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A snake in paradise: Disturbance of plant reproduction
following extirpation of bird flower-visitors on Guam
Hanne Skovgaard Mortensen, Yoko Luise Dupont*, Jens M. Olesen
Department of Biological Sciences, University of Aarhus, Ny Munkegade Block 1540, DK-8000 Aarhus C, Denmark
A R T I C L E I N F O
A B S T R A C T
Article history:
The introduction of an alien top predator, the brown treesnake (Boiga irregularis), has
Received 29 February 2008
resulted in severe losses of native vertebrate populations in Guam. Among these are impor-
Received in revised form
tant pollinators and seed dispersers. This study is a first attempt to document cascading
14 May 2008
effects on vertebrate-pollinated native plant species in Guam. We investigated flower visi-
Accepted 19 June 2008
tation, seed set and germination in two native plants, the mangrove tree Bruguiera gymno-
Available online 31 July 2008
rrhiza and the forest tree Erythrina variegata var. orientalis. Both species are bird-pollinated.
Studies were conducted on two Mariana islands, Guam (with high density of snakes) and
Keywords:
Saipan (with nearly no snakes). Visitation rates by birds were high on Saipan, but zero
Boiga irregularis
on Guam. Insects and lizards visited flowers to a low extent on both islands. Only lizards
Brown tree snake
were potential effective pollinators. Seed set of both species were significantly higher on
Cascade extinction
Saipan compared to Guam, and for B. gymnorrhiza, seedling recruitment was significantly
Indirect effects
higher on Saipan. Hence, these bird-pollinated species appear highly dependent on bird
Pacific
visitors for reproduction. The eradication of flower-visiting birds by the invasive treesnake
Mariana Islands
thus secondarily results in broken mutualistic interactions, which may, in turn, result in a
lower recruitment of native plants. Thus, the treesnake affects not only potential prey species, but its effects cascade through the entire ecosystem on Guam. Conservation actions
should be directed towards an improved recruitment (artificial pollination, planting) of
the affected plant species.
2008 Elsevier Ltd. All rights reserved.
1.
Introduction
Island species are predisposed to extirpation by invaders due
to their small geographic range and population size, and lack
of coevolution with continental predators and competitors
(Vermeji, 1991; Paulay, 1994; D’Antonio and Dudley, 1998).
An invasion may ramify through the entire island ecosystem
by indirect effects, i.e. one species altering the effect that another species has on a third species (O’Dowd et al., 2003;
White et al., 2006).
One major disturbance on islands is the break-down of
mutualistic plant–animal interactions because of predation
by invasives (Cox and Elmqvist, 2000; Kremen and Ricketts,
2000). Native island plant–animal networks have a markedly
lower ratio of animal to plant species compared to those of
mainland areas (Olesen and Jordano, 2002). Thus, animal-pollinated insular plants are sensitive to extinctions among their
species-poor pollinator fauna (Cox and Elmqvist, 2000). Animal extinctions may result in secondary extinction of plant
species, unless an efficient alternative pollinator or seed disperser replaces the original mutualist partner (Cox, 1983; Olesen and Jain, 1994; Riera et al., 2002; Traveset and Riera, 2005).
It has been suggested that many native island plant
species are dependent on endemic pollinators (Cox and Elmqvist, 2000). In the Pacific Islands, ecosystem-wide studies on
pollination are lacking. However, the emerging picture from
* Corresponding author: Tel.: +45 8942 3127; fax: +45 8942 2722.
E-mail address: [email protected] (Y.L. Dupont).
0006-3207/$ - see front matter 2008 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2008.06.014
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B I O L O G I C A L C O N S E RVAT I O N
a number of case studies is alarming. On some islands entire
sets of pollinators, including native birds, bats, and insects
are disappearing (Fritts and Rodda, 1998; Cox and Elmqvist,
2000). Although cascading effects on plants following extinction of their animal pollinators and seed dispersers have been
suggested, it has rarely been documented (e.g. Bond, 1994).
Secondary extinction and decline of species following extinction of their mutualist partners, may, however, potentially affect a large number of species (Koh et al., 2004).
One of the worst known cases of an introduced predator
species is the brown treesnake (Boiga irregularis) to the island
of Guam (Savidge, 1987; Fritts and Rodda, 1998; Wiles et al.,
2003). The brown treesnake, native to eastern Indonesia,
New Guinea, Solomon Islands and the coastal areas of northern and eastern Australia, was accidentally introduced to
Guam around 1950 (Savidge, 1987; Rodda et al., 1992; Fritts
and Rodda, 1998). The snake rapidly dispersed throughout
the island in the 1980s (Savidge, 1987), reaching a peak density of >100 snakes/ha (Rodda et al., 1992; Rodda and Savidge,
2007). Presently, the population appears to have stabilized at
an equilibrium of c. 50 snakes/ha (Rodda and Savidge, 2007).
