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Dependence on sunbird pollination for fruit set in three West African montane mistletoe species

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  • Department of Conservation, New Zealand

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Theory predicts that not all plant species will be equally affected by disruption to their pollinator mutualisms because traits such as breeding system and mutualism strength can affect their response. We investigated these traits in three species of Afromontane mistletoe Globimetula braunii, Agelanthus brunneus and A. djurensis in Ngel Nyaki Forest Reserve, Nigeria, to test whether the traits were reliable indicators of relative reproductive success and could be used to predict relative vulnerability to pollinator loss. For each mistletoe species, insect and bird visitors were identified during a 160–240-min observation period of 4–10 plants and their roles in flower opening and fruit set were investigated using exclusion experiments applied to 250–500 flowers. We found that all three mistletoes are self-compatible but not capable of autonomous self-fertilization. The pollinator assemblage comprised four species of sunbird (Cyanomitris spp., Cinnyris spp.) and a small social wasp (Vespinae). None of the mistletoes requires birds for flower opening: G. braunii flowers self-opened in the absence of pollinators, whereas insects opened both Agelanthus spp. Irrespective of flower opening, each mistletoe species requires sunbirds for effective pollination and fruit set. Only G. braunii demonstrated pollen limitation (pollen limitation index = 0.504) which may be an early indication of mutualism breakdown. We suggest that mistletoes be considered as indicators of habitat condition and functioning within Afromontane forest ecosystems.
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Journal of Tropical Ecology (2012) 28:205–213. © Cambridge University Press 2012
doi:10.1017/S026646741100068X
Dependence on sunbird pollination for fruit set in three West African
montane mistletoe species
Kerry A. Weston
,1
, Hazel M. Chapman
, Dave Kelly
and Elena V. Moltchanova
School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand
Mathematics and Statistics Department, University of Canterbury, Private Bag 4800 Christchurch, New Zealand
Abstract: Theory predicts that not all plant species will be equally affected by disruption to their pollinator mutualisms
because traits such as breeding system and mutualism strength can affect their response. We investigated these traits
in three species of Afromontane mistletoe Globimetula braunii, Agelanthus brunneus and A. djurensis in Ngel Nyaki Forest
Reserve, Nigeria, to test whether the traits were reliable indicators of relative reproductive success and could be used to
predict relative vulnerability to pollinator loss. For each mistletoe species, insect and bird visitors were identified during
a 160–240-min observation period of 4–10 plants and their roles in flower opening and fruit set were investigated
using exclusion experiments applied to 250–500 flowers. We found that all three mistletoes are self-compatible but not
capable of autonomous self-fertilization. The pollinator assemblage comprised four species of sunbird (Cyanomitris spp.,
Cinnyris spp.) and a small social wasp (Vespinae). None of the mistletoes requires birds for flower opening: G. braunii
flowers self-opened in the absence of pollinators, whereas insects opened both Agelanthus spp. Irrespective of flower
opening, each mistletoe species requires sunbirds for effective pollination and fruit set. Only G. braunii demonstrated
pollen limitation (pollen limitation index = 0.504) which may be an early indication of mutualism breakdown. We
suggest that mistletoes be considered as indicators of habitat condition and functioning within Afromontane forest
ecosystems.
Key Words: Afromontane forest, Agelanthus brunneus, Agelanthus djurensis, Globimetula braunii, Loranthaceae,
mutualism, Nigeria, pollen limitation, self compatibility, sunbirds
INTRODUCTION
Disruption of pollination mutualisms resulting from
anthropogenic disturbance can lead to reduced seed
set (Aizen & Feinsinger 1994), an increased risk
of extinction (Bond 1994) and a cascade of effects
throughout entire ecosystems (Anderson et al. 2011,
Pauw 2007, Sekercioglu 2011). Understanding plant–
pollinator relationshipsis vital for identifying plant species
at risk of reproductive failure. Across much of Africa,
studies on pollination relationships are lacking (Rodger
et al. 2004).
Theory predicts that not all plant species will
be equally affected by disruption to their pollinator
mutualisms because certain traits confer resilience to
pollinator loss (Aguilar et al. 2006, Bond 1994). Self-
1
Corresponding author. Current address: Department of Zoology,
University of Otago, P.O. Box 56, Dunedin, New Zealand.
Email: kerry-anne.weston@otago.ac.nz
compatible plants capable of autonomous self-fertilization
are least dependent on pollinators while in contrast, self-
incompatible, obligate outbreeders are entirely dependent
on their pollinator mutualists. The more specialized
the pollination mutualism, the more vulnerable it is to
disruption through anthropogenic activity (Johnson &
Steiner 2000). Recently, the credibility of pollination
syndromes as a means of predicting plant–pollinator
relationshipshas been questioned as studies have revealed
a wider suite of pollinators than the pollination syndrome
would suggest (Hingston & McQuillan 2000, Kelly et al.
1996, 2010; Ollerton 1998, Pauw 1998, Robertson et al.
2005).
In this study we aim to describe the plant–pollinator
mutualism of three loranthaceous Afromontane forest
mistletoes occurring in the Ngel Nyaki Forest Reserve,
Nigeria, and determine whether these three species differ
in breeding system and the strength of their pollinator
mutualisms. From these data we will predict their relative
vulnerability to reduced pollinator abundance and/or
diversity.
