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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

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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: ackerman.upr@gmail.com

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

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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.

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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

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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.

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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

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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

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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

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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.

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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

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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.

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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

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