoe seeds to tall trees
(Aukema & Martı́nez del Rio 2002, Ward et al. 2006),
so any difference in size among potential host species
could result in differential distribution of mistletoes among
host trees. However, A. karroo and A. caffra trees did
not differ in size (height and dbh) in either site, so
differences in mistletoe infection cannot be attributed
to size differences in the host species. We found that
infected trees were taller and had a greater trunk diameter
than uninfected host trees for both host species in both
sites. This may be a consequence of the behaviour of
dispersers, as birds differentially perch on tall trees and
may deposit mistletoe seeds in the process. Moreover,
tall trees are generally older and have had more time
to become infected by mistletoes (Aukema & Martı́nez del
Rio 2002, Donohue 1995, Overton 1994). Thus, large
trees are frequently observed to have a greater number
of mistletoe infections than smaller trees (Aukema 2004,
Donohue 1995, Roxburgh & Nicolson 2007, Ward et al.
2006).
Overton (1994) explained the frequency of mistletoe
infection as an accumulation function of infection with
time as the tree gets older. As in previous studies (Aukema
2004, Donohue 1995, Roxburgh & Nicolson 2007),
linear regression analysis in this study produced a weak
correlation between height of tree and infection intensity.
This analysis may be inappropriate, however, because the
data in these other studies followed a negative binomial
distribution. An alternative (GLIM) analysis explained
the observed patterns better because the frequency
distribution of the number of mistletoes per tree (infection
intensity) is a good fit to the negative binomial distribution
(i.e. most individual trees are free of mistletoes and a
few individuals are highly infected). Previous infection
increases the likelihood of further infection and it causes
a clumped or aggregated distribution which is likely due to
the limited dispersal distance of mistletoe seeds from their
161
source (Aukema 2004, Overton 1994, Ward & Paton
2007).
There was a steep slope for the regression of tree height
to mistletoe prevalence because birds differentially visit
tall trees. Trees with big trunks are often tall but this
is not always the case; this may explain why there is
a weaker relationship between prevalence and dbh as
compared with tree height. For example, at Highover, A.
caffra trees were tall but they did not have big trunks.
In addition, tall trees are usually more branched and
provide more twigs with a suitable diameter than short
trees (Sargent 1995). Mistletoes deposited on tall trees also
have greater success because tall trees are less likely to be
shaded by neighbours, thereby providing adequate light
for mistletoes (Lamont 1982, Okubamichael et al. 2011a,
Ward & Paton 2007, Ward et al. 2006). Tall trees may
supply more nutrients and water to the mistletoes due
to deeper and broader root systems (Ward et al. 2006).
Tall trees may also protect mistletoes from browsing by
large herbivores (Roxburgh & Nicolson 2005, 2007).
Mistletoes are often selected by herbivores over their
host trees because the mistletoes have higher mineral
and nitrogen concentrations and have few physical and
chemical defence mechanisms. Thus, herbivores can limit
mistletoes in natural communities (Midgley & Joubert
1991). Associated with this, Agelanthus natalitius growing
on A. karroo may be better protected against foragers
because A. karroo has longer spines than A. caffra and
is better defended against herbivores (see also Martı́nez
del Rio et al. 1996).
Reciprocal transplant experiment
Our study supports previous findings that germination
of mistletoes is independent of site and substrate provided
that the pericarp is removed (Ladley & Kelly 1996, Lamont
1983, Rödl & Ward 2002, Roxburgh & Nicolson 2005).
Hypocotyl length and growth form, however, showed
crossed reaction norms, indicating that there were
significant differences due to G × E interactions in this
mistletoe species. The growth patterns of the hypocotyl
varied based on site, source and the substrate on which
they were placed. This implies that morphologically
identical mistletoes may be genetically different, such
that early seedling development is greatest when there
is correspondence between maternal and seedling host
species. Several studies also demonstrated that the
development of the haustorium is more successful when
mistletoe seeds are placed on their source host species
(Arruda et al. 2006, Clay et al. 1985, Rödl & Ward
2002, Yan 1993b). Unfortunately, measuring lifetime
fitness differences in reciprocal transplant experiments
in long-lived perennial plants requires more time than
was available for this study. For this reason quantitative
162
DESALE Y. OKUBAMICHAEL, MEGAN E. GRIFFITHS AND DAVID WARD
genetic analysis should be considered in future studies
of the relationship between this mistletoe species and its
hosts.
Host compatibility, host selection, host recognition,
localization of gene flow and spatial segregation of host
species or populations promote host race formation in
mistletoe populations (Glazner et al. 1988). Our findings
show that differences in host utilization of source and
non-source host species may have a genetic basis,
leading to differential success of individuals from one
mistletoe population when grown on a different host
species or in different areas. However, it is still not
clear what mechanisms the mistletoes use to differentiate
between hosts of different species and from different
localities.
The haustorium is a distinct and unifying structure
of parasitic plants. Thus, investigating haustorium
formation and adaptation provides a holistic approach
to study both infection patterns and host specificity
in parasitic plants (Calvin & Wilson 2006, Thorogood
et al. 2009). Although the chemical interactions
between aerial parasites and their hosts are as yet
unstudied, it has been found in root parasites that hostderived chemicals stimulate germination and haustorium
formation (Bouwmeester et al. 2003, Chang & Lynn 1986,
Matvienko et al. 2001, Tomilov et al. 2004, Yoder 1999).
The results of this study suggest that chemical interactions
between mistletoes and their host trees may occur during
post-germination development and this may be the basis
for the G × E interactions we observed at the early stage
of the mistletoe growth (see also Runyon et al. 2006,
Thorogood & Hiscock 2010).
Survival over 6 mo clearly showed that mistletoes
transferred to non-source host species and to non-local
sites had lower survival. This demonstrates that mistletoes
have mechanisms that facilitate compatibility to their
parental hosts. In addition, the fact that mistletoes on
A. caffra did not show any difference in survival at
Highover may indicate that this population of mistletoes
uses A. caffra opportunistically and the mistletoes that
can grow on A. caffra may not be as specific as those
that grow on A. karroo at this site. We found that
mistletoe seedlings had longer hypocotyls when grown
on A. karroo, regardless of the host their parent plant
occurred on, which could reflect an adaptation to the
most frequently encountered host tree. Similar findings
were reported by Norton & Carpenter (1998) and by
Rödl & Ward (2002). Further studies on mistletoe
performance (in terms of hypocotyl growth, survival and
reproduction) should focus on combinations of reciprocal
transplant experiments. For example, differences in
mistletoe performance should be tested on parental versus
non-parental hosts and preferred versus non-preferred
hosts to determine the underlying mechanisms that
determine host compatibility.
ACKNOWLEDGEMENTS
We thank Leeza Musthafa for help in the field and Vanessa
Stuart for technical assistance. Many thanks for the
hospitality and assistance of the managers at Highover
and Mtontwane. We thank J.R. Kambatuku for comments
on an earlier draft. We are grateful for the Claude Leon
Foundation for postdoctoral research funding to M.E.G.
and the National Research Foundation for funding to
D.W.
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