206 KERRY A. WESTON ET AL.
Self-compatibility is common within the Loranthaceae,
however the capacity to self-pollinate is rare and
outbreeding is considered the norm (Aizen 2005, Azpeitia
& Lara 2006, Bernhardt et al. 1980, Docters van
Leeuwen 1954, Ladley et al. 1997). Most African
Loranthaceae display some form of explosive flower
opening (Evans 1895) but exhibit wide diversity in
terms of the floral characteristics and signals presented
to pollinators (Kirkup 1998, Polhill 1989). Explosive
opening is typically obligate, where the flower cannot
open unless visited by a biotic agent and is an adaptive
strategy for specialized pollination by birds (Docters van
Leeuwen 1954, Feehan 1985, Ladley et al. 1997). Flower
opening takes place in either one or two stages (Feehan
1985, Kirkup 1993). Two-stage flowers open further at
the second touch of the pollinator and it is not until the
second stage that the anthers are forced to shed their
pollen explosively (Kirkup 1993, Ladley & Kelly 1995).
Success in the two steps of the pollination process, flower
opening and pollen deposition, can be independent with
success at one step not necessarily ensuring success at t he
other (Robertson et al. 2005).
The specific objective of this study was to determine
whether traits such as breeding system and plant–
pollinator mutualism strength could be used to predict
whether three common and sympatric species of
loranthaceous mistletoes (Globimetula braunii, Agelanthus
brunneus and A. djurensis) are likely to differ in their
response to changes in pollinator abundance and/or
diversity. Reduced pollinator abundance and diversity
is a common response to habitat degradation and
fragmentation (Ewers & Didham 2006, Potts et al. 2010),
both of which are ongoing within Ngel Nyaki Forest
Reserve (Chapman et al. 2004). We hypothesize: pollen
limitation and reduced fruit/seed set will be more severe
in species (1) with only one or a small assemblage
of pollinators relative to species with a wide range of
pollinating taxa and (2) exhibiting a dependence on
pollinators relative to species which have self-opening
flowers and are self-compatible.
STUDY SITE AND SPECIES
Ngel Nyaki Forest Reserve is located between 1400–1600
m asl on the Western Escarpment of the Mambilla Plateau,
in Taraba State, Nigeria (7
14
N, 11
04
E). The reserve
is approximately 46 km
2
in area, c. 7.2 km
2
of which
comprises the most floristically diverse submontane forest
in Nigeria (Chapman & Chapman 2001).
The climate of the Mambilla Plateau is highly seasonal.
Mean annual rainfall is c. 1800 mm, falling almost
entirely during the rainy season from April to October
(Nigerian Montane Forest Project rainfall data). Mean
monthly maximum and minimum temperature for the
rainy and dry season are 26
C and 13
C, and 23
Cand
16
C, respectively (Upper Benue River Basin records).
The reserve is comprised of remnant forest fragments
and is under ongoing pressure from subsistence f arming.
Immediate threats are trampling and overgrazing by
Fulani cattle and the annual burning of grassland and
savannaalong the forest perimeter(Chapman et al.2004).
Mistletoe species
The three Loranthaceae species studied in this contri-
bution (Globimetula braunii (Engl.) Danser, Agelanthus
brunneus (Engl.) Balle & Hall
´
eandAgelanthus djurensis
(Engl.) Polhill & Wiens are endemic to tropical Africa.
All Globimetula species are described as having two-stage
explosively opening flowers whilst Agelanthus have a
one-stage explosive mechanism (Kirkup 1993, Polhill &
Wiens 1998). African Loranthaceae often occur most
abundantly along forest edges (Polhill 1989). Within the
study site all three species occur interdispersed along the
edges of the forest fragments and less frequently high in
the canopy of the forest interior.
Sunbirds (Nectariniidae)
Sunbirds are a large guild of passerines ranging in size
from about 5 to 45 g (Cheke & Mann 2001). They have
a d istinct long, slender and decurved bill used to feed on
nectar, insects and spiders. The majority of the group is
concentrated in Africa, where 88 species in 11 genera
are currently recognized (Cheke & Mann 2001). Despite
the adaptation that many sunbirds have made to human-
modified landscapes, the majority of species in tropical
Africa are recorded in primary forest (Borrow & Demey
2001, Cheke & Mann 2001). Sunbirds visit species from
approximately 59% of subtropical and tropical African
plant families, but particularly members of the Fabaceae
and Loranthaceae (Fleming & Muchhala 2008).
METHODS
Plant selection
Individual plants used in this study were selected on the
basis that they carried sufficient early flower buds and
were accessible with a ladder (along the forest edge and
within 4 m of the ground). Work on Loranthaceae in New
Zealand showed that pollination of plants < 4 m from the
ground did not differ from those higher in the canopy
(Robertson et al. 2008). All three plant species were
sampled along the forest edge where they predominantly
Pollination in West African montane mistletoes 207
occur and it is anticipated that they will beequally exposed
to any potential edge effects (Murcia 1995).
Flower visitors
Flower visitation observations were carried out on a
total of 10 G. braunii plants from 20 November 2007–2
December 2007, eight A. brunneus plants from 3 January
2008 to 20January 2008and four A. djurensis plants from
23–24 November 2008, during the p eak flowering period
of all observation plants. All observations were carried
out during the dry season when weather conditions were
warm with little wind.
Two G. braunii,oneA. brunneus or four A. djurensis
plants were observed per day. Prior to the start of
observation (around sunrise at 6h00), on each plant the
number of ripe buds and open flowers within a designated
field of view, referred to here as the ‘focal area’, was
recorded. The size of the focal area varied among plants
and was delimited with the aim of achieving a clear field
of view to several branches bearing many ripe buds and
freshly opened flowers.
