1 23
Biological Invasions ISSN 1387-3547 Biol InvasionsDOI 10.1007/s10530-014-0676-3
Biotic resistance and invasional meltdown:consequences of acquired interspecificinteractions for an invasive orchid,Spathoglottis plicata in Puerto Rico
James D. Ackerman, Wilfredo Falcón,Jonathan Molinari, Carlos Vega,Isamalish Espino & Ana A. Cuevas
1 23
Your article is protected by copyright and
all rights are held exclusively by Springer
International Publishing Switzerland. This e-
offprint is for personal use only and shall not
be self-archived in electronic repositories. If
you wish to self-archive your article, please
use the accepted manuscript version for
posting on your own website. You may
further deposit the accepted manuscript
version in any repository, provided it is only
made publicly available 12 months after
official publication or later and provided
acknowledgement is given to the original
source of publication and a link is inserted
to the published article on Springer's
website. The link must be accompanied by
the following text: "The final publication is
available at link.springer.com”.
ORIGINAL PAPER
Biotic resistance and invasional meltdown: consequencesof acquired interspecific interactions for an invasive orchid,Spathoglottis plicata in Puerto Rico
James D. Ackerman • Wilfredo Falcon •
Jonathan Molinari • Carlos Vega •
Isamalish Espino • Ana A. Cuevas
Received: 5 September 2013 / Accepted: 12 March 2014
� Springer International Publishing Switzerland 2014
Abstract Invasiveness of non-native species often
depends on acquired interactions with either native or
naturalized species. A natural colonizer, the autoga-
mous, invasive orchid Spathoglottis plicata has
acquired at least three interspecific interactions in
Puerto Rico: a mycorrhizal fungus essential for seed
germination and early development; a native, orchid-
specialist weevil, Stethobaris polita, which eats peri-
anth parts and oviposits in developing fruits; and ants,
primarily invasive Solenopsis invicta, that forage at
extrafloral nectaries. We tested in field experiments
and from observational data whether weevils affect
reproductive success in the orchid; and whether this
interaction is density-dependent. We also examined
the effectiveness of extrafloral nectaries in attracting
ants that ward off weevils. Only at small spatial scales
were weevil abundance and flower damage correlated
with flower densities. Plants protected from weevils
had less floral damage and higher fruit set than those
accessible to weevils. The more abundant ants were on
inflorescences, the less accessible fruits were to
weevils, resulting in reduced fruit loss from larval
infections. Ants did not exclude weevils, but they
affected weevil activity. Native herbivores generally
provide some biotic resistance to plant invasions yet
Spathoglottis plicata remains an aggressive colonizer
despite the acquisition of a herbivore/seed predator
partly because invasive ants attracted to extrafloral
nectaries inhibited weevil behavior. Thus, the invasion
of one species facilitates the success of another as in
invasional meltdowns. For invasive plant species of
disturbed habitats, having ant-tended extrafloral nec-
taries and producing copious quantities of seed, biotic
resistance to plant invasions can be minimal.
Keywords Ants � Extrafloral nectaries �Florivory � Seed predation � Plant invasion �Orchidaceae �Weevils
Introduction
When plants experience dispersal through natural or
human-assisted means that carry them beyond their
Electronic supplementary material The online version ofthis article (doi:10.1007/s10530-014-0676-3) contains supple-mentary material, which is available to authorized users.
J. D. Ackerman (&) � W. Falcon � J. Molinari �C. Vega � I. Espino � A. A. Cuevas
Department of Biology, University of Puerto Rico,
PO Box 23360, San Juan, PR 00931-3360, USA
e-mail: [email protected]
J. D. Ackerman � C. Vega � A. A. Cuevas
Center for Applied Tropical Ecology and Conservation,
University of Puerto Rico, PO Box 23341, San Juan,
PR 00931-3341, USA
Present Address:
W. Falcon
Institute of Evolutionary Biology and Environmental
Studies, University of Zurich, Winterthurerstrasse 190,
8057 Zurich, Switzerland
123
Biol Invasions
DOI 10.1007/s10530-014-0676-3
Author's personal copy
native range, the suite of species with which they
interact may be quite different from that of their
original distribution (Mitchell et al. 2006). The loss or
gain of species interactions may strongly influence
whether an immigrant plant becomes established,
naturalized, and capable of successfully spreading to
additional locations (e.g., Williams and Karl 1996;
Nunez et al. 2009; Liu and Pemberton 2010). Those
interactions gained in novel sites can have either
positive or negative effects, and when multiple species
interactions are involved, they can have unforeseen
consequences (Prider et al. 2010), non-additive or
synergistic, as when non-indigenous species facilitate
the invasion of others (invasional ‘‘meltdown’’, e.g.,
Simberloff and Von Holle 1999; Lach et al. 2010).
Such processes can have severe impacts on native
species and ecosystem integrity (e.g., O’Dowd et al.
2003), especially for island systems (Kueffer et al.
2010).
Most invasive species tend to be generalists
because species-specific interactions are not likely to
be transferrable from native to novel sites (Richardson
et al. 2000). This may explain why orchids, many of
which are renowned for highly specific interactions,
are disproportionately underrepresented among inva-
sive species (Tremblay 1992; Otero et al. 2002;
Daehler 1998; Waterman and Bidartondo 2008;
Swarts et al. 2010; Pauw and Bond 2011; but see
Ogura-Tsujita and Yukawa 2008; Gowland et al.
2013), despite having dust-like seeds, often occurring
in disturbed ephemeral habitats, and behaving as
metapopulations (Ackerman 1983; IUCN/SCC Orchid
Specialist Group 1996; Tremblay et al. 2006). Cur-
rently, less than 0.1 % of nearly 30,000 orchid species
are known to be invasive, and a search for a common
denominator in ecological and reproductive traits
among some of them has given equivocal results
(Ackerman 2007). An alternative approach would be
to assess the capacity for orchid species invasiveness
based on common conceptual themes in invasion
biology such as enemy release, biotic resistance, and
invasional meltdown, all of which may involve multi-
species interactions.
Our subject is Spathoglottis plicata Blume, the
‘‘Philippine Orchid’’, a native of SE Asia, Malaysia,
Indonesia, northeastern Australia, Melanesia and the
Philippines. It is a natural colonizer of disturbed
habitats and has the distinction of being one of the first
vascular plants to become established on the remnants
of Krakatau after the 1,883 explosion destroyed the
island (Partomihardjo 2003). Within its native range,
S. plicata engages in at least three significant inter-
specific interactions. The first involves mycorrhizal
fungi. As in all orchids, successful germination
appears dependent on exploiting a fungus, an interac-
tion that may be parasitic at first and mutualistic later.
It is usually maintained throughout its lifetime, though
not necessarily with the same fungus (Rasmussen
1995; McCormick et al. 2006; Cameron et al. 2006,
2008). The second interaction involves pollinators.
Large bees, e.g. Xylocopa spp., are pollinators in both
native and invasive parts of its range. However, some
native populations of the orchid are autogamous
(T. W. Yam, E. de Vogel, M. Clements, pers. comm.