The spread of the snake on Guam is directly linked to declines in several animal populations. Since the 1960s, the fauna of Guam has undergone major changes; especially
vertebrate populations have suffered from predation by the
brown treesnake (e.g. Savidge, 1984, 1987; Rodda and Fritts,
1992; Rodda et al., 1997, 1999; Fritts and Rodda, 1998; Wiles
et al., 2003). The most heavily affected species are small birds,
small mammals, and medium-sized lizards (Rodda et al.,
1999). Most native forest bird species have disappeared (Savidge, 1987; Wiles et al., 2003). Six out of 10–12 native lizard
species have been extirpated, and only three species were
common in the late 1990s (Fritts and Rodda, 1998). Likewise,
two of Guam’s three bat species have disappeared (Wiles,
1987; Fritts and Rodda, 1998). The loss of most insectivorous
birds and many lizard species leaves Guam vulnerable to a
variety of insect pests (Fritts and Rodda, 1998; Rodda et al.,
1999). As native birds and fruit bats are important pollinators
and seed dispersers of shrubs and forest trees, predation by
snakes may indirectly affect maintenance of forest diversity
(Fritts and Rodda, 1998; Perry and Morton, 1999). However,
no studies have so far quantified indirect effects of the brown
treesnake. Here we investigate cascading effects by the invasive snake on plant reproduction through its predation on
pollinators.
We compared the reproduction of bird-pollinated plant
species on Guam with that on the nearby island of Saipan,
where the snake is not invasive (Rodda et al., 1999; Vogt and
Williams, 2004; Rodda and Savidge, 2007). The biota of Saipan
is similar to that of Guam. However, no established population of the brown treesnake has been detected to date, and
consequently no major bird, bat and lizard extirpations have
occurred due to predation. In response to hunting, habitat
disturbances and predation by introduced rats (Rattus exulans)
and feral cats (Felis catus), some bird and bat populations have
declined. However, flower-visiting and fruit-eating forest
birds are still numerous on Saipan (Craig, 1996).
As study species, we used two native plant species, the
mangrove tree Bruguiera gymnorrhiza and the canopy species
Erythrina variegata var. orientalis. Bruguiera gymnorrhiza is one
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of the dominant plant species in the ecologically important
mangrove forest, which is in urgent need of conservation
and restoration in the Mariana Islands (Vogt and Williams,
2004). E. variegata var. orientalis is found in the species-rich native forest, of which only small remnants are left in the Mariana Islands. Both B. gymnorrhiza (Tomlinson et al., 1979;
Tomlinson, 1986; Kondo et al., 1987) and Erythrina spp. (Hernández and Toledo, 1982; Bruneau, 1997; Etcheverry and Trucco Alemán, 2005) are considered bird-pollinated. These species
are thus expected to be heavily affected by vertebrate extirpation. Here we approach the questions (1) Do flower-visitors of
the plants differ on Guam and Saipan? (2) Is seed set pollination-limited? and (3) Do recruitment of seedlings and age
structure of the two species differ between the two islands?
2.
Materials and methods
2.1.
Study species
2.1.1.
Bruguiera gymnorrhiza (L.) Savigny (Rhizophoraceae)
This species is native to East Africa, coasts of the Indian
Ocean, Ceylon, Indonesia, Micronesia, Polynesia, northward
to the Ryukyu Islands (Japan) and southwards to tropical Australia (Stone, 1970; Tomlinson, 1986; Allen and Duke, 2006). B.
gymnorrhiza is a medium-sized tree. It is essentially ever-flowering, although seasonal peaks of flowering and fruiting
occurs (Allen and Duke, 2006). Flowers are solitary, large
(c. 4 cm long), hermaphroditic, pendulous and campanulate,
consisting of (8)10–14 petals, which are usually red/orange
and cupped in a reddish tubular calyx (Stone, 1970; Tomlinson
et al., 1979; Tomlinson, 1986). Pollen is released by an explosive mechanism, which is triggered by large flower-visiting
animals (Tomlinson et al., 1979; Tomlinson, 1986; Kondo
et al., 1987). The plant is viviparous. Hypocotyls (germinated
fruits) are up to 25 cm long (Tomlinson, 1986).
2.1.2.
Erythrina variegata var. orientalis (L.) Merr. (Fabaceae)
E. variegata is native throughout the tropical Pacific. On Guam
and Saipan, the variety E. variegata var. orientalis (hereafter E.
variegata) occurs in native forests and is typically found along
or at the top of limestone ridges, often near the sea. In addition, it is widely distributed in other habitats and as a cultivated plant (L. Raulerson, personal communication). It is a
deciduous, upper-canopy tree, which flowers in the dry season in the Marianas. The leguminose flowers are hermaphroditic, bright red, large (c. 6 cm long), and borne in dense
terminal or axillary inflorescences (Stone, 1970; Whistler
and Elevitch, 2006). Inflorescences are up to 20 cm long, consisting of >100 flowers, which open acropetally (personal
observation). Flowering is mostly diurnal with a few open
flowers (8–15) per inflorescence per day (personal observation). Fruits are long, brownish pods, with 5–10 maroon-coloured, kidney-shaped seeds (Whistler and Elevitch, 2006).