All plants were observed through Nikon 9 ×40
binoculars. Each of the ten G. braunii plants were observed
for four 10-min intervals per day between each of
06h00–09h00, 11h00–14h00 and 15h00–18h00 on
two consecutive days, resulting in a total observation time
of 240 min per observation plant. Each of the eight A.
brunneus plants were observed for eight 10-min intervals
between the same time periods but on the same day,
resulting again in 240 min of observation per plant. Two
A. djurensis plants were observed concurrently for four
10-min intervals between 07h00–08h00 and 15h00–
16h00, whilst another pair was observed immediately
after; between 08h00–09h00 and 16h00–17h00. On
day two, the time intervals were swapped around so the
second pair was observed first during both time intervals.
This resulted in a total observation time of 160 min per
plant for A. djurensis. The length of time each bird spent
within the focal area was recorded. Insect visitors to all
plants were recorded.
All A. djurensis observation plants were checked for
visitation by an unidentified Vespinae wasp species,
as were an additional four plants used for pollination
treatments. Actual flower visits and time spent within
the focal area were not recorded for wasps because the
observation stations were too far from the focal plant, in
order to not disrupt bird visits.
All avian flower visitors were identified on site using
a field guide (Borrow & Demey 2001), whilst insect
specimens were photographed using a Canon Power Shot
A640 camera and later identified to family level (R.
Didham pers. comm.). Footage of sunbirds foraging on G.
braunii flowers was also obtained using a Canon handheld
digital video camera.
Breeding system and dependence on pollinators
Fruit set and its dependence upon pollinators were tested
with tagged buds subjected to a range of pollination
treatments. The treatments were: (1) Bagged ripe
unopened buds were enclosed inside a 50 ×40-cm
nylon bag (0.5-mm mesh) to exclude all pollinators
and ascertain whether buds were capable of self-
opening and/or autonomous selfing or apomixis. The
bag remained secured until the ovary either aborted or
began swelling; (2) Caged a wire cage with a mesh size
of 2 ×2.5-cm was secured around ripe unopened buds
to exclude avian pollinators but allow insect pollinators
access. The cage remained secured until the ovary either
aborted or began swelling. Previous studies have found
no significant effect of the cages on insect visitation rates
to mistletoe flowers (Robertson et al. 2005); (3) Natural
ripe buds were tagged and left accessible to all pollinators
to quantify natural flower opening and fruit set; (4)
Hand-selfed ripe unopened buds were hand-opened and
pollen from at least four flowers on the same plant was
applied to the stigma using a fine paintbrush to test for
self-compatibility. Flowers were then enclosed inside a
bag to prevent cross-pollination. Hand self-pollination
was repeated 2 d later, then the bag left in place until
the ovary either aborted or began swelling; (5) Hand-
crossed ripe buds were tagged, hand-opened and cross-
pollinated using a cocktail of pollen from flowers on at
least four nearby plants. The next day cross-pollination
was repeated. Flowers were left unbagged.
The five treatments were applied to ten flowering G.
braunii plants, five A. brunneus
plants and eight A. djurensis
plants (four of which were those used for pollinator
observations). Thus, the total number of buds tagged was
500 for G. braunii, 250 for A. brunneus and 400 for A.
djurensis.
Following pollination treatment, each ripe bud was
revisited every few days to monitor whether it opened
and whether it set fruit. Four flower buds observed to
contain a lepidopteran larva were excluded from the data
for a nalyses. A flower was considered to have successfully
set fruit if the developing ovary remained on the plant >
8wkforG. braunii, > 4wkforA. brunneus and > 5wkfor
A. djurensis. These time spans were selected by identifying
the development period beyond which the majority of
early fruit failures ceased and reflects the variation in
fruit development times between species.
For G. braunii, a further experiment was carried out
to test whether excluding all pollinators had an effect on
number of days a flower bud remained unopened in the
ripe condition before self-opening. A total of 25 bagged
208 KERRY A. WESTON ET AL.
and 32 unmanipulated G. braunii buds distributed across
three different plants were followed daily and the number
of days from when the bud first became ripe until when it
was first observed open was recorded. Where buds were
observed as open before achieving full ripeness, this was
recorded as 0 days in ripe condition.
Data analysis
To examine the possible effect of time of day on the time
pollinators spent within the focal area, a generalized
linear mixed-effects model with exponential response
distribution was fitted for each species. The response
variable was total time with visitors in plant (per 80-min
observation period). In the full model, plant was entered
as a random effect and time of day as the fixed effect.
For comparisons between mistletoe species, the total
time spent in the focal area of each plant during each
80-min observation period was converted to an hourly
rate per flower by dividing the time spent by the number
of ripe buds and open flowers within the focal area.
This calculation provides an estimate of the attention
each flower would likely receive by pollinators per hour,
following Robertson et al. (1999, 2005). Visits for G.
braunii were combined from day one and day two,
and visitation rates per 80-min observation period were
calculated using the average number of ripe buds and
flowers between the two days.
To examine the effect of pollination treatment on (1)
flower opening and (2) fruit set, generalized logistic linear
mixed-effects models were fitted. The response variables
were (1) flower opened or unopened, and (2) successful
fruit set or failure. Where the fate of the bud was
unknown, data were not included in the analysis. In the
full model, plant was entered as a random effect and the
fixed effects were species and treatment. An interaction
between species and treatment was also included to test
for differences between species in the effect of treatment
on flower opening or fruit set.