2011). The third interaction involves extrafloral nec-
taries (circumfloral nectaries of Rico-Gray and Thien
2007) whereby the plant offers a resource sufficiently
attractive to ants that they would defend it, providing
the plant with defense against herbivores (Rico-Gray
and Thien 1989; Subedi et al. 2011). Although we do
not know what herbivore pressure S. plicata experi-
ences within its native range, the distribution of the
orchid does overlap with the florivorous orchid-weevil
genus, Orchidophilus (Curculionidae). Both larvae
and adults of these weevils are known to cause
significant damage to a spectrum of orchid genera,
including Spathoglottis (Swezey 1945; Hara and Mau
1986; Prena 2008). In addition, we have seen herbar-
ium specimens of S. plicata at Kew that had been
collected from its native range and have insect damage
very similar to what we observe in Puerto Rico.
Throughout the tropics, Spathoglottis plicata has
been introduced and has become naturalized in many
regions, from Hawai’i to Central America, the Carib-
bean, parts of Africa, and the Mascarene Islands
(Catling 1990; Ackerman 1995; Jolliffe 2010). While
likely losing the species with which it had associated
in its native range, S. plicata has either found them in
its novel range, circumvented the need for them, or has
encountered substitutes. Plants that have escaped
cultivation are the self-pollinating forms so the
absence of pollinators is not a problem. We assume
that S. plicata either engages widespread mycorrhizal
fungi or can utilize a broad range of species, as do
some other weedy and widespread orchids (Otero et al.
2004; Bonnardeaux et al. 2007; Ogura-Tsujita and
Yukawa 2008). As for ants and extrafloral nectaries
(EFN), these are generally not highly specific
J. D. Ackerman et al.
123
Author's personal copy
interactions (Schemske 1982) and those of orchids are
no exception (Fisher and Zimmerman 1988; Damon
and Perez-Soriano 2005). Thus, novel habitats now
occupied by S. plicata likely have ants that forage at
EFN, as they do in the Caribbean island of Guadeloupe
(Jaffe et al. 1989). This interaction, though, may not be
relevant if the orchid left its enemies behind and did
not acquire new ones. Such conditions form the basis
for the enemy release hypothesis, a commonly
invoked explanation for invasion success (Elton
1958; Keane and Crawley 2002; Liu and Stiling
2006, but see Chun et al. 2010).
From a single population 30 years ago, the autog-
amous Spathoglottis plicata has spread across the
Caribbean island of Puerto Rico. While the orchid may
have escaped from enemies of its original distribution,
in Puerto Rico it has encountered new ones. Occa-
sionally, scale insects are found on inflorescences, rust
fungi are on the leaves, and cows eat all the above-
ground parts. The most commonly encountered neg-
ative interaction involves a weevil, the native orchid
specialist, Stethobaris polita (Chevrolat) (Curculion-
idae, Baridinae) (O’Brien and Turnbow 2011), which
damages flowers, fruits, and inflorescence rachises
(Fig. 1; Supplemental material). This interaction con-
stitutes biotic resistance, as inflorescence-feeding
insects can have a dramatic negative impact on plant
population growth (Louda and Potvin 1995). We
already know that the orchid in its native range is
weedy and in Puerto Rico it is rapidly spreading across
the island, suggesting that such resistance is weak,
perhaps altered by a third trophic interaction.
Spathoglottis in Puerto Rico are frequently visited
by foraging ants, mostly exotic Solenopsis invicta, to
tend EFNs. These ants are particularly common in the
open disturbed habitats favored by the orchid. We
occasionally observed ants attacking the weevil, their
expected role in this ant-plant interaction.
What are the consequences of acquired interactions
to reproductive success in Spathoglottis plicata?
Although we do not expect an orchid invasion to have
substantial ecosystem consequences (Simberloff
2011), the links that they establish may illustrate the
extent by which seemingly innocuous invaders are
integrated into the community. Herein we examine the
multispecies interactions involving the exotic orchid,
invasive ants, and a native insect florivore/seed
predator. Using field experiments and observational
data, we ask whether the weevil affects reproductive
success of the orchid and whether ants provide
protection services for the plant. Do weevils damage
Spathoglottis flowers and reduce plant reproductive
success? Are ants that are attracted to extrafloral
nectaries effective defenders of Spathoglottis flowers?
We expected that plants attacked by weevils would
have lower fruit set than weevil-free plants. We also
expected that ants exploiting extrafloral nectaries
would ward off intruders such as weevils resulting in
higher fruit set than in plants in which ants are
excluded. Furthermore, we ask if weevil infestation is
density-dependent by relating weevil frequency and
fruit production with Spathoglottis population densi-
ties. Based on answers to these questions, we speculate
on the future of Puerto Rican populations of this
orchid, and the implications for naturally weedy,
invasive plants.
Methods
Primary field site
Our field primary site was located along Highway 10,
at about 225 m elevation in the municipality of
Arecibo, Puerto Rico (18�2001200N, 66�4003600W).
The highway runs through a complex karst region
composed of haystack hills and sinkholes locally
known as the ‘‘mogotes’’. The region lies at the border
of the subtropical moist and wet forest life zones of the
Holdrige Life Zone system (Ewel and Whitmore
1973) where annual precipitation is 1,651–2,159 mm
and average maximum temperatures vary 29.5–30 �C.
An evergreen, broadleaf forest covers the area, but the
Spathoglottis grow along open road cuts among
grasses, ferns and scattered shrubs up to the forest
edge. Populations in the area are a mixture of both
white and pink flowered individuals.
The species
Spathoglottis plicata are caespitose herbs dependent
on seed production and wind dispersal for population
growth and spread. In Puerto Rico populations flower
and fruit throughout the year (voucher: Maldonado
and Fagua 2, UPRRP). Plants generally produce one
racemose inflorescence at a time. The autogamous
flowers are produced sequentially and offer no nectar
or any other pollinator rewards. There are two color
Biotic resistance and invasional meltdown
123
Author's personal copy
forms, white and pink, both of which we included
since preliminary studies revealed no ant or weevil
preferences. Undamaged flowers remain open for
several days until fruits begin to develop. Unpollinated
flowers and aborted fruits dehisce leaving a noticeable
scar on the raceme. Extrafloral nectaries occur on
buds, young flowers, ovaries, and fruits. Perianth
EFNs seem to become inactive shortly after the buds
open. Jaffe et al. (1989) found that extrafloral nectar
produced by S. plicata in Guadeloupe contained
approximately 35 % sugar, mostly glucose, and an
inflorescence with 10 flowers and 12 fruits produced
0.5 ml of extrafloral nectar in 48 h.