2.2.
Study sites
Guam (135 0 N; 14445 0 E) is the largest (560 km2), and southern-most island in the Mariana Archipelago. The second largest island (122 km2) is Saipan (1512 0 N; 14543 0 E), c. 200 km
northeast of Guam, with three smaller islands intervening.
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The Mariana Islands have a tropical oceanic climate with a
uniform temperature year round, and a dry and a rainy
season.
The flora of the Mariana Islands encompasses 1029 native
plant species of which c. 25% are endemic (Stone, 1970; Vogt
and Williams, 2004). The native flora has suffered from various threats, such as the introduction of invasive species, poor
land management practices, and overexploitation. The main
vegetation types are limestone forest, ravine forest, weedy
secondary growth, savanna, wetlands (mangrove), and strand
habitat (Stone, 1970; Vogt and Williams, 2004). Today undisturbed habitats are uncommon on all of the major Mariana Islands (Perry and Morton, 1999).
Bruguiera gymnorrhiza was studied in a small protected
area of mangrove forest at a dry dock in Apra harbour on
the west coast of Guam. On Saipan, B. gymnorrhiza was studied in a small area of mangrove vegetation on the west coast
of the island, west of and within the American Memorial Park.
Tidal conditions and sizes of trees were similar at the study
sites. The mangrove on Guam was dominated by Rhizophora
apiculata (Rhizophoraceae). B. gymnorrhiza was common in
the back mangrove, where the density of R. apiculata was lower. The mangrove on Saipan consisted mainly of dense stands
of B. gymnorrhiza trees.
Erythrina variegata was studied using trees growing in mixed
secondary vegetation and small remnants of native forest.
Unfortunately, no access was provided to the US military areas,
which include most of the remaining native forest on Guam.
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(c. 1 · 6 m). The observation distance was mostly less than
3.5 m, because human presence did not appear to disturb
the activity of flower-visiting animals. Each plot had 80–150
flowers, including buds, newly opened flowers and old flowers. In total, B. gymnorrhiza was observed for 53 h (20 h in period 1 + 33 h in period 2) on Guam and 56 h (23 + 33 h) on
Saipan, representing 2.5 ± 0.9 observation hours (Guam) and
2.7 ± 1.2 h (Saipan) in each hour of the day from 5.00 to
19.30 h. The time spent by a visitor in a flower of B. gymnorrhiza was measured to the nearest 5 min for beetles (N = 20).
Foraging time of the Micronesian honeyeater (Myzomela rubratra) was scored to the nearest 0.5 min by recording the time a
bird was foraging in a plot (N = 20).
No night observations of pollinators were made. As an
alternative, newly opened and untouched flowers of B. gymnorrhiza (N = 100 on Guam, N = 50 on Saipan), were randomly
chosen within the study area and tagged at around 19.00 h.
Before 7.30 h the following morning, flowers were examined
to score if the explosive mechanism of petals had been triggered during the night.
2.3.2.
Erythrina variegata
Flower-visitor observations were carried out in the dry season, from February to June, in two different periods for B. gymnorrhiza and one period for E. variegata on each island (Table
1). Observations were done regularly throughout the study
periods from 5.00 to 19.30 h on days without rain and strong
wind. Average daily temperatures were relatively constant,
c. 27–28 C. Flower-visitors were observed from stationary
posts in 1-hour trials, up to 4 h per day. Observation trials
were preceded by a 5–10 min pre-observation period, in which
visits were not registered. Only animals visiting the flowers
were recorded, and their flower probing behaviour observed.
Four individuals on Guam and five on Saipan were used for
observation. All trees were at least 5 m tall with a large crown,
and flowered throughout the study period. A total of 105 h
were spent on observation, representing 4.0 ± 1.2 observation
hours (Guam) and 3.7 ± 1.3 h (Saipan) in each hour from 5.00
to 19.00 h (18.00 h on Saipan). The number of flowers per tree
was counted or estimated before an observation session using
binoculars (Guam: 46–193 flowers; Saipan: 42–202 flowers).
During an observation trial, flowers of one tree were observed
at a distance of 4–6 m, sometimes using binoculars. A bird visit was defined as the number of bird arriving to a tree during
the observation session.
Furthermore, visitation rate at the level of inflorescence of
the most common visitor (N = 20), bridled white-eye, was recorded as the number of inflorescences visited per bird during
a visit to one tree. In addition, we recorded the number of
birds visiting an inflorescence during 30 min (N = 15). We
monitored visitation rates at the level of tree and inflorescence rather than per flower, because flowers were difficult
to distinguish individually.
2.3.1.
2.4.
2.3.