A pollen limitation index (PLI) was calculated for each
mistletoe species using the formula PLI = 1 (P
n
/P
x
),
where P
n
is the per cent fruit set of naturally pollinated
flowers and P
x
is the per cent fruit set by plants that
received hand-crossed pollen. A PLI of 0 indicates no
pollen limitation in the population studied, whereas a PLI
of 1 indicates complete pollen limitation (Larson & Barrett
2000).
To examine the effect of excluding pollinators through
bagging on number of days a flower bud remained
unopened in the ripe condition (for G. braunii only) a
generalized logarithmic mixed-effects model was fitted.
The response variable was time until open. In the full
model, plant was entered as a random effect and the fixed
effect was treatment.
All the models were fitted within Bayesian framework.
Standard non-informative priors were used in all models:
N(0, 1000
2
) for all the fixed-effect sizes and N(0, τ )
for the random effects, with the precision τ assigned a
standard non-informative prior Gamma (0.001, 0.001).
All the models were estimated using the WinBUGS
software (Lunn et al. 2000). In each case 10 000 burn-
in was deemed sufficient and a further 40 000 iterations
were used for monitoring. The convergence was assessed
visually. Posterior means and 95% credible intervals
were evaluated for all the parameters of interest, and the
Deviance Information Criteria (DIC) was used for model
comparison. (The smaller DIC corresponding to the better
model fit. The WinBUGS manual suggests that a difference
of 10 units definitely rules out the comparatively worse
model.)
RESULTS
Flower visitors
Four species of sunbird from two genera were observed
visiting mistletoe flowers; Cyanomitra obscura (western
olive sunbird), Cyanomitra verticalis (green-headed
sunbird), Cinnyris reichenowi (northern double-collared
sunbird) and Cinnyris venustus (variable sunbird) (Table
1). The honey bee (Apis mellifera) and a small social wasp
species (subfamily: Vespinae) were also observed to visit
the flowers of A. brunneus and A. djurensis respectively
(Table 1).
There was no evidence for the time-of-day effect on
the length of time sunbirds spent foraging within the
focal area for either Agelanthus sp. given that the DIC
for the full model did not markedly differ from that for the
null model: 168 compared with 166 for A. brunneus and
105 compared with 110 for A. djurensis. For Globimetula
braunii, there was a small time-of-day effect with sunbirds
spending slightly longer foraging in the morning.
All eight A. djurensis study plants were visited by
Vespinae wasps. Closer investigation of the wasps on
A. djurensis flowers revealed they were harvesting pollen
from unopened flowers by curling their body around the
flower tip and prising open the corolla lobes with their legs
and mandibles, just enough to clean the newly exposed
anthers of their pollen. TwoA. brunneus plants were visited
by Apis mellifera which robbed nectar from the flowers.
Breeding system and dependence on pollinators
There was evidence for the effect of treatment on
mistletoe flower opening and for its variability between
species as shown by the best-fit model being the full
model containing the effect of species, treatment and
Pollination in West African montane mistletoes 209
Table 1. Mean visitation rates (all sunbirds combined, S per flower h
1
± SE) and species of flower visitors
observed at each of the three mistletoe species Globimetula braunii (n = 10 plants), Agelanthus brunneus (n = 8)
and Agelanthus djurensis (n = 4) in Ngel Nyaki Forest Reserve.
= observed, X = not observed.
Flower visitor Body length (cm) G. braunii A. brunneus A. djurensis
Sunbird:
Visitation rate 0.107 ± 0.025 0.101 ± 0.028 0.125 ± 0.042
Cyanomitra obscura 13–15
√√√
Cyanomitra verticalis 13–14
X
Cinnyris reichenowi 11.5
√√√
Cinnyris venustus 10
√√
X
Other:
Apis mellifera 1.3 X
X
Vespinae sp. 0.8–1 X X
an interaction between species and treatment. This
shows that the three mistletoes exhibited quite different
pollination biology. The flowers of G. braunii are able
to self-open in the absence of pollinators, but have
a significantly higher probability of opening when
bird pollinators have access (Figure 1). There was no
significant difference in the proportion of flowers opened
between the bagged and caged treatment (Figure 1)
showing that insects do not contribute significantly to
flower opening in G. braunii. The time a ripe G. braunii
bud took to open was considerably longer under bagged
conditions than natural conditions as shown by the
fact that the model containing treatment effects was a
significantly better fit to the data than the null model
(DIC 253 compared with 285). When buds were e nclosed
within a bag to exclude all pollinators, ripe buds remained
unopened for an average of 8.6 d (95% CI = 5.4–
14.1 d) before self-opening. In contrast, under natural
conditions ripe buds opened after 1.7 d (95% CI = 1.1–
2.6 d).
In contrast to G. braunii, flowers of A. brunneus and A.
djurensis almost never opened within bags indicating that
the flowers of these species do not self-open (Figure 1). The
probability of a flower opening under natural conditions
was only slightly higher than the probability of a flower
opening within a cage for both Agelanthus spp. (Figure 1).
This indicates that insects alone are opening the flowers of
these two mistletoes as effectively as when sunbirds also
have access.
The effect of treatment on fruit set d iffered between
the three mistletoe species as shown by the best-fit
model being the full model containing the effect of
Figure 1. Estimated probability of a flower opening under bagged, caged and natural treatments within Ngel Nyaki Forest Reserve, Nigeria, for
Globimetula braunii, Agelanthus brunneus and Agelanthus djurensis. Bars show the posterior mean probability of opening (p) and the corresponding
95% credible interval.