Stethobaris polita are small, black weevils
(2.8–3 mm long) native to Puerto Rico, Dominica,
Guadeloupe and St. Vincent (Fig. 1; O’Brien and
Turnbow 2011). In Puerto Rico it is widespread in
moist to wet habitats from near sea level to approx-
imately 780 m elevation. Specializing on orchids,
adults are florivorous (Wolcott 1948) and lay their
eggs in developing fruits and perhaps inflorescence
rachises as well (Light, pers. comm. 2011). Exit holes
in rotting fruits are commonly seen, as are larvae when
we open deformed fruits. The weevils show no
preference for flower color form (average number on
pink-flowered inflorescences: 1.24, N = 55; white:
Fig. 1 Spathoglottis plicata interactions. a The orchid weevil,
Stethobaris polita, on a damaged pink flower. b Heavily
damaged white-flowered inflorescence. c Solenopsis invicta, red
fire ants, attacking the orchid weevil. d Orchid weevil
ovipositing in damaged developing fruit
J. D. Ackerman et al.
123
Author's personal copy
1.40, N = 50; t test = - 0.65, p = 0.52), The most
severely damaged inflorescences have rotting fruits,
buds and rachis apices. A larger, unidentified weevil
was also seen on the flowers but only very rarely.
The easily identifiable invasive red fire ants,
Solenopsis invicta Buren, are native to South America
and have been in Puerto Rico for more than three
decades where they are currently distributed through-
out the island (Buren 1982; Davis et al. 2001). The
timing of their spread roughly corresponds to that of
Spathoglottis plicata, but began in the southern dry
regions of the island eventually spreading northward
into wetter habitats. The fire ants out-number other
species of ants on Spathoglottis inflorescences by 2–1
in our study site, a common pattern found in areas
invaded by non-native ants (Lach 2003 and references
therein; Savage et al. 2009). They were also the only
ants that we consistently observed to interact aggres-
sively towards the weevil (Fig. 1; Supplemental
material). White flowered inflorescences generally
had more ants than pink-flowered ones, so we included
flower color as a random effect in our Generalized
Linear Mixed Model analyses (see below).
Effects of weevils and ants
From September 2009 to May 2010, we conducted a
field exclusion experiment designed to detect the
effects of weevils and ants on fruit set. We chose a site
that was not visible from the road (exclusion cages
may attract vandalism) and by happenstance it was a
population of almost entirely white-flowered plants.
We selected 68 plants with developing inflorescences
and randomly assigning them to one of four treat-
ments: (1) control (n = 20), (2) ant-exclusion
(n = 18), (3) weevil exclusion (n = 16), (4) ant and
weevil (total) exclusion (n = 14). The controls were
unmanipulated. Ants were excluded by applying
Tangle Trap� (a very tacky, non-toxic, petroleum
product) to the base of the inflorescence and cutting
away any vegetation in contact with the inflorescence.
There were no apparent ill effects on the plant caused
by the application of the Tangle Trap. Weevils were
excluded by covering inflorescences with a cylinder
composed of a stiff wire frame covered by a fine fabric
netting, loosely secured at the base to allow access by
ants. Total exclusion was accomplished by applying
tangle trap to the base of the scape and by covering it
with the fine net cylinder, and firmly securing the
netting to the base of the inflorescence. We tested for
morphological bias among our four groups by com-
paring the average number of leaves, the length of the
longest leaf and height of the inflorescence with single
classification ANOVAs. There were no differences
among the groups. During the experiment, usually
once a week, we counted the number of flowers and
fruits produced and the number of weevils and ants on
the inflorescences. Each inflorescence was checked
2–5 times, depending on the duration of flowering.
Any treatment plant that failed to exclude its target
taxon was immediately removed from the experiment
and substituted with another inflorescence. We com-
pared differences in mean fruit set among the four
treatment groups. Because our field data were often
populated by zeros and consequently were irrevocably
non-normal, we used non-parametric statistics (Wil-
coxon and Kruskal–Wallis) to test differences among
treatment groups for weevil abundance and overall
fruit set. To establish the relationship between weevil
and ant abundance, and the abundance of ants or
weevils with fruit set, we used Spearman’s Rank
Correlation analyses. To determine whether the
frequencies of weevil and ant presence were indepen-
dent of one another, we employed a Chi square test of
independence. All statistical tests were a priori and run
on JMP� software, except for Kendall’s tau, and the
GLMM analyses described below, which were run on
R (2.11.1).
We sought evidence of ant and weevil abundance
and their relationship with S. plicata reproductive
success. We established fifteen 2 9 2 m plots each
with a minimum of 6 new inflorescences. Plots
contained both pink and white forms, but the latter
were dominant. Weekly from 15 Oct to 12 Nov 2011,
we counted the number of ants and weevils on each
flowering inflorescence once in the morning and once
in the afternoon. We also recorded the extent of
weevil damage to flowers in the inflorescences. We
considered the flowers as damaged when weevil
damage to the perianth was [20 % (estimated by
visually assessing each flower of the inflorescence).
At the end of the monitoring period we assessed the
total number of fruits produced, the proportion
damaged by weevil oviposition, and the proportion
of inflorescences with damaged apical meristem per
plot. With Pearson correlations coupled with linear
regressions we tested the relationship between ant
abundance and fruit set, and ant abundance and weevil
Biotic resistance and invasional meltdown
123
Author's personal copy
abundance, and weevil abundance and flower damage.
We also used generalized linear mixed models
(GLMM) to reveal the importance of the mean
number of ants and weevils per inflorescence on the
reproductive output of the invasive orchids. We fitted
the GLMMs using a binomial distribution and Laplace
approximation, taking into account the variable inter-
actions, effects of overdispersion due to individual
inflorescence variation (influencing only the variance
of the reproductive output), and setting plots and
flower color as sources of random variation. Weevil
damage to the inflorescences represents a two-step
process in which (1) weevils feed on flowers (prob-
ably reducing the number of flowers that turn into
fruits) and then (2) weevils oviposit in the fruits, thus
limiting the number of fruits that contribute to the
production of seeds. We modeled this by using the
following response variables: (1) the proportion of
flowers that turn into fruits (‘‘Fundamental fruit set’’),
(2) the proportion of fruits that survive without weevil
oviposition (‘‘Fruit survival’’), and (3) the combined
process, where we used the proportion of flowers that
turn into fruits and are not damaged by weevil
oviposition (‘‘Realized fruit set’’). For the different
measures of reproductive success, we compared three
different models in a stepwise fashion, going from the
more complicated model to the simplest one, such
that: (A) the complex model includes the mean
number of ants and weevils present at the inflores-
cences as well as their interaction, (B) the interme-
diate model does not consider the interaction between
variables and (C) the simplest model only considers
the one variable that significantly affects the repro-
ductive output in the previous models (if detected).
The models were fitted using the R package ‘lme4’.
To assess the quality of the models, we used the
Akaike Information Criterion (AIC).