Visitation rate
Bruguiera gymnorrhiza
Seven plots, each including one individual of B. gymnorrhiza,
were observed on Guam. Because of a high density of trees
on Saipan, flower-visitors were censused in two plots
Pollination experiment
In order to assess the importance of animal pollen vectors for
seed set, we did exclusion experiments. Flower buds were
Table 1 – Flower visitor observations
Observation days
Average daily temperature Ca
15 February – 15 March 2005
17 March – 6 April 2005
7 April –26 May 2005
27 May – 3 June 2005
13
8
10
7
28.2 ± 0.5
27.5 ± 0.5
27.2 ± 0.7
27.7 ± 1.1
12 April – 23 May 2005
18 March – 6 April 2005
16
12
28.3 ± 0.6
27.7 ± 0.5
Plant
Island
Observation period
Bruguiera gymnorrhiza
Guam
Saipan
Guam
Saipan
Erythrina variegata
Guam
Saipan
a Average daily temperature of visitation observation days from weather station at Guam International Airport, www.weather.gov/climate/
index.php?wfo=guam (accessed 28 April 2008).
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bagged in 1 mm meshed nets prior to anthesis to exclude visitors from flowers. As a control, flowers were marked with
flagging tape and left for natural pollination. After flowering
had ceased and fruit development initiated, seed set was recorded. For B. gymnorrhiza seed set was defined as presence
of vivipary.
In B. gymnorrhiza, 300 flower buds from six trees on Guam,
and 50 flower buds from five trees on Saipan were bagged.
Using the same trees, 500 flowers on Guam and 338 flowers
on Saipan were tagged as controls. Instead of buds, flowers
no longer producing nectar were used as controls, because
newly opened flowers were often destroyed by rats on Saipan.
In one E. variegata tree on Saipan, two flowering stems,
each containing more than 200 flowers, were bagged. On a
nearby stem, 112 flowers of an inflorescence were tagged as
controls. Unfortunately other inflorescences were inaccessible because branches bore thorns, and the height of the canopy mostly exceeded 5 m.
2.5.
Seed set and germination
2.5.1.
Bruguiera gymnorrhiza
On both Guam and Saipan, the numbers of buds, flowers and
hypocotyls (germinated fruits) of B. gymnorrhiza were counted
on randomly chosen, large (2.0–2.5 m long) branches of similar size, from four trees. Furthermore, the number and size of
saplings were monitored. On Guam, trees were widely spaced.
Thus, all saplings were counted within a circle of radius 1–
1.5 m around each of 16 large (>2.5 m) trees. Saplings were
classified as small (<0.5 m) or large (0.5–1.5 m). On Saipan,
individual trees could not be delimited due to a high density
of trees. Instead, two plots, 4 · 3 m and 2 · 2 m, which included 18 trees taller than 2.5 m, were chosen, and the number of small and large saplings counted.
2.5.2.
Erythrina variegata
Fruit set was quantified as the number of pods per infructescence (Saipan N = 80; Guam N = 50), and seed set as number of
developed seeds per pod (Saipan N = 85; Guam N = 90). Infructescences and pods were chosen at random from five trees
on Guam and three on Saipan, which had finished flowering.
Number of developed seeds was assessed from the outside of
the fruits as the number of swellings on the pods from five
trees on each island. The proportion of seeds surviving seed
predation was assessed by opening the pods and counting
the number of intact seeds (Saipan N = 1000 and Guam
N = 300 developed seeds).
Seed germination was tested using 110 seeds collected
from P5 trees from each island. Germination experiments
were carried out in a greenhouse in Denmark with an average
daily temperature of 21 C, 90% relative humidity, and average
daylight period of 12:30 h/day ± 56 min. In comparison, climate at the study sites were nearly uniform year-round with
an average daily temperature of 27.3 ± 0.8 C, 77% relative
humidity, and an average daily photoperiod of c. 12:10 h/
day ± 10 min during the germination trial (data from Astronomical Applications Departments, aa.usno.navy.mil/data/,
National Weather Service Forecast Office, www.weather.gov/
climate, and Guam Government, ns.gov.gu/climate). Erythrina
variegata has a wide distribution range, and is known to thrive
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under a range of environmental conditions (Whistler and
Elevitch, 2006). Thus, we did not expect the slightly different
conditions of the greenhouse to strongly affect germination
rate. Before sowing, seeds were treated mechanically by making a small scar, in order to improve their water absorption.
Scarcified seeds have been reported to germinate readily,
mostly 5–10 days after planting (Whistler and Elevitch,
2006). Seeds were sown on the 29th of August 2005. Germination rate was checked weekly, until the experiment was ended
on the 9th of October 2005.
2.6.
Data analysis
Data were analyzed using the statistical software JMP version
7 (SAS Institute Inc., Cary, NC, 1989–2007). Because visitation
rates varied diurnally, paired t-tests were used to assess inter-island variation in visitation rates for each hour of the
day. Student’s t-test was used to test if numbers of flowers
of E. variegata differed between flower-visitor observation trials on Guam and Saipan. Between island differences in pod
set per infructescence and seed set per pod was analyzed
using a nested ANOVA, nesting trees within islands. The variables pod set and seed set were Ln-transformed to conform to
the assumptions of parametric tests. Finally, G-tests were
used to compare numbers of small and large saplings and
trees of B. gymnorrhiza, in addition to germination and survival rate of seeds in both plant species.