210 KERRY A. WESTON ET AL.
Figure 2. Estimated probability of a flower setting fruit under bagged, caged, crossed, natural and selfed treatments within Ngel Nyaki Forest Reserve,
Nigeria, for Globimetula braunii, Agelanthus brunneus and Agelanthus djurensis. Bars show the posterior mean probability of fruit set (p) and the
corresponding 95% credible interval.
species, treatment and an interaction between species
and treatment. Fruits were almost never produced inside
bags indicating that the flowers of these mistletoes are
not capable of autonomous self-fertilization (Figure 2).
This was despite an average of 66% of G. braunii flowers
self-opening and hand pollinations revealing high self-
compatibility in all three species (Figure 2). There was a
very low probability of plants producing fruits inside cages
where only insects had access (Figure 2). Hand-pollinated
flowers of Globimetula braunii had significantly higher fruit
set than those under natural conditions (Figure 2). This
indicates that in the years studied, G. braunii was pollen
limitedwith a meanPLI of 0.504.Neither of theAgelanthus
spp. were pollen limited, both with a mean PLI of 0.
DISCUSSION
Our results demonstrate that sunbirds are essential to the
effective pollination of all three mistletoe species included
in this study. However, the details of the mutualism
differed between the two genera.
Role of insects for pollination (flower opening and
reproduction)
Insects were never observed visiting the flowers of
Globimetula braunii and did not play a significant role in
flower opening as confirmed by the exclusion experiments
where approximately the same number of flowers opened
when all pollinators were excluded relative to when
insects had access. In contrast the honey bee (Apis
mellifera) and a species of social wasp (subfamily:
Vespinae) were observed visiting the flowers of A. brunneus
and A. djurensis respectively. Whilst honeybees were only
observed robbing nectar from the flowers of A. brunneus,
the Vespinae wasps were observed opening flowers of A.
djurensis by prising open the corolla lobes with their legs
and mandibles to harvest pollen. However, despite insects
not being observed opening the flowers of A. brunneus,the
exclusion experiments showed insects played a significant
role in opening flowers of both Agelanthus spp. Flower
opening of explosive bird-pollinated mistletoe flowers by
invertebrates has, to our knowledge, only been recorded
once elsewhere. The small native solitary bees Hylaeus
agilis and Leioproctus pango have been observed prising
open the flowers of Peraxilla tetrapetala and P. colensoi in
NewZealand (Donovan 2007, Kellyet al. 1996, Robertson
et al. 2005). In contrast to the New Zealand system
where these insects frequently effect pollination (Kelly
et al. 1996, Ladley et al. 1997, Robertson et al. 2005),
flower-opening by insects in our study area only rarely
resulted in successful pollination.
Role of birds for pollination (flower opening and
reproduction)
Four sunbird species (Cyanomitra obscura, C. verticalis,
Cinnyris reichenowi and C. venustus) were observed visiting
the flowers of the Ngel Nyaki mistletoes, with all four
species visiting G. braunii, and three to each of the
Agelanthus species.
While Globimetula braunii flowers were able to self-open
in the absence of pollinators, bird visitation resulted in
Pollination in West African montane mistletoes 211
significantly more flowers being opened and at a faster
rate. In contrast, neither of the Agelanthus spp. were
able to self-open and birds did not significantly increase
flower opening relative to insects-only. While all four
sunbird species visited open mistletoe flowers, it was
only the largest two species from the genus Cyanomitra,
C. obscura and C. verticalis, with the longest, heaviest
bills (Cheke & Mann 2001) which were observed
opening them. Previous studies of Loranthaceae have
shown flower-opening to be related to pollinator size,
a relationship which can be explained by an increased
selection pressure on larger birds associated with their
higher energetic requirements (Gill & Wolf 1975).
Because the majority of pollen is released explosively from
the anthers onto pollinators during flower opening, C.
obscura and C. verticalis are also the only two sunbird
species likely to pollinate effectively. Moreover as only C.
obscura was observed with large amounts of pollen on
its crown feathers it may be the only effective pollinator.
Future work quantifying pollen removal and deposition
will confirm the contribution to pollination by each
sunbird species.
The fact that the flowers of A. brunneus never set fruit
when birds were excluded and for G. braunii and A.
djurensis only rarely, illustrates that effective pollination
and fruit set in all three species was dependent on a
single guild of at most three to four closely related sunbird
species.
Limiting processes for reproduction, differences among
species
Of the three Ngel Nyaki mistletoes included in our study
only G. braunii was pollen limited (PLI =0.504). This was
unexpected because G. braunii had the largest assemblage
of sunbird pollinators and was not dependent on biotic
agents for flower opening.
However, despite self-compatibility, all three species in
this study lacked autonomous self-fertilization and were
dependent on biotic pollination. Consequently, the self-
opening flowers of G. braunii do not necessarily lead to
pollination and several subsequent visits by pollinators
may be required to deliver sufficient pollen. For example
in New Z ealand the flowers of Peraxilla tetrapetala and P.
colensoi often fail to receive any pollen grains on the stigma
during opening and rely on subsequent accumulation
of pollen over 6–7 d after flower opening for successful
pollination (Robertson et al. 1999, 2005). Furthermore,
because the majority of pollen is released explosively
from the anthers onto pollinators during flower opening,
self-opening may actually be detrimental to the male
reproductive success of G. braunii.
In New Zealand Loranthaceae, pollen-limitation has
been attributed to a decline in pollinating bird species as
a result of predation by introduced mammals (Anderson
et al. 2011, Kelly et al. 2005, Robertson et al. 1999).