Ant: weevil interactions
We sought to determine whether the presence of ants
on inflorescences influenced weevil behavior, which
may explain variation in weevil effects on fruits. We
monitored weevils on 32 inflorescences without ants
and 29 inflorescences with ants. This was done in two
sampling events (January and August 2013). From
mid morning to mid afternoon, we made observations
to each inflorescence at 30 s intervals for an 8 min
period. We recorded the mean number of ants and
weevils on each inflorescence during the observation
period, and whether the weevils were active (copulat-
ing, eating, ovipositing, wandering), or inactive (not
moving). In cases where there was more than one
weevil, we randomly chose and followed one individ-
ual. We compared the proportion of time spent on
active behavior on ant-occupied versus ant-free inflo-
rescences with a Mann–Whitney U-test, and assumed
temporal variation to be insignificant. We also fitted
GLMMs to control for the influence of the number of
weevils and ants on inflorescences (modeled as fixed
effects in addition to ant attendance), and sampling
period and flower color (modeled as random effects)
on the behavior of the weevil individuals that we
followed. The effect of overdispersion due to individ-
ual inflorescence variation was included as indicated
previously.
Density effects
Is the abundance of weevils on Spathoglottis inflores-
cences related to Spathoglottis densities? We expected
that the more Spathoglottis flowers at a site the more
apparent the flowers would be, which would attract
more weevils. Furthermore, we sought to determine
whether there was a positive relationship between
weevil numbers and floral damage. At sites in
proximity to the exclusion experiment, we used two
methods to estimate Spathoglottis flower densities. In
2008–2009 we haphazardly selected a ‘‘target’’ plant
bearing an inflorescence (98 pink-flowered plants, 99
white), and then measured the distance to the five
nearest neighbors (NN) of flowering Spathoglottis.
Each target plant was selected so that it did not share
near neighbors with any other target plant. We counted
the number of flowers on each of the NN plants and
divided the average number of NN flowers by the
average NN distance to the target plant. This ratio was
our measure of density, which we compared with the
abundance of beetles and floral damage on target
plants. We performed linear regression analyses on
Spathoglottis densities versus weevil densities and
flower damage on target plants. In this NN study, we
did not assess ant abundance.
Our second method examined density relationships
at a smaller scale. Here we used flower density data
from the 2 9 2 m plots of the 2011 ant/weevil study.
We examined the relationships between Spathoglottis
flower densities and both weevil abundance and flower
J. D. Ackerman et al.
123
Author's personal copy
damage (as dependent variables) using linear regres-
sion analyses.
Results
Effects of weevils and ants
Average number of weevils per flower was not
significantly different between the ant exclusion and
control treatments (Wilcoxon test, v2 = 2.94,
p = 0.09), despite the fact that weevils averaged
0.34 (SD = 0.49) per flower without ants, and controls
had 0.15 (SD = 0.28). Among control plants
(N = 20) the number of ants was not correlated with
the number of weevils per flower (Spearman’s rank
correlation, r = 0.31, p = 0.18). Weevils were absent
on 55 % of the controls (N = 20) whereas they were
missing on only 33 % of ant-excluded inflorescences
(N = 18), but the difference between the frequencies
was not significant (Chi square test of independence,
v2 = 1.82, N = 38, 1 df, p = 0.18).
Fruit set among the four treatments of the exclusion
experiments was significantly different (Fig. 2; Krus-
kal–Wallis: v2 = 36.06, df = 3, p \ 0.001). Weevils
were detrimental to fruit set. Average fruit set of
control plants (ant and weevil access) was 14.5 %
(±4.5) and for ant exclusion it dropped to 9.7 %
(±4.7) yet the difference between medians of the two
groups was not significant (Pairwise Wilcoxon test
with Bonferroni-Holm correction; p = 0.85). While
the abundance of ants on control inflorescences was
significantly correlated with fruit set (Spearman’s rank
correlation, rs = 0.82, p \ 0.001) the number of
weevils per flower was not (rs = 0.10, p = 0.69).
Average fruit set for the weevil exclusion and total
exclusion treatments were statistically similar
(56.3 % ± 5.0 and 57.5 % ± 5.4, respectively;
p = 0.85), and gave significantly higher results than
the treatments that allowed weevil access: (Pairwise
Wilcoxon tests with Bonferroni-Holm correction; all
four comparisons: p \ 0.001).
Analyses of data from the 2 9 2 plots corroborated
the strong relationship between the presence of ants
and plant reproductive success. The mean number of
ants per inflorescence per plot was strongly correlated
with fruit set per inflorescence per plot (Fig. 3;
Pearson’s r = 0.95; r2 = 0.90 ANOVA F1,13 =
123.7, p \ 0.001). However, there was no relationship
between the mean number of ants/inflorescence/plot
and the mean number of weevils/inflorescence/plot
(linear regression: r2 = 0.008, ANOVA F1,13 = 0.011,
p = 0.75). We also found no relationship between the
Fig. 2 Percent fruit set among treatments of the exclusion
experiment. Control plants allowed access to both weevils and
ants. Treatment groups indicated by a different letter are
significantly different
Fig. 3 Significant relationship between abundance of ants
(Solenopsis invicta) on inflorescences and reproductive success
as expressed by percent fruit set in Spathoglottis plicata. Circles
and solid line indicate the mean % fundamental fruit set per
inflorescence/plot and the regression line respectively, and
triangles and broken line indicate the mean % realized fruit set
per inflorescence/plot and the regression line respectively
Biotic resistance and invasional meltdown
123
Author's personal copy
mean number of weevils per inflorescence and percent
fruit set in the 2 9 2 plots (r2 = 0.003, ANOVA
F1,13 = 0.041, p = 0.84). At the end of the monitor-
ing period, 55 % (SD = 0.18) of the inflorescences
per plot had damaged/destroyed apical meristems
(Table 1).
Our GLMM analyses indicated that the number of
ants was the most likely factor that significantly
explained variation in fruit set and fruit survivorship.
All three models (complex, intermediate, simple) gave
the same results. While AIC values were very similar
among the models for ‘‘Fundamental Fruit Set’’, they
favored the simplest model for ‘‘Fruit Survival’’ and
‘‘Realized Fruit Set’’. Consequently, we use the
simplest model but provide GLMM results for all
three models in supplemental material (Table 1,
supplemental material).
Ant: weevil interactions
Behavioral observations of weevils on ant-free inflo-
rescences versus ant-occupied inflorescences revealed
that the mean proportion of time spent on active
behavior was lower on inflorescences with ants (0.36,
SD = 0.41) than those inflorescences without them
(0.70, SD = 0.33). Comparison of the medians
revealed that this difference between groups was
significant (Mann–Whitney U-test, W = 672,
p = 0.002). Again, the mean number of weevils per
inflorescence was similar when ants were either
present (2.10, SD = 0.94) or absent (2.34,
SD = 1.18), and comparison of the medians con-
firmed that the groups were not significantly different
(Mann–Whitney U-test, W = 503.5, p = 0.557).
Moreover, the fitted GLMM that best explained the
proportion of time weevils were active included only
the presence of ants (Table 2). Neither the mean
number of ants nor the mean number of weevils
significantly impacted weevil behavior.