3.
Results
3.1.
Flower visitation
Two general trends were observed in patterns of flower-visitation of B. gymnorrhiza and E. variegata. Firstly, visitation rates
were significantly higher on Saipan. Secondly, the most dominant visitors were native birds on Saipan and alien beetles on
Guam.
3.1.1.
Bruguiera gymnorrhiza
A highly significant difference was found in total visitation
rate (including all visitors) of B. gymnorrhiza between the
two islands (paired t-test: t = 7.1, df = 13, P < 0.05). Average daily visitation rate to a tree on Saipan was nearly five times the
visitation rate on Guam (118.0 vs. 26.5 visits/tree/day) (Fig. 1).
Visitation rate of birds was high on Saipan, whereas no
birds were observed visiting the flowers on Guam (paired ttest: t = 8.5, df = 13, P < 0.05). Visitation rate of alternative visitors (insects and lizards) was fairly low on both islands,
although significantly higher on Guam compared to Saipan
(paired t-test: t = 4.2, df = 13, P = 0.05) (Fig. 2a).
No difference was found in diurnal visitation rate (visits/
hour 6.00–19.00 h) between the two study periods on Guam
(paired t-test: t = 2.06, df = 10, P > 0.05). The main flower-visitors were the introduced flower beetles, Oriental flower beetle
(Protaetia orientalis) and Midway emerald beetle (P. pryeri)
(Cetoniidae, Scarabaeoidea). Flower-visiting beetles stayed
on average 34.2 ± 19.1 min on a flower (range 0–75, N = 25).
They most often visited old flowers, and appeared to destroy
the flowers. Occasionally, lizards (Lepidodactylus lugubris and
an unidentified species of skink) were observed drinking nec-
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Fig. 1 – Average daily number of visits/tree to flowers of
Bruguiera gymnorrhizaby insects (black), birds (light grey)
and other visitors (dark grey) during the observation periods
on Guam and Saipan.
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Only two adjacent flowers out of the 100 night-tagged flowers
showed indications of visitation (19.00–7.30 h).
On Saipan, birds constituted 98% of the observed visits,
while the remaining 2% were visits by paper wasps. Hourly
visitation rates (5.00–19.00 h) were slightly higher in the first
observation period (paired t-test: t = 3.5, df = 11, P < 0.01). No
visitors were observed before 5.00 h and after 19.00 h. However, 11 of 50 night-tagged flowers showed signs of gnawing
by rats. Rats were considered nectar thieves rather than pollinators because of their destructive behaviour.
The most common visitor was the Micronesian honeyeater
(Myzomela rubratra) (424 visits), followed by the golden whiteeye (Cleptornis marchei) (35 visits) and the bridled white-eye
(Zosterops conspicillatus) (four visits). Bird activity peaked
around 7.00–11.00 h and again at 15.00–18.00 h (Fig. 2a). On
average, the honeyeaters were foraging for 2.7 ± 1.8 min
(N = 20) per visit in an observation plot. All bird species harvested nectar by perching or hanging from a branch. In newly
opened flowers, the insertion of the bill of a bird into the calyx
tube triggered an explosive pollen release mechanism, depositing pollen on the flower-visitor.
3.1.2.
Erythrina variegata
Total visitation rates was significantly higher on Saipan compared to Guam (paired t-test: t = 3.66, df = 12, P < 0.05). The
average daily number of visits per tree on Guam was <3% of
that on Saipan (6.3 vs. 218.4 visits/tree/day) (Fig. 3). No significant difference was found in the number of flowers observed
during observation trials on the two islands (t-test: t = 0.32,
df = 19, P > 0.05).
As in B. gymnorrhiza, visitation rate of birds was high on
Saipan, while no flower-visiting birds were observed on Guam
(paired t-test: t = 3.73, df = 12, P < 0.01). Visitation rates of
alternative flower-visitors did not differ between the two islands (paired t-test: t = 0.04, df = 12, P > 0.05). On Guam, flow-
Fig. 2 – Diurnal pattern in flower-visitation by birds (white
symbols) and insects + others (black symbols) in plots of (a)
Bruguiera gymnorrhiza and (b) Erythrina variegata var.
orientalis on Guam (triangles) and Saipan (circles). Bird
visitation to E. variegata on Guam is not shown, but no birds
were observed on the flowers throughout the day. Time
denotes starting time of an 1-hour observation period.
tar from flowers. Furthermore, a few paper wasps, praying
mantis, ants and crabs (Foniopsis cruentata) were seen on the
flowers, but they never touched the reproductive parts. No
flower visitors were observed before 6.00 h and after 19.00 h.
Fig. 3 – Average daily number of visits/tree to flowers of
Erythrina variegata var. orientalis by insects (black), birds
(light grey) and other visitors (dark grey) during the
observation periods on Guam and Saipan.