In the Patagonian loranth Tristerix corymbosus, pollen
limitation during winter flowering results from seasonally
reduced visitation by hummingbirds (Aizen 2003). For G.
braunii at Ngel Nyaki, it may be that during peak flowering
in December, the sunbirds were foraging on other more
energetically rewarding resources ‘distracting’ them from
G. braunii (Campbell 1985, Gross 1996, Gross & Werner
1983, Murphy & Kelly 2001). A large canopy tree
Anthonotha noldeae (Fabaceae) was in full flower at this
time and large numbers of sunbirds were observed to be
foraging on its flowers in the vicinity of mistletoes (K.
Weston, pers. obs.). However, sunbird visitation rates to
G. braunii
were similar to those of the non-pollen limited
Agelanthus spp., with 0.11 s per flower h
1
equating to
about 14 s of visitation time per flower over its lifetime.
Such visitation rates are also similar to those recorded for
the New Zealand loranth Peraxilla colensoi, which was not
pollen limited (Robertson et al. 1999).
It is possible that the less-specialized actinomorphic
(radially symmetric), two-stage-opening flowers of Globi-
metula comprise a less-efficient pollination mechanism
than that of the Agelanthus spp., rendering G. braunii
more sensitive to pollinator disruption. The brief period
of nectar production by G. braunii flowers after opening
relative to the Agelanthus spp. (2 d vs 5–9 d) (Weston
2009) may also limit ongoing visitation to already open
flowers, resulting in the lower female reproductive success
of G. braunii relative to the Agelanthus spp. The size and
density o f the three mistletoe populations should also be
assessed to investigate the effects o f population spatial
structure on reproductive ecology.
We predicted that pollen limitation and reduced
fruit/seed set would be more severe in species with a
relativelysmaller assemblage ofpollinators and exhibiting
greater dependence on pollinators for flower opening and
reproduction. Consequently, our results were contrary
to those predictions. Only G. braunii demonstrated pollen
limitation, and this species had the largest assemblage
of sunbird pollinators. Furthermore, G. braunii was the
only species found to have self-opening flowers. Therefore,
given our assessments of the plant–pollinator mutualism
and breeding system of these mistletoe species, we were
unable to accurately predict which species were most
vulnerable to reproductive failure.
The pollination limitation revealed in G. braunii may
be an early indication of mistletoe–pollinator mutualism
breakdown in Ngel Nyaki forest. Due to the high incidence
of mistletoe–animal interactions, it seems likely that
disruption to these mutualisms will have cascading effects
within the West African montane forest ecosystem.
Rather than perpetuating the common viewpoint that
mistletoes are destructive weeds, we suggest that the
mistletoes in these ecosystems should be considered as
indicators of habitat condition and functioning.
212 KERRY A. WESTON ET AL.
Limitations
This study was limited to plants located along the forest
edge and consequently the observed interactions may
have been biased by edge effects (Murcia 1995). A recent
literature review of edge effects on plant reproduction
classified species as showing a significant negative effect,
no effect, or a significant positive effect and found 69%
of species showed some effect, the majority of which were
negative (Burgess et al. 2006). Studies of the New Zealand
LoranthaceaePeraxilla tetrapetala have shown higherfruit
set in plants growing along forest edges attributed to
higher visitation rates by birds and bees (Burgess et al.
2006, Kelly et al. 2000). In order to remove any such
bias it would be valuable to study plants high within the
canopy of the forest interior to compare pollen-limitation
in those plants to that recorded for the edge-dwelling
plants included in this study.
The small sample size of plants for pollinator observa-
tions in this study may not provide a full representation
of the pollinator community. This consideration is
particularlyrelevant given that theexclusionexperiments
indicated flower opening by insects for one species,
A. brunneus, where insects were not recorded visiting
flowers throughout observations. Further observations of
flowering plants within the study area would be valuable.
Furthermore, the pollination treatments in this study
were only applied during one season at Ngel Nyaki forest.
It would be beneficial to conduct these experiments over
several consecutive years to account for any differences
in plant responses between flowering seasons.
ACKNOWLEDGEMENTS
We thank Usman Usuf and other staff of the Nigerian
Montane Forest Project for invaluable field assistance. We
are grateful to the Taraba State Forest Service for their
invitation and permission to conduct research. Financial
support came from The North of E ngland Zoological
Society, Nexen Nigeria Inc., A. P. Leventis Foundation
andthe Foundation forResearch, Science andTechnology
under contract CO9X0503. Special thanks to Roger
Polhill for helpful discussions on African mistletoes and to
Steve Johnson and an anonymous referee for suggesting
improvements to the manuscript.
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... The interactions between plants and animals are a shared feature of most ecological systems (Nsor, 2015). Animals interact with plants in several ways, with most except herbivory, mutually benefiting the host plants through for instance pollination and dispersal (Klein, et al., 2007, Weston et al 2012.These interactions between plants and animals are pivotal to ecological stability, network persistence and genetic diversity. These interactions are either pair wise (bipartite) or multi-level (web type) interactions and as such species (plants and animals) in any given ecological community are directly or indirectly involved in series of ecological processes that underpin their survival (Thompson, 2010). ...