Density effects
The relationship between Spathoglottis densities and
weevil abundance and flower damage were highly
variable. Average NN distances ranged from 0.3 to
8.0 m and were skewed to the right. The average NN
distance was 2.0 m and the median was 1.6 m. We
found a negative relationship between Spathoglottis
flower densities and the number of adult weevils per
flower on target plants (Kendall’s tau b = - 0.12,
p = 0.03). Although the slope of the regression line
was significantly different from zero (F1,172 = 5.95,
p = 0.02), the model explained only 3 % of the
variation. However, there was no relationship between
flower damage score and densities of Spathoglottis
flowers (Kendall’s tau b = 0.05, p = 0.32; linear
regression r2 = 0.01, F1,195 = 0.28, p = 0.60).
In contrast to the NN analysis, we found a positive
relationship between the number of open Spathoglottis
flowers in the 2 9 2 m plots and the number of weevils
we observed per inflorescence (Kendall’s tau
b = 0.437, p \ 0.001). Again, considerable variation
existed (r2 = 0.10), but the slope of the linear regression
was significantly different from zero (F1,106 = 11.78,
p \ 0.001). There was also a significant relationship
between damaged flowers and the abundance of
Table 1 Factors that influence reproductive success of Spathoglottis plicata
Response N Parameter Estimate SE z p
Fundamental fruit set 129 Intercept -2.50 0.17 -14.23 \0.001
Ants 0.15 0.27 5.52 \0.001
Fruit survival 91 Intercept -3.55 0.23 -15.10 \0.001
Ants 0.19 0.03 6.31 \0.001
Realized fruit set 129 Intercept -4.33 0.25 -17.05 \0.001
Ants 0.25 0.04 6.88 \0.001
Estimated parameters, fit statistics are based on Generalized Linear Mixed Models. The more complex models that included the
number of weevils and ant-weevil interactions were either non significant or were deemed weaker by AIC and BIC calculations
(Table 1S). ‘‘Fundamental fruit set’’ is the proportion of flowers (fruits ? scars) that become fruits; ‘‘Fruit survival’’ is the proportion
of fruits that survive without weevil damage (oviposition by weevils); and ‘‘Realized fruit set’’ is the proportion of flowers that
become fruits and escape oviposition by weevils. Plots (n = 15) and flower color were specified as the source of random variation in
the analyses
J. D. Ackerman et al.
123
Author's personal copy
Spathoglottis flowers within the plots. The non-para-
metric correlation was highly significant (Kendall’s
tau = 0.71, p \ 0.001) as was the slope of the regres-
sion (r2 = 0.47; F1,124 = 108.9, p \ 0.001). Thus, both
weevil abundance and flower damage were associated
with flower density but only on this small scale.
Discussion
Positive interactions that plant species acquire at novel
locations can facilitate establishment, naturalization
and further range expansion (Simberloff and Von
Holle 1999; Richardson et al. 2000), whether they
involve mycorrhizal associations, seed dispersers or
pollinators (Briscoe 1959; Munoz and Ackerman
2011; Ackerman 2012). And when the positive
interactions are among non-indigenous species, inva-
sional meltdown may ensue (Simberloff and Von
Holle 1999). On the other hand, interactions that result
in negative effects on the demography of new arrivals
are the basis for the biotic resistance hypothesis (Elton
1958) and numerous studies have described them, but
it is not often any particular interaction alone under-
mines the establishment and expansion of new arrivals
(Levine et al. 2004; Lockwood et al. 2007).
Spathoglottis plicata acquired several interactions
in its establishment and march across the island of
Puerto Rico. We know it has been able to exploit
components of the island’s existing fungal diversity
because range expansion outside gardens is through
seed dispersal and orchid germination success is
dependent on exploiting mycorrhizal fungi.
The second interaction acquired is the negative one:
the native orchid weevil attack on flowers and fruits.
Adult weevils not only consumed parts of the perianth,
but females lay eggs in fruits where larvae feed on
developing seed. The wounds caused by weevils often
led to secondary fungal or bacterial infections, which
often destroyed the apical meristem and even the entire
inflorescence. Our field observations suggest that flower
densities play a role in attracting weevils, but only at a
very local scale (within about 2 m), a phenomenon that
is also maintained when other orchid species are
involved (Recart et al. 2013). Weevil abundance is
important as we revealed significant correlations
between the number of weevils observed on an inflo-
rescence and the severity of floral (perianth) damage,
which was comparable to the level of beetle damage
seen in orchids of the Neotropics and Asia (Rico-Gray
and Thien 1989; Subedi et al. 2011). Furthermore, field
experiments demonstrated that fruit production dropped
as much as 83 % when weevils were present. The impact
might have been even greater if our orchid populations
were pollinator-dependent since florivory can influence
pollinator visitation rates (Krupnick and Weis 1999;
Spaethe et al. 2007; but see Cuartas-Domınguez and
Medel 2010), as likely occurs with the sympatric native
orchid, Bletia patula Graham, which suffers increased
weevil florivory and reduced reproductive success in the
presence of S. plicata (Recart et al. 2013).
Spathoglottis plicata in its native habitat presum-
ably benefits from their EFN, perhaps in defense
against orchid specialist weevils (Orchidophilus spp.;
Prena 2008). Throughout Puerto Rico, EFN of Spatho-
glottis attract ants, but during our field observations we
Table 2 Effects of invasive fire ants (Solenopsis invicta) on the behavior of the native orchid weevil (Stethobaris polita) on
inflorescences of the invasive orchid Spathoglottis plicata
Parameter Model A Model B Model C
Est. SE z p D Est. SE z p D Est. SE z p
Intercept 2.315 1.483 1.56 0.119 2.228 1.45 1.54 0.125 2.448 0.700 3.18 \0.001
Attendance -4.298 1.693 -2.54 0.011 -3.94 1.13 -3.49 \0.001 – – – –
Ants 0.068 0.246 0.28 0.781 – – – – -3.972 1.120 -3.55 \0.001
Weevils 0.056 0.537 0.10 0.917 0.09 0.521 0.18 0.859 – – – –
Deviance 204 204.1 204.1
AIC 218 1.9 216.1 2.0 214.1
Response variable is the proportion of time weevils were engaged in active behaviors (eating, copulating, wandering). Estimated
parameters, fit statistics, and comparison of different models using Generalized Linear Mixed Models. ‘‘Attendance’’ indicates the
presence or absence of ants, ‘‘Ants’’ indicate the number of ants and ‘‘Weevils’’ indicate the number of weevils. Flower color and
sampling period were specified as sources of random variation in the analyses
Biotic resistance and invasional meltdown
123
Author's personal copy
noted ants ignoring beetles and at other times ants
would attack them. This is not surprising given that
foraging activities of ants, and thus ant-plant interac-
tions, are constrained by ant behavior, temperature,
water stress, spatial distribution of resources, colony
size, stage, and nutritional requirements, host plant
attributes, and the behavior of other organisms in the
system (Carroll and Janzen 1973; Traniello 1989; Lach
2003, and references therein).
Although the dominant ants on EFN at our study
sites were invasive fire ants (Solenopsis invicta), other
species were evident as is typical of plants with EFN
(Oliveira and Brandao 1991 cited by Ness et al. 2006).