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er-visitors were beetles (P. orientalis and P. pryeri), butterflies,
honeybees (Apis mellifera) and wasps. Insect activity was low
throughout the day (Fig. 2b). Honeybees touched the anthers
and stigma while harvesting pollen, and thus were potential
pollinators. Other insect visitors did not touch the reproductive organs.
On Saipan, the dominant flower-visitors were birds (95.5%
of visits), mainly bridled white-eyes (Z. conspicillatus), but also
a few Micronesian honeyeaters (M. rubratra), golden whiteeyes (C. marchei) and a single black drongo (Dicrurus macrocerus). The remaining 4.5% of visits were by green tree skinks
(Lamprolepis smaragdina), honeybees, wasps and rats. The contribution of insect visitation to the total visitation rate was
found to be almost the same on the two islands (Fig. 3). On
average, 9.9 and 6.3 insect visits per day per tree were observed on Saipan and Guam, respectively. Birds were the only
regular visitors, which made contact with the reproductive
parts, and thus were likely to act as pollinators. Visitation
by birds was highly variable, because they often foraged in
flocks. Bird activity peaked in the morning hours (6.00–
10.00 h), with an average of 195.5 birds per tree per hour
(Fig. 2b). No birds were observed before 5.00 h and after
17.00 h. The most common visitor, the bridled white-eye (Z.
conspicillatus), foraged on an average of 14.7 inflorescences
per visit in a tree (SD ± 10.7, N = 20). Each flower visit only
lasted a few seconds. One inflorescence (with 4–6 open flowers) was on average visited by 6.3 birds during a 30-minute
period (SD ± 3.0, N = 15). Green tree skinks visited flowers less
frequently, but touched reproductive parts while foraging for
nectar, thus acting as a pollen vector.
3.2.
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than on Guam (N = 447, df = 2, G2 = 48.65, P < 0.05), in particular, the proportion of small saplings (<0.5 m) was much higher
on Saipan (Fig. 5).
3.3.2.
Erythrina variegata
Average ± SD number of pods per infructescence (Saipan:
5.63 ± 3.25 (N = 80); Guam: 2.52 ± 1.82 (N = 50)) and average
number of seeds per pod (Saipan: 7.91 ± 2.58 (N = 85); Guam:
3.84 ± SD 1.78 (N = 90)) were significantly higher on Saipan
compared to Guam (Table 2). Pod set per infructescence, but
not seed set per pod, varied among trees (Table 2).
The survival rate of seeds was significantly higher on
Guam (G2 = 214, df = 1, P < 0.01), with an average of 73.3% surviving seeds (N = 300) compared to an average of only 26.4%
on Saipan (N = 1000). All seed destruction was caused by lar-
a
b
Fig. 4 – Proportions of buds (black), flowers (light grey) and
hypocotyls (dark grey) on branches of Bruguiera gymnorrhiza
(four trees) on (a) Guam and (b) Saipan.
Pollination experiment
Vivipary was not observed in bagged flowers of B. gymnorrhiza
(N = 350), indicating that pollination was necessary for seed
set. In contrast, vivipary of control flowers was 5.4% (27 fruits
in two clusters) on Guam and 16.0% on Saipan. Vivipary was
significantly higher on Saipan compared to Guam (N = 838,
df = 1, G2 = 25.35, P < 0.05).
None of the bagged flowers of E. variegata produced seeds,
suggesting self-incompatibility. However, none of the control
flowers set any seed either.
3.3.
Seed and fruit set and seedling recruitment
3.3.1.
Bruguiera gymnorrhiza
The number of hypocotyls relative to flowers and buds per
branch was significantly higher on Saipan than on Guam
(N = 838, df = 1, G2 = 25.35, P < 0.05, Fig. 4). Numbers of small
and large saplings per tree on Saipan were significantly higher
Fig. 5 – Seedlings (<0.5 m) and saplings (0.5–1.5 m)
associated with 16 and 18 trees (>2.5 m) of Bruguiera
gymnorrhiza on Guam (black bars) and Saipan (white bars),
respectively.
Table 2 – Results of nested ANOVA of pod and seed set of Erythrina variegata trees on Guam and Saipan
Independent variable
Transformation
Source of variation
df
SS
F
P
Pods/infructescence
Log
Seeds/pod
Log
Island
Tree [Island]
Island
Tree [Island]
1
6
1
8
22.5
7.1
24.3
1.4
57.5
3.0
106.1
0.8
<0.0001
0.0085
<0.0001
0.621
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vae of the introduced fruit-piercing moth, Eudocima fullonia
(Noctuidae). Germination rates of seeds sown in a greenhouse
were 89% and 85.5% for Guam and Saipan, respectively.
4.
Discussion
4.1.
Broken interactions and alternative pollinators
On Saipan, the mangrove tree B. gymnorrhiza and the forest
tree E. variegata var. orientalis were visited frequently by birds.
Similar native bird species were found on Guam before the
invasion by the brown treesnake. Today, however, no avian
visitors were observed on Guam. On the other hand, other visitor groups may act as alternative pollinators.