... About 80 % of tropical plants depend on insects for their pollination and reproductive success (Klein et al., 2007) with only a minority utilizing other biotic agents such as birds and bats on the one hand, and abiotic pollen vectors mainly wind on the other hand (Ollerton et al., 2011). Apart from insects, birds contribute to the reproduction and fitness of several angiosperms species (Weston et al., 2012, Nsor et al., 2019. Studies have shown the relative efficiency of birds especially sunbirds as pollinators in the old world tropics (Weston et al., 2012;Nsor and Chapman, 2013;Nsor et al., 2017 andNsor et al., 2019) and hummingbirds in the new world tropics (Sanfiorenzo et al., 2018;Machac, 2020). ...
... Apart from insects, birds contribute to the reproduction and fitness of several angiosperms species (Weston et al., 2012, Nsor et al., 2019. Studies have shown the relative efficiency of birds especially sunbirds as pollinators in the old world tropics (Weston et al., 2012;Nsor and Chapman, 2013;Nsor et al., 2017 andNsor et al., 2019) and hummingbirds in the new world tropics (Sanfiorenzo et al., 2018;Machac, 2020). ...
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... venustus), and Beautiful (C. pulchella) sunbirds are the most active in West Africa (Boussim et al., 1993;Raji et al., 2021;Weston et al., 2012). Olive-bellied (Cinnyris chloropygius) and Collared (Hedydipna collaris) sunbirds have been specified as potential pollinators of Tapinanthus bagwensis in Ghana (Room, 1972b), while Copper Sunbird (Cynnyris cupreus) -of Agelanthus dodoneifolius in Nigeria (Raji et al., 2021). ...
... The genus Helixanthera, regarded as the most primitive of the African Loranthaceae, might be the only one having flowers adapted to insect pollination (Dibong et al., 2008;Polhill & Wiens, 1998). The honeybee (Apis mellifera) and a small social wasp from the Vespinae visited the flowers of Agelanthus brunneus and A. djurensis in Nigeria, robbing nectar by making perforations in the bases of corollas (Weston, 2009;Weston et al., 2012). ...
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... Although very little literature existed (Ash et al., 1989) on the rich avifauna of this region, the establishment of the Nigerian montane forest project (NMFP), about a decade ago, has remarkably boosted research interest in the faunal diversity of Ngel Nyaki forest (NMFP annual report, 2012(NMFP annual report, , 2013. In addition, the high species richness and endemism of birds in Ngel Nyaki forest reported by some of the earliest surveys (Hall, 1976) has recently attracted more ornithological research (Ezealor, 2001;Weston et al., 2012;. However, none of this research has focused on detailed assessment of the distribution and diversity of specific taxon, or specifically investigated the diversity and abundance of sunbird species (Nectariniidae). ...
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... Interactions of birds with their food plants have been widely reported to be regulated by plant structures (Weston et al. 2012;Wenny 2016;Tella et al. 2020). The interaction and close association of avian frugivores with mistletoes may be further enhanced, because these fruit dispersers may find the fruit reward available all year round in some species (Mellado and Zamora 2016) or at times of general food scarcity (Grebriel 2017; Koenig et al. 2018). ...
... However, generally, frugivores are considered as the legitimate fruit dispersers, because they often swallow and peck on mistletoe fruits (Corlett 2017). The long-tailed Glossy Starling was found foraging both on the nectar and fruits of T. dodoneifolius mistletoes in the present study, which corroborates with the findings that some bird species act as pollinators as well as seed dispersers (Kuijt 1969;Robertson et al. 1999;Aizen 2003;Weston et al. 2012). Additionally, several avian insectivores visited T. dodoneifolius mistletoes in the present study, suggesting that they provide foraging opportunities as many insects are associated with mistletoes as both pollinators and herbivores (Shaw et al. 2004;Watson 2009). ...
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... However, across Africa in many cases there is no obvious trait matching between flower traits and sunbird bills (Pauw, 1998;Rebelo, Siegfried & Crowe, 1984;Turner & Midgley, 2016) and often sunbird-visited flowers may be primarily pollinated by insects (Nsor & Chapman, 2013;Padyšáková, Bartoš, Tropek & Janeček, 2013). Even when a plant depends on sunbird pollination for seed set (e.g., Bartoš et al., 2012;Beavon & Chapman, 2011;Turner & Midgley, 2016;Weston, Chapman, Kelly & Moltchanova, 2012), they are likely pollinated by more than one sunbird species. ...
... While one explanation could be the relative paucity of flowers with adaptations for bird pollination, some kind of niche complementarity does exist. For example, the mistletoe G. braunii, totally dependent on sunbirds for seed set (Weston et al., 2012), is only visited by three sunbird species from the genus Cinnyris, but we found pollen on the bills of only two of these, the orange-tufted and northern Double-collared Sunbirds. Similarly, the strictly bird-pollinated A. noldeae (Beavon & Chapman, 2011) was visited by six sunbird species but pollen was only found on the bills of the northern double-collared and variable sunbirds. ...
Article
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Sunbirds play a major role in the pollination of Old World nectivorous plants. However, with the exception of the Cape Floristic Region there is a major knowledge gap around African nectivore interaction networks—a stark contrast from the abundance of neotropical hummingbird–plant networks. Here, we describe a sunbird pollen transfer network (PTN) which we use in conjunction with a sunbird flower visitation network (FVN) to explore levels of sunbird specialization within an Afromontane forest habitat. Both networks were generalized compared with similar‐sized hummingbird networks, reflecting the wide range of flower types visited, the generalist diet, and bill characteristics of sunbirds. Three sunbird species from the genus Cinnyris accounted for 85% of flower visits and 77% of all pollen transported. Of the 17 plant species across both networks, 15 are predominantly pollinated by insects while Anthonotha noldeae (Fabaceae–Caesalpinioideae) and Globimetula braunii (Loranthaceae) depend on sunbirds for seed set. Sunbird species average bill lengths varied between 14.5 mm (the variable sunbird) and 23.6 mm (the Green‐headed Sunbird), but, while more pollen was carried on longer bills, we found no evidence for a relationship between bill length and type of flower visited. Both networks were nested. Some specialization was observed in both networks although this does not appear to be driven much by sunbird–flower trait matching. Overall, our results suggest that in contrast to nectivores elsewhere, factors such as phenology and/or environment, rather than morphology, may play important roles in limiting potential sunbird–flower interactions and need further investigation.