In fact, Jaffe et al. (1989) observed four different ant
species at EFNs of Spathoglottis in naturalized
populations on Caribbean island of Guadeloupe. The
dominant species was Ectatomma ruidum (Ponerinae),
which were twice seen carrying lepidopteran larvae
from inflorescences. Fire ants were not among those
that they reported.
In Puerto Rico, nearly all of the aggressive inter-
actions toward weevils were by the fire ant, which
were not effective at reducing weevil presence, but
they did alter weevil behavior, by harassment and the
‘‘scarecrow effect’’, resulting in a reduction in the time
they spent damaging flowers and fruits, as occurs in
other systems (Janzen 1966; Carroll and Janzen 1973;
Freitas and Oliviera 1996; Holway et al. 2002 and
references therein; Lach 2003). This, in turn, affected
fruit set and survival. Unlike the Catalpa-Solenopsis
system (Ness 2003) where red fire ants do not forage
from EFNs but rather prey upon animals found on the
plant, the invasive ants on S. plicata consume and
likely benefit from the extrafloral nectar resulting in a
facultative food-for-protection mutualism (Koptur
1992). Another factor that may be acting to reduce
damage by weevils to inflorescences, and that we did
not take into account in this study is egg and larval
predation by red fire ants. On two occasions, the fire
ants were observed entering damaged fruits through
exit holes, and coming out with weevil larvae, but
were never seen carrying adult weevils (fruits may
have from 1 to several larvae in different develop-
mental stages; WF pers. obs.). In other systems,
S. invicta is known to feed on eggs, larvae, and pupae
of damaging herbivores (e.g., McDaniel and Sterling
1979, 1982; Jaffe et al. 1989; Taber 2000; Ness 2003).
Spathoglottis may have left its native enemies
behind, but it encountered new ones where it has
colonized in Puerto Rico. The acquisition of enemies
by Spathoglottis likely has affected the demographic
dynamics in Puerto Rico, since the orchid weevils
reduce fruit set and much variation in orchid seedling
establishment is a consequence of seed limitation
(Ackerman et al. 1996). This biotic resistance, how-
ever, is weakened by the invasive, novel ant-plant
interaction. The orchid’s continuing spread across the
island probably also benefited by seed production of
plants at peripheral, low-density populations where
weevil damage is not so severe.
Besides factors discussed above, at least three other
factors have likely facilitated the Spathoglottis inva-
sion. First, these plants usually occupy highly dis-
turbed sites (landslides, roadsides, etc.), which may
foster non-equilibrium co-existence and where com-
petitive interactions may be insignificant. Secondly,
like most orchids, the fruits of Spathoglottis contain
thousands of minute dust-like, wind-dispersed seed.
Propagule production is enormous in this self-polli-
nating orchid, which may overcome any constraints
imposed by the weevils. In some systems, propagule
pressure can be the most important factor in whether a
species becomes invasive or not (e.g., Von Holle and
Simberloff 2005; Richardson and Pysek 2006). Third,
humans occasionally dig up plants seen along road-
sides and take them home and from there they may
spread seed locally, establishing additional popula-
tions, accelerating invasional spread (Reichard and
White 2001).
Availability of carbohydrates can have very
positive effects on population growth in invasive ants
(Davidson 1997, 1998; Savage et al. 2009, 2011), and
invasive ants can facilitate the invasion of EFN-
bearing plant species (Koptur 1979; Hoffmann et al.
1999; Lach et al. 2010). Although we did not assess the
effects of the availability of EFNs on fitness of the
invasive fire ants, the results of this study, and those of
Recart et al. (2013), suggest that the invasive ants and
the invasive orchids are acting synergistically, causing
an invasional meltdown in the system. When sufficient
numbers of invasive ants visit inflorescences of the
invasive orchids, weevil damage to fruits is reduced,
and presumably seed production is increased. This
may in turn result in a higher recruitment rate for the
invasive orchids, which would mean more resources
for both invasive ants (resulting in positive feedbacks
between invasive species) and native beetles. Conse-
quently, native orchids may suffer spillover effects
J. D. Ackerman et al.
123
Author's personal copy
from elevated beetle numbers. Indeed, the pollinator-
dependent Bletia patula, which coexists with Spatho-
glottis plicata and does not possess EFNs, suffers from
apparent competition mediated by the native weevils,
resulting in a significantly lower reproductive output
(Recart et al. 2013). Whether the interactions between
the invasive orchids and ants amplify the impacts of
apparent competition between the orchid species is
unknown and merits further research.
We discovered that the invasive Spathoglottis
plicata has acquired at least two interspecific interac-
tions in Puerto Rico besides the mycorrhizae fungi that
are essential for seedling establishment: native weevils
attack the flowers and fruits reducing reproductive
output; and invasive fire ants forage at EFN and affect
weevil behavior, reducing fruit loss and thereby ame-
liorating the severity of weevil attack consistent with
invasional meltdowns. Whereas native herbivores gen-
erally provide some biotic resistance to plant invasions
(Parker et al. 2006), the acquisition of a specialist
enemy by Spathoglottis plicata did generate significant
losses particularly when ant abundances were low, yet
did not alter its colonizing behavior as might be
expected (Verhoeven et al. 2009). By specializing on
disturbed habitats, having ant-tended EFN and produc-
ing copious quantities of seed, biotic resistance to
Spathoglottis plicata invasion is apparently minimal.
Acknowledgments We thank Marilyn Light for insights on
Stethobaris and related taxa; Gabriel Maldonado, Camilo Fagua
and Alvaro Bravo for field assistance; Wilnelia Recart and
anonymous reviewers for critiques; and Raymond Tremblay and
Dennis Hansen for statistical advice. Financial and logistical
support was provided by the Department of Biology and the
Center for Applied Tropical Ecology and Conservation,
University of Puerto Rico, and the following grants from the
National Science Foundation (USA): Undergraduate Mentoring
in Environmental Biology (DBI 0602642, Alonso Ramırez, PI),
Centers for Research in Engineering, Science and Technology
(HRD-074826, Elvira Cuevas, PD) and Louis Stokes Alliance
for Minority Participation (HRD-0601843, Manuel Gomez and
Ana-Rita Mayol, co-PIs).
References
Ackerman JD (1983) On the evidence for a primitively epiphytic
habit in orchids. Syst Bot 8:474–477
Ackerman JD (1995) An orchid flora of Puerto Rico and the
Virgin Islands. Mem New York Bot Gard 73:1–203
Ackerman JD (2007) Invasive orchids: weeds we hate to love?
Lankesteriana 7:19–21
Ackerman JD (2012) Orchids gone wild: discovering natural-
ized orchids in Hawai’i. Orchids 81:88–93
Ackerman JD, Sabat AM, Zimmerman JK (1996) Seedling
establishment in an epiphytic orchid: an experimental
study of seed limitation. Oecologia 106:192–198
Bonnardeaux Y, Brundrett M, Batty A, Dixon K, Koch J, Siv-
asithamparam K (2007) Diversity of mycorrhizal fungi of
terrestrial orchids: compatibility web, brief encounters,
lasting relationships and alien invasions. Mycol Res
111:51–61
Briscoe CB (1959) Early results of mycorrhizal inoculation of
pine in Puerto Rico. Caribb Forester 20(3/4):73–77
Buren WF (1982) Red imported fire ant now in Puerto Rico.