In general, visitation by insects to the ornithophilous
plants was low. Two introduced species of flower beetles, P.
orientalis and P. pryeri were the most regular visitors of B. gymnorrhiza, and E. variegata on Guam. A Protaetia species, possibly P. orientalis was first noted on Guam in 1972 (Schreiner
and Nafus, 1986), and the first report of a beetle matching
the description of P. pryeri was in 1990 (Schreiner, 1991). Predation of insectivorous birds by the invasive brown treesnake
may have facilitated the rapid spread of beetles on Guam.
Protaetia orientalis has been introduced to Saipan, but here it
is much less abundant, possibly due to predation by birds
(e.g. kingfishers). Protaetia spp. are known from many islands
(Kato, 2000; Olesen et al., 2002), and scarab beetles are reported as important pollinators of some plant species (Young,
1988; Garcı́a-Robledo et al., 2004). However, Protaetia spp. have
also been reported to eat flowers and to cause damage to
fruits including many crops, on Pacific islands (Jackson and
Klein, 2006).
Beetles may be sufficiently large to trigger the pollen release mechanism in flowers of B. gymnorrhiza, although this
was never observed in the present study. Although some individuals carried pollen (H.S. Mortensen, unpublished data),
their destructive feeding behaviour and preference of old
flowers, suggest that these beetles were inefficient pollinators. In E. variegata, commercial honeybees appeared as legitimate pollinators. Introduced honeybees may sufficiently
pollinate endemic island plants (e.g. Dupont et al., 2004).
However, honeybees were only occasional visitors to E. variegata. Other insect visitors (wasps, ants, praying mantis, and
rats) did not act as pollen vectors of the study species.
Lizards were another group of occasional visitors to flowers of B. gymnorrhiza and E. variegata. The native small day-active gecko, the mourning gecko (Lepidodactylus lugubris) is still
common on Guam (Rodda and Fritts, 1992; Fritts and Rodda,
1998). Although this lizard species is mainly insectivorous
(Vogt and Williams, 2004), individuals were observed drinking
nectar from flowers of B. gymnorrhiza, and touching the reproductive parts. Moreover, several individuals carried pollen
(H.S. Mortensen, unpublished data), indicating that these visitors may act as effective alternative pollinators of B. gymnorrhiza on Guam. Spatially clustered seed sets, as observed in
the present study in B. gymnorrhiza trees on Guam is likely
to be attributed to the visitation behaviour of lizards. Noronha
skinks (Euprepis atlanticus, Scincidae) are reported as pollinators of Erythrina velutina on Fernando de Noronha Archipel-
1 4 1 ( 2 0 0 8 ) 2 1 4 6 –2 1 5 4
ago, northeast of Brazil (Sazima et al., 2005). The introduced
green tree skink (L. smaragdina), which was observed visiting
flowers of E. variegata had a nectar-drinking behaviour similar
to that of the Noronha skinks.
Lizards are important pollinators and seed dispersers on
islands, and may reach high densities because of release from
predators and expansion of their diet to include nectar, pollen
and fruit. Flower-visiting lizards typically seek nectar in flowers or inflorescences with a high nectar production, and flowers, which can be accessed by climbing (Olesen and Valido,
2003). These conditions are met by both B. gymnorrhiza and
E. variegata. Thus, lizards may be the most effective alternative pollinators of these ornithophilous plants on Guam.
4.2.
Plant reproductive failure
Both study plant species are habitat generalists, being able to
grow under a range of physical conditions (Allen and Duke,
2006; Whistler and Elevitch, 2006). Yet, our study suggests that
the plants are vulnerable to lack of pollination. For B. gymnorrhiza, a significantly higher frequency of vivipary and recruitment was found on Saipan compared to Guam, suggesting
importance of avian pollinators for reproduction. For E. variegata, the role of animal pollen vectors could not be assessed
from the current study, because neither bagged nor control
flowers set seed. Natural fruit sets of Erythrina spp. are generally low, mostly a few percent of flowers develop fruit (Feinsinger et al., 1979; Steiner, 1979; Hernández and Toledo,
1982; Etcheverry and Trucco Alemán, 2005). However, as for
B. gymnorrhiza, fruit and seed production of E. variegata was
much higher on Saipan than on Guam.
In both plant species, flower morphology and nectar secretion patterns were similar on the two islands (H.S. Mortensen,
unpublished data), as were abiotic conditions. Seasonal differences in flowering and/or behaviour of the birds are unlikely
to explain the observed differences between flower-visitors
on Guam and Saipan. Firstly, both plant species have extended periods of flowering, covering the entire study period
(Allen and Duke, 2006). Secondly, low seasonal variation in
density has been reported for the three most common species
of flower-visiting birds, Micronesian honeyeater, bridled
white-eye, and golden white-eye (Craig, 1996). Thirdly, nests
of the dominant bird visitor of B. gymnorrhiza, Micronesian
honeyeater, has been observed throughout the period of the
study (Craig, 1996; Sachtleben et al., 2006), while breeding
periods of the main visitor of E. variegata, bridled white-eye,
is consistently outside the study periods (Craig, 1996).