... Leonotis nepetifolia is pollinated by large sunbirds, but its flower shape does not show specific adaptations to particular species (Gill & Conway, 1979). Members of the Loranthaceae family are well known to be specialized for bird pollination (Polhill & Wiens, 1998), but again no adaptations for particular bird species have been reported (Gill & Wolf, 1975;Weston et al., 2012). Tight specializations have been suggested within the families Marantaceae and Balsaminaceae. ...
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I used field experiments to examine the effect of pollinator sharing on seed set in the understory herb Stellaria pubera. In piedmont North Carolina the solitary bee and fly pollinators of this species are also frequent visitors to Claytonia virginica. Removals of nearby flowers of C. virginica increased seed set of S. pubera. Examination of seed set in populations of potted plants indicated that the effect was due to change in species composition rather than plant density. Variation in seed production was high, however, and even when flowers were provided with excess pollen through supplemental hand pollinations, only 20% of ovules produced seeds. Competition for pollination appears to be one of several selective forces that act on blooming time of S. pubera. Stellaria pubera blooms slightly later than C. virginica. Whereas the seeds set of early flowers was increased 13% by removal of C. virginica and 19% by hand pollination, seed set of late flowers was unaffected. Plants forced to bloom early also tended to be more pollinator-limited than control plants. Removal of C. virginica did not, however, increase the seed set of S. pubera plants forced to bloom early significantly more than that of control plants. Other forces are probably also involved in the maintenance of blooming time.
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Dispersal patterns of Loranthaceae are described, the main agents being tinkerbirds (Pogoniulus, Capitonidae), and flowers generally being well-adapted for bird pollination. The biogeography of different species is outlined, some with maps. The oldest sections show a fragmented distribution of species with strong intercontinental connections. The more advanced sections show a strong latitudinal or longitudinal bias. Only slight visible modifications exist as a result of speciation from the equatorial forests into the wooded grasslands and woodlands to the north and south. Contrasts exist between the uniformity of the dispersal arrangements and the high levels of speciation and convergence of the pollination mechanisms. -S.J.Yates
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Diurnal visitors to the flowers of many native plant species were identified in a wide range of Tasmanian sclerophyllous vegetation between September 1996 and April 1997. These foraging profiles were analysed to determine whether they were characteristic of various floral morphologies in predictable ways. It was found that although visitor profiles were sometimes consistent with classic pollination syndromes, these syndromes were unreliable predictors of floral visitors. Very few flowers were exclusively bird-pollinated, and none were strictly fly-, beetle-, wasp-, or butterfly-pollinated. The majority of flowering plants were unspecialized in their morphology, and consequently hosted a diverse array of visitors. In addition, visitor profiles to congeners with similar floral morphologies, and even to conspecifics, differed between habitats. Altitude was a major factor in determining visitors, with flies being the most abundant visitors above 700 m. However, congeners in several genera of Epacridaceae, as well as the genus Correa, which differed in floral morphology also differed in visitor profiles. Tubular flowers were associated with birds, while flowers with more accessible nectar were visited by insects. The only taxa exhibiting a bee-pollination syndrome that were largely visited by bees were the Fabaceae and Goodenia ovata Sm. Several species with purple or pink flowers were also predominantly visited by bees, but did not strictly conform to the melittophilous syndrome. In contrast, other flowers exhibiting an ostensibly mellitophilous syndrome hosted very few bees. Of these, species that occurred at high altitude were mainly visited by flies, while others received very few potential pollen vectors.
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We conducted a comparative analysis to determine life history and ecological correlates of pollen limitation among 224 species of animal-pollinated flowering plants. To test predictions concerning the occurrence of pollen limitation, species were classified categorically for six life-history traits (self-compatible vs. self-incompatible, autogamous vs. non-autogamous, specialized vs. unspecialized floral morphology, nectariferous vs. nectarless, monocarpic vs. polycarpic, herbaceous vs. woody) and two ecological conditions (presence in open vs. forested habitats and temperate vs. tropical biomes). Pollen limitation of species in contrasting categories was compared using non-parametric tests (TIPs analysis) and phylogenetically-independent contrasts (PICs). The results of TIPs and PICs analyses were generally congruent, although fewer significant contrasts were evident with PICs, probably because of low statistical power. Overall the results suggest that the influence of phylogenetic history on the intensity of pollen limitation was not particularly strong. Nonetheless, significant variation in the degree of pollen limitation was demonstrated among seven angiosperm families suggesting some phylogenetic component to the phenomenon. With both TIPs and PICs, pollen limitation was less intense in self-compatible and autogamous species. TIPs analysis demonstrated that herbaceous, nectariferous, and temperate species were less likely to be pollen-limited, but using PICs this could only be corroborated for those that were self-incompatible. None of the traits were singularly unambiguous predictors of pollen limitation, possibly reflecting the stochastic nature of pollinator service.