Florida Entomol 65:188–189
Cameron DD, Leake JR, Read DJ (2006) Mutualistic mycor-
rhiza in orchids: evidence from plant-fungus carbon and
nitrogen transfers in the green = leaved terrestrial orchid
Goodyera repens. New Phytol 171:405–416
Cameron DD, Johnson I, Read DJ, Leake JR (2008) Giving and
receiving: measuring the carbon cost of mycorrhizas in the
green orchid, Goodyera repens. New Phytol 180:176–184
Carroll CR, Janzen DH (1973) Ecology of foraging by ants. Ann
Rev Ecol Syst 4:231–257
Catling PM (1990) Autopollination in the Orchidaceae. In:
Arditti J (ed) Orchid biology: reviews and perspectives V.
Timber Press, Portland, pp 121–158
Chun YJ, van Kleunen M, Dawson W (2010) The role of enemy
release, tolerance and resistance in plant invasions: linking
damage to performance. Ecol Lett 13:937–946
Cuartas-Domınguez M, Medel R (2010) Pollinator-mediated
selection and experimental manipulation of the flower
phenotype in Chloraea bletioides. Funct Ecol 24:1219–1227
Daehler CC (1998) The taxonomic distribution of invasive
angiosperm plants: ecological insights and comparison to
agricultural weeds. Biol Conserv 84:167–180
Damon A, Perez-Soriano MA (2005) Interaction between ants
and orchids in the Soconusco region, Chiapas, Mexico.
Entomotropica 20:59–65
Davidson DW (1997) The role of resource imbalances in the
evolutionary ecology of tropical arboreal ants. Biol J Linn
Soc 61:153–181
Davidson DW (1998) Resource discovery versus resource
domination in ants: a functional mechanism for breaking
the trade-off. Ecol Entomol 23:484–490
Davis LR Jr, Vander Meer RK, Porter SD (2001) Red imported
fire ants expand their range across the West Indies. Florida
Entomol 84:735–736
Elton CS (1958) The ecology of invasions by plants and animals.
Methuen, London
Ewel JJ, Whitmore TN (1973) The ecological life zones of
Puerto Rico and the U.S. Virgin Islands. Forest service
research paper ITF-18, Institute of Tropical Forestry,
Forest Service, U.S. Department of Agriculture
Fisher BL, Zimmerman JK (1988) Ant/orchid associations in the
Barro Colorado National Monument, Panama. Lindleyana
3:1–16
Freitas AVL, Oliviera PS (1996) Ants as selective agents on
herbivore biology: effects on the behavior a non-myrme-
cophilous butterfly. J Anim Ecol 65:205–210
Gowland KM, van der Merwe MM, Linde CC, Clements MA,
Nicotra AB (2013) Host bias of three epiphytic Aeridinae
Biotic resistance and invasional meltdown
123
Author's personal copy
orchid species is reflected, but not explained, by mycor-
rhizal fungal associations. Am J Bot 100:764–777
Hara AH, Mau RFL (1986) The orchid weevil, Orchidophilus
aterrimus (Waterhouse): insecticidal control and effect on
Vanda orchid production. Proc Hawaiian Entomol Soc
26:71–75
Hoffmann BD, Andersen AN, Hill GJE (1999) Impact of an
introduced ant on native forest invertebrates: Pheidole
megacephala in monsoonal Australia. Oecologia
120:595–604
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002)
The causes and consequences of ant invasions. Ann Rev
Ecol Syst 33:181–233
IUCN/SSC Orchid Specialist Group (1996) Orchids: status
survey and conservation action plan. IUCN, Gland and
Cambridge
Jaffe K, Pavis C, Vansuyt G, Kermarrec A (1989) Ants visit
extrafloral nectaries of the orchid Spathoglotis [sic] plicata
Blume. Biotropica 21:278–279
Janzen DH (1966) Coevolution of mutualism between ants and
acacias in Central America. Evolution 20:249–275
Jolliffe K (2010) Epiphytic orchids of the Seychelles. Kapisen
10:6–8
Keane RM, Crawley MJ (2002) Exotic plant invasions and the
enemy-release hypothesis. Trends Ecol Evol 17:164–170
Koptur S (1979) Facultative mutualism between weedy vetches
bearing extrafloral nectaries and weedy ants in California.
Am J Bot 66:1016–1020
Koptur S (1992) Extrafloral nectar-mediated interactions
between insects and plants. In: Bernays E (ed) Insect/plant
interactions, vol 4. CRC Press, Boca Raton, pp 85–132
Krupnick GA, Weis AE (1999) The effect of floral herbivory on
male and female reproductive success in Isomeris arborea.
Ecology 80:135–149
Kueffer C, Daehler CC, Torres-Santana CW, Lavergne C,
Meyer J-Y, Otto R, Silva L (2010) A global comparison of
plant invasions on oceanic islands. Perspect Plant Ecol
Evol Syst 12:145–161
Lach L (2003) Invasive ants: unwanted partners in ant-plant
interactions? Ann Missouri Bot Gard 90:91–108
Lach L, Tillberg CV, Suarez AV (2010) Contrasting effects of
an invasive ant on a native and an invasive plant. Biol
Invasion 12:3123–3133
Levine JM, Adler PB, Yelenik SG (2004) A meta-analysis of
biotic resistance to exotic plant invasions. Ecol Lett
7:975–989
Liu H, Pemberton R (2010) Pollination of an invasive orchid,
Cyrtopodium polyphyllum (Orchidaceae), by an invasive
oil-collecting bee, Centris nitida, in southern Florida.
Botany 88:290–295
Liu H, Stiling P (2006) The enemy release hypothesis: a review
and meta-analysis. Biol Invasion 8:1535–1545
Lockwood JL, Hoopes HF, Marchetti MP (2007) Invasion
ecology, 2nd edn. Blackwell Publishing, London
Louda SM, Potvin MA (1995) Effect of inflorescence-feeding
insects on the demography and lifetime fitness of a native
plant. Ecology 76:229–245
McCormick MK, Whigham DF, Sloan D, O’Malley K, Hod-
kinson B (2006) Orchid-fungus fidelity: a marriage meant
to last? Ecology 87:903–911
McDaniel SG, Sterling WL (1979) Predator determination and
efficiency on Heliothis virescens eggs on cotton using 32P.