Although we cannot exclude incompatibility or inbreeding
depression of the plant populations on Guam as a factor contributing to low seed set, our results strongly indicate lack of
efficient pollinators as an important cause of low plant
recruitment. Future studies should aim at investigating the
level of pollen limitation, and thus assess the role of avian
pollinators for plant reproduction.
A curious finding was the significantly lower seed predation by fruit piercing moths on Guam compared to Saipan.
This may be attributed to a higher density of spiders on
Guam. Spiders may have benefitted from increased availability of insect prey due to declines of insectivorous vertebrate
species (Rodda et al., 1999).
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B I O L O G I C A L C O N S E RVAT I O N
4.3.
Cascade effects on Guam and other islands
Reproductive failure due to eradication of vertebrate pollinators may occur in other plant species native to Guam. These
include Calophyllum inophyllum, Lumnitzera littorea, Eleaocarpus
joga, Guettarda speciosa, Intsia bijuga and Serianthes nelsonii; all
are species which are thought to be pollinated mainly by birds
or bats (A. Brooke and H.S. Mortensen, unpublished data). Declines of entire pollinator guilds have been reported in other
Pacific Islands (Cox et al., 1991; Cox and Elmqvist, 2000). In
some cases, introduced organisms have substituted extinct
native pollinators (e.g. Cox, 1983), but in other cases the pollinator niches of native plants have remained empty (Cox and
Elmqvist, 2000). Thus, restoring conditions for natural pollination or managing reproduction (e.g. planting of seedlings)
of vertebrate-pollinated plants is critical in the long-term
conservation of native vegetation types on Guam. Efforts are
now made to conserve the few remaining larger areas of
uniform forest vegetation, e.g. the conservation action plan
‘Guam Comprehensive Wildlife Conservation Strategy’
(GCWCS,
2005,
http://www.guamdawr.org/Conservation/
gcwcs2/ (accessed 23 February 2008)). This includes management actions such as ungulate control and planting of native
plant species to enhance habitat quality.
There are few other documented cases where introduced
species have produced such dramatic effects on a native food
web, as is the case for the brown treesnake on Guam (see Section 1). However, the brown treesnake is not unique in terms
of diet or behaviour (Rodda et al., 1997; Rodda et al., 1999), and
the environment of Guam is similar to other oceanic islands.
Thus, cascade effects may occur in other ecosystems, where
invasive predators are introduced (Fritts and Rodda, 1998).
Predation of native vertebrates by invasives is known from
many other islands, e.g. the Hawaiian archipelago, West Indies, and New Zealand have been infested with rats (Rattus
spp.), cats (F. catus), and mongooses (Herpestes spp.) (Atkinson,
1977; D’Antonio and Dudley, 1998). Extinction of important
vertebrate pollinators and seed dispersers disrupt mutualistic
interactions, and hence in turn reproduction and/or distribution patterns of the plant partners (Cox and Elmqvist, 2000;
Riera et al., 2002; Traveset and Riera, 2005). Island populations
of plants are vulnerable because of reduced genetic diversity,
small population size, and obligate dependence on a depauperate set of pollinating species (Cox et al., 1991; Paulay,
1994; Francisco-Ortega et al., 2000). Hence, the disruption of
plant–pollinator interactions may play an important role in
plant extinction on islands.
5.
Conclusion
The introduction of an alien top predator, the brown treesnake (Boiga irregularis), has caused a cascade of unforeseen
effects on the ecosystem of Guam. Several native vertebrate
species have been extirpated, including important pollinators
and seed dispersers. The plant species of this study, and possibly several other native plant species on Guam, are dependent on pollination by birds. Thus, extirpation of birds
results in broken mutualistic interactions. Although alternative pollinators are attracted to the flowers, these only par-
1 4 1 ( 2 0 0 8 ) 2 1 4 6 –2 1 5 4
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tially fulfill the role as efficient pollen vectors, resulting in
low recruitment, and consequently a decline in native plant
populations. The case of Guam illustrates ramifications of
indirect effects of an invasive predator throughout an island
ecosystem, and highlights the importance of dealing with
introduced species and invasional problems worldwide.
Acknowledgements
We thank Anne Brooke for valuable discussion, logistic support and help in the field, Lynn Raulerson and Aubrey Moore
for answering questions, and Diana Greenough and Laura L.
Williams for logistic support. Jørgen Christiansen, Påskehøjgaard Experimental Farm (University of Aarhus) is thanked
for help during the germination experiments. We are grateful
to Jannie Fries Linnebjerg, Anne Brooke, and two anonymous
referees for constructive comments on an earlier draft of the
manuscript. This project was funded by the University of Aarhus faculty foundation (H.S.M.), the Carlsberg Foundation
(Y.L.D.) and the Danish Science Research Council (J.M.O.).
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