Environ Entomol 8:1083–1087
McDaniel SG, Sterling WL (1982) Predation of Heliothis vi-
rescens (F.) eggs on cotton in east Texas. Environ Entomol
11:60–66
Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA,
Klironomos JN, Maron JL, Morris WF, Parker IM, Power
AG, Seabloom EW, Torchin ME, Vazquez DP (2006)
Biotic interactions and plant invasions. Ecol Lett
9:726–740
Munoz MC, Ackerman JD (2011) Spatial distribution and per-
formance of native and invasive Ardisia (Myrsinaceae)
species in Puerto Rico: the anatomy of an invasion. Biol
Invasion 13:1543–1558
Ness JH (2003) Contrasting exotic Solenopsis invicta and native
Forelius pruinosus ants as mutualists with Catalpa big-
nonioides, a native plant. Ecol Entomol 28:247–251
Ness JH, Morris WF, Bronstein JL (2006) Integrating qualityand quantity of mutualistic service to contrast ant species
protecting Ferocactus wislizeni. Ecology 87:912–921
Nunez MA, Horton TR, Simberloff D (2009) Lack of below-
ground mutualisms hinders Pinaceae invasions. Ecology
90:2352–2359
O’Brien CW, Turnbow RH Jr (2011) An annotated list of
Curculionidae (Coleoptera) of Dominica (excluding
Scolytinae and Platypodidae). Insecta Mundi 0179:1–31
O’Dowd DJ, Green PT, Lake PS (2003) Invasional ‘meltdown’
on an oceanic island. Ecol Lett 6:812–817
Ogura-Tsujita Y, Yukawa T (2008) High mycorrhizal specific-
ity in a widespread mycoheterotrophic plant, Eulophia
zollingeri (Orchidaceae). Am J Bot 95:93–97
Oliveira PS, Brandao CRF (1991) The ant community associ-
ated with extrafloral nectaries in the Brazilian cerrados. In:
Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford
University Press, Oxford, pp 198–212
Otero JT, Ackerman JD, Bayman P (2002) Diversity and host
specificity of mycorrhizal fungi from tropical orchids. Am
J Bot 89:1852–1858
Otero JT, Ackerman JD, Bayman P (2004) Differences
in mycorrhizal specificity between two tropical orchids.
Mol Ecol 13:2393–2404
Parker D, Burkepile DE, Hay ME (2006) Opposing effects of
native and exotic herbivores on plant invasions. Science
301:1459–1461
Partomihardjo T (2003) Colonisation of orchids on the Krakatau
islands. Telopea 10:299–310
Pauw A, Bond WJ (2011) Mutualisms matter: pollination rate
limits the distribution of oil-secreting orchids. Oikos
120:1531–1538
Prena J (2008) A synopsis of the orchid weevil genus Orchi-
dophilus Buchanan (Curculionidae, Baridinae), with tax-
onomic rectifications and description of one new species.
Zootaxa 1783:18–30
Prider JN, Facelli JM, Watling JR (2010) Multispecies inter-
actions among a plant parasite, a pollinator, and a seed
predator affect the reproductive output of an invasive plant,
Cytisus scoparius. Austral Ecol 36:167–175
Rasmussen HN (1995) Terrestrial orchids from seed to myco-
trophic plant. Cambridge University Press, Cambridge
J. D. Ackerman et al.
123
Author's personal copy
Recart W, Ackerman JD, Cuevas AA (2013) There goes the
neighborhood: apparent competition between native and
invasive orchids mediated by a specialist florivorous
weevil. Biol Invasions 15:283–293
Reichard SH, White P (2001) Horticulture as a pathway of
invasive plant introductions in the United States. Biosci-
ence 51:103–113
Richardson DM, Pysek P (2006) Plant invasions: merging the
concepts of species invasiveness and community invisi-
bility. Prog Phys Geogr 30:409–431
Richardson DM, Allsopp N, D’Antonio CM, Milton SJ,
Rejmanek M (2000) Plant invasions: the role of mutual-
isms. Biol Rev 75:65–93
Rico-Gray V, Thien LB (1989) Effect of different ant species on
reproductive fitness of Schomburgkia tibicinis (Orchida-
ceae). Oecologia 81:487–489
Rico-Gray V, Thien LB (2007) The ecology and evolution of
ant-plant interactions. Chicago University Press, Chicago
Savage A, Rudgers JA, Whitney KD (2009) Elevated domi-
nance of extrafloral nectary-bearing plants is associated
with increased abundances of an invasive ant and reduced
native ant richness. Divers Distrib 15:751–761
Savage AM, Johnson SD, Whitney KD, Rudgers JA (2011)
Do invasive ants respond more strongly to carbohydrate
availability than co-occurring non-invasive ants? A test
along an active Anoplolepis gracilipes invasion front.
Austral Ecol 36:310–319
Schemske DW (1982) Ecological correlates of a Neotropical
mutualism: ant assemblages at Costus extrafloral nectaries.
Ecology 63:932–941
Simberloff D (2011) How common are invasion-induced eco-
system impacts? Biol Invasions 13:1255–1268
Simberloff D, Von Holle B (1999) Positive interactions of
nonindigenous species: invasional meltdown? Biol Inva-
sion 1:21–32
Spaethe J, Moser WH, Paulus HF (2007) Increase of pollination
attraction by means of visual signal in the sexually
deceptive orchids, Ophrys heldreichii (Orchidaceae). Plant
Syst Evol 264:31–40
Subedi A, Chaudhary RP, Van Achterberg C, Heijerman T, Lens
F, Van Dooren TJM, Gravendeel B (2011) Pollination and
protection against herbivory of Nepalese Coelogyninae
(Orchidaceae). Am J Bot 98:1095–1103
Swarts ND, Sinclair EA, Francis A, Dixon KW (2010) Eco-
logical specialization in mycorrhizal symbiosis leads to
rarity in an endangered orchid. Mol Ecol 19:3226–3242
Swezey OH (1945) Insects associated with orchids. Proc
Hawaiian Entomol Soc 12:343–403
Taber SW (2000) Fire ants. Texas A&M University Press,
College Station
Traniello JFA (1989) Foraging strategies of ants. Ann Rev
Entomol 34:191–210
Tremblay RL (1992) Trends in the pollination ecology of the
Orchidaceae: evolution and systematics. Can J Bot
70:642–650
Tremblay RL, Melendez-Ackerman EJ, Kapan D (2006) Do
orchids behave as metapopulations? Evidence from colo-
nization, extinction rates and asynchronous population
dynamics. Biol Conserv 129:70–81
Verhoeven KJF, Biere A, Harvey JA, van der Putten WH (2009)
Plant invaders and their novel natural enemies: who is
naıve? Ecol Lett 12:107–117
Von Holle B, Simberloff D (2005) Ecological resistance to
biological invasion overwhelmed by propagule pressure.
Ecology 86:3212–3218
Waterman RJ, Bidartondo MI (2008) Deception above, decep-
tion below: linking pollination and mycorrhizal biology of
orchids. J Exp Bot 59:1085–1096
Williams PA, Karl BJ (1996) Fleshy fruits of indigenous and
adventive plants in the diet of birds in forest remnants,
Nelson, New Zealand. New Zealand J Ecol 20:127–145
Wolcott GN (1948) The insects of Puerto Rico, Coleoptera.
J Agric Univ Puerto Rico 32:225–416
Biotic resistance and invasional meltdown
123
Author's personal copy
Top Related